Book - Outline of Comparative Embryology: Difference between revisions

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|| [[file:Mark_Hill.jpg|90px|left]] This historic 1931 embryology textbook by Richards was designed as an introduction to the topic. Currently only the text has been made available online, figures will be added at a later date.  My thanks to the Internet Archive for making the original scanned book available.
| [[File:Mark_Hill.jpg|90px|left]] This historic 1931 embryology textbook by Richards was designed as an introduction to the topic. Currently only the text has been made available online, figures will be added at a later date.  My thanks to the Internet Archive for making the original scanned book available.
{{History Links}}
{{History Links}}


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==Preface==
==Preface==


As the result of a number of years of experience in introducing stu-
As the result of a number of years of experience in introducing students to the subject of embryology, the writer has found it desirable
dents to the subject of embryology, the writer has found it desirable
to ‘depart from the common practice of studying chiefly the special
to ‘depart from the common practice of studying chiefly the special
embryology of the chick, pig, and perhaps of amphioxus and the frog,
embryology of the chick, pig, and perhaps of amphioxus and the frog,
and to devote much attention to the principles of general embryology.
and to devote much attention to the principles of general embryology.
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of general knowledge forms a desirable starting point for the study of
of general knowledge forms a desirable starting point for the study of
special embryology to be taken up later. As comparative anatomy has
special embryology to be taken up later. As comparative anatomy has
proven to be the best basis for the later study of anatomy, so compara-
proven to be the best basis for the later study of anatomy, so comparative embryology forms a proper basis for a study of special embryology.
tive embryology forms a proper basis for a study of special embryology.
Unfortunately there has been no book in our language which brings
Unfortunately there has been no book in our language which brings
together in a small compass the principles of general comparative
together in a small compass the principles of general comparative
embryology.
embryology.


In this book it is the aim to set up the general principles of develop-
In this book it is the aim to set up the general principles of development so that the student may see how his special case—chick, starfish,
ment so that the student may see how his special case—chick, starfish,
or other form—is merely one of several types and what its relation to
or other form—is merely one of several types and what its relation to
the other types may be. The writer holds that the most effective pre-
the other types may be. The writer holds that the most effective presentation of the subject matter of embryology is the laboratory study of
sentation of the subject matter of embryology is the laboratory study of
desirable types, supported by text-book and “quiz” work on these forms
desirable types, supported by text-book and “quiz” work on these forms
and accompanied by the consideration from a comparative standpoint
and accompanied by the consideration from a comparative standpoint
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In Part One are taken up those phases of development which are
In Part One are taken up those phases of development which are
passed through in the embryology of most higher forms of animals.
passed through in the embryology of most higher forms of animals.
A comparative study of these phases no doubt forms the basis of nine-
A comparative study of these phases no doubt forms the basis of ninetenths of the courses in this subject. Of the vast amount of material
tenths of the courses in this subject. Of the vast amount of material
from which choice must be made, the decision as to whether any certain
from which choice must be made, the decision as to whether any certain
topic should be discussed has been based always upon a single criterion.
topic should be discussed has been based always upon a single criterion.
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to follow through for these forms the later stages in their development
to follow through for these forms the later stages in their development
and differentiation. If completeness were the goal, it would be necessary
and differentiation. If completeness were the goal, it would be necessary
to include the special embryology of the many forms about which investi-
to include the special embryology of the many forms about which investigators would desire information, an obviously impossible task. It is
gators would desire information, an obviously impossible task. It is
hoped, however, that a basis is here laid for understanding the detailed
hoped, however, that a basis is here laid for understanding the detailed
embryology of any of the types and for working out later stages in
embryology of any of the types and for working out later stages in
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easily available. Discussions of many of them are not available in brief
easily available. Discussions of many of them are not available in brief
form in any English text, although they concern matters about which
form in any English text, although they concern matters about which
students of zoology should be informed, for they are chiefly problems of
students of zoology should be informed, for they are chiefly problems of
normal development.
normal development.


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only by chemists or physicists in years gone by are now every-day tools
only by chemists or physicists in years gone by are now every-day tools
of the embryologists, for descriptive embryology alone is inadequate to
of the embryologists, for descriptive embryology alone is inadequate to
give a complete understanding of development. Yet experimental em-
give a complete understanding of development. Yet experimental embryology runs the danger of considering only processes and those out of
bryology runs the danger of considering only processes and those out of
relation to structures. It is in structures that functions are inherent,
relation to structures. It is in structures that functions are inherent,
for one cannot understand the workings of a machine with which he is
for one cannot understand the workings of a machine with which he is
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Undoubtedly numerous errors are to be found in this volume. Much
Undoubtedly numerous errors are to be found in this volume. Much
that is discussed has been the subject of life-long study by many investi-
that is discussed has been the subject of life-long study by many investigators and has concerned material collected from all over the world.
gators and has concerned material collected from all over the world.
To understand all adequately so that each may be mentioned correctly
To understand all adequately so that each may be mentioned correctly
and weighted properly in a brief outline, is a task hardly to be accomplished, and many inconsistencies of treatment must be apparent to the
and weighted properly in a brief outline, is a task hardly to be accomplished, and many inconsistencies of treatment must be apparent to the
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Acknowledgments are due for assistance in almost every section.
Acknowledgments are due for assistance in almost every section.
The material treated in a work of this kind is by no means new, and it
The material treated in a work of this kind is by no means new, and it
would be impossible to present any one phase of it without finding
would be impossible to present any one phase of it without finding
parallel treatment in some source of information available to students
parallel treatment in some source of information available to students
of embryology of this day. There is no claim to originality in the book,
of embryology of this day. There is no claim to originality in the book,
not even in the treatment of many chapters. The book will have served
not even in the treatment of many chapters. The book will have served
its purpose, however, if it appears to have sufficient pedagogical back-
its purpose, however, if it appears to have sufficient pedagogical background and if it presents in sufficiently compact form these principles,
ground and if it presents in sufficiently compact form these principles,
many of which I think are not briefly summarized elsewhere in the
many of which I think are not briefly summarized elsewhere in the
English language, and which are needed to give students a basis for work
English language, and which are needed to give students a basis for work
in special embryology,-either medicalor experimental.
in special embryology,-either medicalor experimental.
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Korschelt and Heider’s “Lehrbuch der vergleiehenden Entwicklungs—
Korschelt and Heider’s “Lehrbuch der vergleiehenden Entwicklungs—
geschichte” is a great treasure house of embryological learning to which
geschichte” is a great treasure house of embryological learning to which
constant reference has been made. In many places (particularly in Chap-
constant reference has been made. In many places (particularly in Chapters VII and VIII, Part One) even their arrangement has been so much
ters VII and VIII, Part One) even their arrangement has been so much
the best that only minor departures from it are to be found here. In
the best that only minor departures from it are to be found here. In
others an entirely different organization of the same material is here
others an entirely different organization of the same material is here
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Permission has been granted by the following publishers to make use
Permission has been granted by the following publishers to make use
of the figures indicated either as modified, or in the case of numbers
of the figures indicated either as modified, or in the case of numbers
1, 2, 3, 135, 136, 142, 153, 1-81 of the figures themselves. By Henry
1, 2, 3, 135, 136, 142, 153, 1-81 of the figures themselves. By Henry
Holt & Co. permission has been given to use from Loey’s “Biology and
Holt & Co. permission has been given to use from Loey’s “Biology and
Its Makers,” our figures 1, 2, and 3; to use from Kellicott’s “General
Its Makers,” our figures 1, 2, and 3; to use from Kellicott’s “General
Embryology” our figure 5; from Kellicott’s “Chordate Development”
Embryology” our figure 5; from Kellicott’s “Chordate Development”
our figures 135, 136, 142, 144, and 181; and from Lillie’s “Embryology
our figures 135, 136, 142, 144, and 181; and from Lillie’s “Embryology
of the Chick” our figures 151, 152. By P. Blakiston’s Son & Co., Inc.,
of the Chick” our figures 151, 152. By P. Blakiston’s Son & Co., Inc.,
permission has been given to use from Folsom’s “Entomology with
permission has been given to use from Folsom’s “Entomology with
Special Reference to Its Ecological Aspects,” 3rd edition, our figures
Special Reference to Its Ecological Aspects,” 3rd edition, our figures
117, 161, and 162; and from Patten’s “Embryology of the Pig,” figure 7. The Oxford University Press has permitted the use from Jenkinson’s
117, 161, and 162; and from Patten’s “Embryology of the Pig,” figure 7. The Oxford University Press has permitted the use from Jenkinson’s
“Vertebrate Embryology” of our figures 81 and 173. The Princeton
“Vertebrate Embryology” of our figures 81 and 173. The Princeton
University Press has granted permission to use from Conklin’s “ Heredity
University Press has granted permission to use from Conklin’s “ Heredity
and Environment” our figures 7 and 8. The U. S. Bureau of Fisheries
and Environment” our figures 7 and 8. The U. S. Bureau of fisheries
has given permission to use from Herrick’s “American Lobster” figures
has given permission to use from Herrick’s “American Lobster” figures
113, and 1973.. And William Wood & Co. have permitted the modifica-
113, and 1973.. And William Wood & Co. have permitted the modification of figures from Bailey and Miller’s “Textbook of Embryology”
tion of figures from Bailey and Miller’s “Textbook of Embryology”
represented in figures 140 and 141. Macmillan & Co., Ltd., has sold us
represented in figures 140 and 141. Macmillan & Co., Ltd., has sold us
permission to make use of our figures 103, 109, 110 from McBride’s
permission to make use of our figures 103, 109, 110 from McBride’s
“Textbook of Embryology, Vol. I, Invertebrate Embryology,” and of
“Textbook of Embryology, Vol. I, Invertebrate Embryology,” and of
our figures 167, 168, and 170 from Graham Kerr’s “Textbook of Em-
our figures 167, 168, and 170 from Graham Kerr’s “Textbook of Embryology, Vol. II, Vertebrate Embryology.” The graciousness of the
bryology, Vol. II, Vertebrate Embryology.” The graciousness of the
various publishing companies in thus facilitating our work is deeply
various publishing companies in thus facilitating our work is deeply
appreciated.
appreciated.
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wife, Mrs. Mildred Hoge Richards. My colleagues of the Department
wife, Mrs. Mildred Hoge Richards. My colleagues of the Department
of Zoology of the University of Oklahoma, Doctor A. O. Weese and
of Zoology of the University of Oklahoma, Doctor A. O. Weese and
Doctor A. I. Ortenburger have assisted with advice and have read por-
Doctor A. I. Ortenburger have assisted with advice and have read portions of the text. Professor J. F. Paxton of the Department of Greek
tions of the text. Professor J. F. Paxton of the Department of Greek
has aided me with questions of terminology. And finally my assistants
has aided me with questions of terminology. And finally my assistants
Mrs. Celeste Whaley Taft and Miss Kara J. Fullerton have given the
Mrs. Celeste Whaley Taft and Miss Kara J. Fullerton have given the
most painstaking attention to a multitude of details. To all of these
most painstaking attention to a multitude of details. To all of these
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but interest in and curiosity as to the events of the pre—natal period in
but interest in and curiosity as to the events of the pre—natal period in
animals or of the life and growth of an embryo, especially of the chick
animals or of the life and growth of an embryo, especially of the chick
before hatching, goes back to the ancients, as evidenced by the contribu-
before hatching, goes back to the ancients, as evidenced by the contributions by Aristotle and Galen among the Greeks. Aristotle was the author
tions by Aristotle and Galen among the Greeks. Aristotle was the author
of three works of great zoological importance, in one of which, “De
of three works of great zoological importance, in one of which, “De
Generatione Animalium,” are given the results of his observations on
Generatione Animalium,” are given the results of his observations on
Line 210: Line 195:
and of course were very incomplete. The advance of embryological
and of course were very incomplete. The advance of embryological
knowledge waited for the application of the lens to the study of life forms
knowledge waited for the application of the lens to the study of life forms
and processes which began seine four hundred years ago. With the inven-
and processes which began seine four hundred years ago. With the invention of the microscope the subject wen fresh impetus until it became one
tion of the microscope the subject wen fresh impetus until it became one
of the major biological sciences when supported by exact cell studies
of the major biological sciences when supported by exact cell studies
in the last century.
in the last century.
Line 224: Line 208:
de Generatione Animalium”) in which are recorded observations on the
de Generatione Animalium”) in which are recorded observations on the
development of the chick and some facts of mammalian embryology.
development of the chick and some facts of mammalian embryology.
He also discussed the nature of development and deduced from observa-
He also discussed the nature of development and deduced from observations the important principles that all animals come from ova and
tions the important principles that all animals come from ova and
that the development is a new formation, not more growth or enlargement. His study was made with simple lenses which did not enable him
that the development is a new formation, not more growth or enlarge-
ment. His study was made with simple lenses which did not enable him
to trace the genesis of the embryo from its earliest stages. Malpighi,
to trace the genesis of the embryo from its earliest stages. Malpighi,
who was more of a microscopist than Harvey, outranks him as an
who was more of a microscopist than Harvey, outranks him as an
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embryologist. His work on the development of the chick, published in
embryologist. His work on the development of the chick, published in
1672, shows Harvey’s influence, but by means of excellent descriptions
1672, shows Harvey’s influence, but by means of excellent descriptions


and many sketches carries the account of the development back to the
and many sketches carries the account of the development back to the
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Wolff, whose “Theoria Generationis” was first published in 1759. At
Wolff, whose “Theoria Generationis” was first published in 1759. At


that time embryology was dominated by the conception of pref0rma-
that time embryology was dominated by the conception of pref0rma
 
Fur. 1. William Harvey. (From Loey.)
Fur. 1. William Harvey. (From Loey.)


tion which had gradually grown up around the observations of Malpighi,
tion which had gradually grown up around the observations of Malpighi,
Leeuwenhoek, Boerhaave, and oth.'-rs. Although the point of view main-
Leeuwenhoek, Boerhaave, and oth.'-rs. Although the point of view maintained by Wolff, that of epigenesis, had also been that of Harvey and
tained by Wolff, that of epigenesis, had also been that of Harvey and
Aristotle, he is to be regarded as the first active proponent of that
Aristotle, he is to be regarded as the first active proponent of that
doctrine. He was opposed by the great physiologist, Haller, and by
doctrine. He was opposed by the great physiologist, Haller, and by
Bonnet, a very prolific writer on the subject. Led by these men, the
Bonnet, a very prolific writer on the subject. Led by these men, the
1)1-eforination-epigenesis controversy held the attention of embryologists
1)1-eforination-epigenesis controversy held the attention of embryologists
to the close of the eighteenth century.
to the close of the eighteenth century.
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of three layers in the early embryo from which the later organs are
of three layers in the early embryo from which the later organs are
developed. Obviously this is a conclusive argument against the old
developed. Obviously this is a conclusive argument against the old
preformation views. Von Bacr, however, is responsible for the germ-
preformation views. Von Bacr, however, is responsible for the germ
 
fiG. 2. K.ul Ernst um Bu-1 (Fmm Lot-\.l
FIG. 2. K.ul Ernst um Bu-1 (Fmm Lot-\.l


layer doctrine as a ;1(*m‘l.lllA2l,tl()n, and fun the (‘\])()~itiOn of the manner
layer doctrine as a ;1(*m‘l.lllA2l,tl()n, and fun the (‘\])()~itiOn of the manner
Line 272: Line 251:
discovered the egg in the ovary of mammals and of man and pointed
discovered the egg in the ovary of mammals and of man and pointed
out the similarity in the mode of origin of these animals to those lower
out the similarity in the mode of origin of these animals to those lower
in the scale. He was the first to recognize the notochord as occurring in
in the scale. He was the first to recognize the notochord as occurring in
all vertebrate animals and to point out the value of comparative embry-
all vertebrate animals and to point out the value of comparative embryology for anatomy and zoology. With von Baer the modern pmiml of
ology for anatomy and zoology. With von Baer the modern pmiml of
4 llIS'l‘Ol{l(‘\l. l)|l\ l,l.()l’.\IlCN'l‘ OI" EMl§RY()l.0GY
4 llIS'l‘Ol{l(‘\l. l)|l\ l,l.()l’.\IlCN'l‘ OI" EMl§RY()l.0GY


Line 281: Line 259:
is due to Fritz Miillcr in 1863. Von Baer called attention to the greater
is due to Fritz Miillcr in 1863. Von Baer called attention to the greater
similarity that exists between embryos of related groups than between
similarity that exists between embryos of related groups than between
adults. The younger the embryos the more alike are they. The recapitu-
adults. The younger the embryos the more alike are they. The recapitulation theory will be considered on a later page.
lation theory will be considered on a later page.


4. The period following von Baer is one of rich biological achievement.
4. The period following von Baer is one of rich biological achievement.
The discovery of the cell, nuclei, mitosis, the publication of the evolu-
The discovery of the cell, nuclei, mitosis, the publication of the evolution doctrine, the birth of histology and pathology, all wrought changes
tion doctrine, the birth of histology and pathology, all wrought changes
in the aspects of biology that necessarily had their influence on embry
in the aspects of biology that necessarily had their influence on embry-
 
   
   


FI(. C l \l llillnm (l“minl,m\)
fi(. C l \l llillnm (l“minl,m\)


ology. The facts of development were harmonized by the conception of
ology. The facts of development were harmonized by the conception of
evolution, and both comparative anatomy and paleontology threw light
evolution, and both comparative anatomy and paleontology threw light
on the reasons for some of the ()bs(‘u1'0 embryological phenomena dis-
on the reasons for some of the ()bs(‘u1'0 embryological phenomena discovered. This period saw established the relation of cells, tissues, and
covered. This period saw established the relation of cells, tissues, and
organs in the embryo, recognition of egg and sperm as cells, the process of
organs in the embryo, recognition of egg and sperm as cells, the process of
fertilization, many details in the development of both vertebrates and
fertilization, many details in the development of both vertebrates and
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5. The period of Balfour was one of exact morphological research.
5. The period of Balfour was one of exact morphological research.
Balfour was a young English embryologist (1851-1882) whose “Mono-
Balfour was a young English embryologist (1851-1882) whose “Monograph on the Development of Elasmobranch fishes” (1878), and whose
graph on the Development of Elasmobranch Fishes” (1878), and whose
“'l‘r<-alise on (‘mnp:11'ati\<- l3lml)ryology” (1880-1881), Won the highest
“'l‘r<-alise on (‘mnp:11'ati\<- l3lml)ryology” (1880-1881), Won the highest
EVENTS OF IMPORTANCE IN THE HISTORY OF EMBRYOLOGY 5
EVENTS OF IMPORTANCE IN THE HISTORY OF EMBRYOLOGY 5
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the science greatly enriched. The newer science of cytology is a direct
the science greatly enriched. The newer science of cytology is a direct
offshoot of the embryology of this period due to the pushing farther and
offshoot of the embryology of this period due to the pushing farther and
farther back of the questions on the origin of germ cells and the fertiliza-
farther back of the questions on the origin of germ cells and the fertilization and early development of the egg. One of the most notable advances
tion and early development of the egg. One of the most notable advances
of this period lay in the field of cell lineage. The investigations of the
of this period lay in the field of cell lineage. The investigations of the
eighties and nineties established for the eggs of many animals a complete
eighties and nineties established for the eggs of many animals a complete
history from the one-celled egg to the larval form with definite funda-
history from the one-celled egg to the larval form with definite fundaments of organs which later by specialization and elaboration make up
ments of organs which later by specialization and elaboration make up
the body of the adult. Thus is the organized character of the young
the body of the adult. Thus is the organized character of the young
embryo made clear even before the germ-layer stage. Thus also we know
embryo made clear even before the germ-layer stage. Thus also we know
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6. While much of a morphological character remains to be learned
6. While much of a morphological character remains to be learned
by embryologists of the future, it is not to be supposed that the nature
by embryologists of the future, it is not to be supposed that the nature
of the organic mechanism could be investigated only from that stand-
of the organic mechanism could be investigated only from that standpoint. With the increase of exact knowledge of the structure of the
point. With the increase of exact knowledge of the structure of the
organism, we demand information as to its method of operation. To the
organism, we demand information as to its method of operation. To the
developing animal must be applied not only the laws of physiology,
developing animal must be applied not only the laws of physiology,
with a correspondingly better understanding of the origin and develop-
with a correspondingly better understanding of the origin and development of these functions, but also the laws of physics and chemistry, and
ment of these functions, but also the laws of physics and chemistry, and
particularly physical chemistry must be appealed to. The study of
particularly physical chemistry must be appealed to. The study of
development in the light of these laws is the dominant note of the
development in the light of these laws is the dominant note of the
embryology of the present day, and as an experimental science it is
embryology of the present day, and as an experimental science it is
making remarkable strides forward. The present is the period of experi-
making remarkable strides forward. The present is the period of experimental embryology, although of course there are many problems of
mental embryology, although of course there are many problems of
morphological character which are still to be solved.
morphological character which are still to be solved.


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AN('1aN'r 'l‘IMEs. Much information and many observations known to have
AN('1aN'r 'l‘IMEs. Much information and many observations known to have
been accumulated, but not recorded as a body of knowledge. Systems
been accumulated, but not recorded as a body of knowledge. Systems
of medicine were developed both in Greece and in Egypt in Pre-
of medicine were developed both in Greece and in Egypt in PreAristotelean times.
Aristotelean times.


4-TH CENTURY, B.C. Aristotle (384—322 B.C.) made first system of classification
4-TH CENTURY, B.C. Aristotle (384—322 B.C.) made first system of classification
of animals and plants, published first accounts which are extant of
of animals and plants, published first accounts which are extant of
natural history, anatomy, and embryology. Wrote “De Generatione
natural history, anatomy, and embryology. Wrote “De Generatione
Line 355: Line 322:
anatomy and physiology, but without aid of human dissection.
anatomy and physiology, but without aid of human dissection.


16TH CENTURY. Vesalius (1514-1564) reformed teaching of anatomy. intro-
16TH CENTURY. Vesalius (1514-1564) reformed teaching of anatomy. intro-6 HISTORICAL DEVELOPMENT OF EMBRYOLOGY
-6 HISTORICAL DEVELOPMENT OF EMBRYOLOGY


.ducing dissection and replacing appeal to ancient authorities. “Struc-
.ducing dissection and replacing appeal to ancient authorities. “Structure of Human Body” published 1543.
ture of Human Body” published 1543.
V _ 1625. K Fabricius’ (1537-1619) treatise on development of chick published.
V _ 1625. K Fabricius’ (1537-1619) treatise on development of chick published.
‘1,7'1jH'C1:N'rURY. Harvey (1578-1667) instituted experimental study of living
‘1,7'1jH'C1:N'rURY. Harvey (1578-1667) instituted experimental study of living
Line 365: Line 330:
.“De ’Motu Cordis et Sanguinis” in 1628. Published in 1651 “De
.“De ’Motu Cordis et Sanguinis” in 1628. Published in 1651 “De
Generations Animalium,” an embryological treatise.
Generations Animalium,” an embryological treatise.
Invention of compound microscope had occurred by early years of seven-
Invention of compound microscope had occurred by early years of seven! teenth century and it was applied to biological uses by middle of
! teenth century and it was applied to biological uses by middle of
'- century.
'- century.
16-15. Severinus (1580-1656) published “Zootomia Democritae” giving
16-15. Severinus (1580-1656) published “Zootomia Democritae” giving
Line 388: Line 352:
1675. Leeuwenhoek discovered spermatozoa (also attributed to Hamm,
1675. Leeuwenhoek discovered spermatozoa (also attributed to Hamm,


' a medical student). Leeuwenhoek accordingly became a strong prefor-
' a medical student). Leeuwenhoek accordingly became a strong preforlniationist, adhering to the school of the “spermists.”
lniationist, adhering to the school of the “spermists.”
18TH CENTURY. 1713. Leeuwenhoek discovered parthenogenesis in plants.
18TH CENTURY. 1713. Leeuwenhoek discovered parthenogenesis in plants.
' 1735. ‘Linnaeus (1707-1778) published first edition of “Systcma Naturae.”
' 1735. ‘Linnaeus (1707-1778) published first edition of “Systcma Naturae.”
Line 399: Line 362:
position of epigenesis.
position of epigenesis.


1768. He published “De Formatione Intcstinorum,” the greatest master-
1768. He published “De Formatione Intcstinorum,” the greatest master‘piece of embryology before V011 Bacr.
‘piece of embryology before V011 Bacr.


1799. Cuvier (1769-1832) founded comparative anatomy.
1799. Cuvier (1769-1832) founded comparative anatomy.
Line 425: Line 387:
theory.
theory.


1841. Remak (1815-1865) figured cell division (amitosis). His work and
1841. Remak (1815-1865) figured cell division (amitosis). His work and
that of Kiilliker laid foundations for a theory of cell division.
that of Kiilliker laid foundations for a theory of cell division.


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gastrula stage.
gastrula stage.


1862-1869. Pasteur (1822-1805) and Tyndall (1820-1893) disproved spon-
1862-1869. Pasteur (1822-1805) and Tyndall (1820-1893) disproved spontaneous generation.
taneous generation.


1868. Use of stains in study of cells and protoplasm introduced.
1868. Use of stains in study of cells and protoplasm introduced.
Line 466: Line 427:
1874. Balfour and Foster published “Elements of limbryology.”
1874. Balfour and Foster published “Elements of limbryology.”


1875. Fleininiiig (1843-1905) discovered centrosome.
1875. fleininiiig (1843-1905) discovered centrosome.


1875. Strasburger (1844-1912) first figured adequatel_v chromosomes and
1875. Strasburger (1844-1912) first figured adequatel_v chromosomes and
cell division.
cell division.


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cell lineage in the next two decades.
cell lineage in the next two decades.


1879. Flemming distinguished between direct and indirect types of cell
1879. flemming distinguished between direct and indirect types of cell
division. ‘
division. ‘


188()—1881. Balfour (1851-1882) published “Comparative Embryology.”
188()—1881. Balfour (1851-1882) published “Comparative Embryology.”


1882. Flemming discovered longitudinal split of chromosomes.
1882. flemming discovered longitudinal split of chromosomes.


1883. Roux (1850-1924) began studies of experimental embryology using
1883. Roux (1850-1924) began studies of experimental embryology using
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Since 1890 the advances of embryology have been so numerous and so many
Since 1890 the advances of embryology have been so numerous and so many
investigators have been concerned that it is impossible now to choose between
investigators have been concerned that it is impossible now to choose between
them as to historical significance.
them as to historical significance.


Bibliographic Note
Bibliographic Note


Among the more important accounts of the subjects contained in this chapter
Among the more important accounts of the subjects contained in this chapter
are the following: Locy, Osborne, Foster, Wilson, Gerould, Hertwig, and Norden-
are the following: Locy, Osborne, Foster, Wilson, Gerould, Hertwig, and Nordenskiold. These works are cited in full in the bibliography on page 406.
skiold. These works are cited in full in the bibliography on page 406.


===Chapter II The Germ-Cell Cycle===
===Chapter II The Germ-Cell Cycle===
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The ontogeny of an organism includes its entire cycle of development
The ontogeny of an organism includes its entire cycle of development
from its earliest beginnings to old age and death. Embryology includes
from its earliest beginnings to old age and death. Embryology includes
the first part of this cycle. Broadly considered, it may be held to include
the first part of this cycle. Broadly considered, it may be held to include
the development of the germ cells (gametogenesis) in their preparation
the development of the germ cells (gametogenesis) in their preparation
for fertilization and cleavage, and most text-books treat of these matters.
for fertilization and cleavage, and most text-books treat of these matters.
It is our purpose, however, in the present study to give but brief treat-
It is our purpose, however, in the present study to give but brief treatment to this phase of the subject, for general introductory courses in
ment to this phase of the subject, for general introductory courses in
zoology commonly include a brief outline of gametogenesis, and a more
zoology commonly include a brief outline of gametogenesis, and a more
thorough study deserves more treatment than can be given in a course
thorough study deserves more treatment than can be given in a course
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Embryonic development in its narrower sense may be said to begin
Embryonic development in its narrower sense may be said to begin
with fertilization of the egg and to consist of four periods. These are:
with fertilization of the egg and to consist of four periods. These are:
first, cleavage; second, formation of germ layers; third, period of organ
first, cleavage; second, formation of germ layers; third, period of organ
development; fourth, period of histological differentiation. It is to be
development; fourth, period of histological differentiation. It is to be
noted that in many animals these four periods are not sharply separated
noted that in many animals these four periods are not sharply separated
from each other. The principles which are of importance from a com-
from each other. The principles which are of importance from a comparative standpoint are chiefly illustrated by the first three of these
parative standpoint are chiefly illustrated by the first three of these
periods.
periods.


Line 525: Line 483:
be distinguished from the other cells and organs of the body. Strictly
be distinguished from the other cells and organs of the body. Strictly
speaking, the embryology of an animal would require us to trace the
speaking, the embryology of an animal would require us to trace the
germ cells from their very first appearance on up through the stages
germ cells from their very first appearance on up through the stages
of their development and to trace the formation of the matured sperm
of their development and to trace the formation of the matured sperm
and ovum as well as the fertilization, cleavage, germ-layer formation
and ovum as well as the fertilization, cleavage, germ-layer formation
and the subsequent stages, if we were to give a complete account of
and the subsequent stages, if we were to give a complete account of
development. But it has come to be the practice to begin the embry-
development. But it has come to be the practice to begin the embryologieal account with fertilization and cleavage, and we shall therefore deal with the germ-cell history only briefly, leaving the cytological details for other more exhaustive treatments.
ologieal account with fertilization and cleavage, and we shall there-
fore deal with the germ-cell history only briefly, leaving the cyto-
logical details for other more exhaustive treatments.


Our knowledge of this development is a matter of the last half cen-
Our knowledge of this development is a matter of the last half century, and so voluminous has the accumulated information become on
tury, and so voluminous has the accumulated information become on


the problems connected with the cell that it now constitutes an entirely
the problems connected with the cell that it now constitutes an entirely
Line 541: Line 495:
THE GERM-CELL CYCLE 9
THE GERM-CELL CYCLE 9


separate division 0" zoological science, namely cytology. The founda-
separate division 0" zoological science, namely cytology. The foundations of this science were laid in the last two decades of the nineteenth
tions of this science were laid in the last two decades of the nineteenth
century by investigators who sought information concerning earlier and
century by investigators who sought information concerning earlier and
earlier stages of germ-cell development. These studies received a great
earlier stages of germ-cell development. These studies received a great
Line 566: Line 519:
in early cleavage divisions. In other cases, however, it has not been
in early cleavage divisions. In other cases, however, it has not been
found possible to trace the history of the primordial germ cells back of
found possible to trace the history of the primordial germ cells back of
their first appearance in the gonads. The origin of the primordial germ
their first appearance in the gonads. The origin of the primordial germ
cells is an embryological problem of considerable importance in itself
cells is an embryological problem of considerable importance in itself
aside from its relation to the germ-plasm doctrine, and as such it is
aside from its relation to the germ-plasm doctrine, and as such it is
Line 578: Line 531:
new conception of the germ plasm has now showed itself to be more
new conception of the germ plasm has now showed itself to be more
acceptable to many students of these problems than that of Weismann.
acceptable to many students of these problems than that of Weismann.
According to this new view, each cell contains material which corre-
According to this new view, each cell contains material which corresponds to both the germ plasm and soma, the chromatin representing
sponds to both the germ plasm and soma, the chromatin representing
the former and the cytoplasm the latter. This interpretation explains
the former and the cytoplasm the latter. This interpretation explains
many facts which had previously proven difficult to understand and
many facts which had previously proven difficult to understand and
Line 595: Line 547:
only when the somatic structures are well on the way to their adult
only when the somatic structures are well on the way to their adult
condition. Somatic structures are produced by the differentiation of
condition. Somatic structures are produced by the differentiation of
the cytoplasmic portions of the cells (giving rise to the familiar his-
the cytoplasmic portions of the cells (giving rise to the familiar histological distinctions between tissues), and must obviously precede
tological distinctions between tissues), and must obviously precede
those activities which have for their end the reproduction of the organism. On the other hand, specialization of the nuclear structures involved
those activities which have for their end the reproduction of the organ-
ism. On the other hand, specialization of the nuclear structures involved
in the function of mitotic cell division is responsible for reproduction
in the function of mitotic cell division is responsible for reproduction
and must wait until the proper development of the somatic structure
and must wait until the proper development of the somatic structure
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it does not necessarily begin at the same stage in the life cycle, nor does
it does not necessarily begin at the same stage in the life cycle, nor does
it consist of the same number of cell divisions. It is said that in the
it consist of the same number of cell divisions. It is said that in the
grasshopper there are eight divisions in this period; thus each pri-
grasshopper there are eight divisions in this period; thus each primordial germ cell would produce as a result 256 descendants. The cells
mordial germ cell would produce as a result 256 descendants. The cells
undergoing the various divisions of the multiplication period are knovsn
undergoing the various divisions of the multiplication period are knovsn
as gonia; the male cells are sperrnatogonia and the female oiigonia, alike
as gonia; the male cells are sperrnatogonia and the female oiigonia, alike
Line 615: Line 564:


b. Growth Period. At the end of the multiplication peziod, that is, with
b. Growth Period. At the end of the multiplication peziod, that is, with
the formation of the primary oiigonia or spermatogonia, the active pro-
the formation of the primary oiigonia or spermatogonia, the active proliferation of cells ceases and there follows a growth period. During this
liferation of cells ceases and there follows a growth period. During this
period without further division the cells increase in size and store up
period without further division the cells increase in size and store up
nutrient material, deutoplasm, to furnish them with energy for the
nutrient material, deutoplasm, to furnish them with energy for the
further activities they are to undergo. In the case of the oogonia this
further activities they are to undergo. In the case of the oogonia this
material is the yolk, often present in large amount to furnish food for
material is the yolk, often present in large amount to furnish food for
the embryo until it has become at least in part able to obtain suste-
the embryo until it has become at least in part able to obtain sustenance from its surroundings. The amount and distribution of this yolk
nance from its surroundings. The amount and distribution of this yolk
material is a very important factor in determining the type of cleavage
material is a very important factor in determining the type of cleavage
and future development of the embryo, for cell division becomes increas-
and future development of the embryo, for cell division becomes increasingly difiicult with the accumulation of inert yolk material. (This point
ingly difiicult with the accumulation of inert yolk material. (This point
should be kept in mind, for frequent use must be made of it in the study
should be kept in mind, for frequent use must be made of it in the study
of cleavage types.) These cells are new primary spermatocytes or
of cleavage types.) These cells are new primary spermatocytes or
Line 631: Line 577:


c. Maturation Period. Two maturation divisions now succeed each
c. Maturation Period. Two maturation divisions now succeed each
other, usually with some degree of rapidity. They constitute the matu-
other, usually with some degree of rapidity. They constitute the matuMATURATION PERIOD 11
MATURATION PERIOD 11


ration period during which nuclear events of the utmost importance
ration period during which nuclear events of the utmost importance
Line 651: Line 596:


Cytes
Cytes
spermafids Poiocytes o o o
spermafids Poiocytes o o o
I and 4 4 4
I and 4 4 4
« Mature Egg 5
« Mature Egg 5
Line 664: Line 609:
   
   


FIG. 4. Diagram to illustrate the processes of gametogenesia.
fiG. 4. Diagram to illustrate the processes of gametogenesia.


as spermatogenesis there are two divisions which are similar in all
as spermatogenesis there are two divisions which are similar in all
Line 686: Line 631:
the polocyte, is cut off from the larger “egg cell” which is now the
the polocyte, is cut off from the larger “egg cell” which is now the
second oécyte. In the second maturation division both cells divide, the
second oécyte. In the second maturation division both cells divide, the
“egg cell” again unequally producing a matured egg and another polo-
“egg cell” again unequally producing a matured egg and another polocyte, and the first polocyte two other polocytes. This size dil’ferentiation
cyte, and the first polocyte two other polocytes. This size dil’ferentiation
of the four cells which are descendants of the primary oiigonia allows
of the four cells which are descendants of the primary oiigonia allows
the normal nuclear events of maturation to go on unmodified, but con-
the normal nuclear events of maturation to go on unmodified, but concentrates the ooplasmie materials, which are necessary to the nourishment of the embryo, in one functional cell.
centrates the ooplasmie materials, which are necessary to the nourish-
ment of the embryo, in one functional cell.


Gametogenesis is now completed. Sperm and egg are ready for the
Gametogenesis is now completed. Sperm and egg are ready for the
Line 701: Line 643:
or the development of the zygote, and the restoration of the chromatin
or the development of the zygote, and the restoration of the chromatin
material equivalent to that lost in reduction. This complicated process
material equivalent to that lost in reduction. This complicated process
has been the subject of much study during the last two decades, espe-
has been the subject of much study during the last two decades, especially from the viewpoint of experimental or physiological embryology,
cially from the viewpoint of experimental or physiological embryology,
and many fundamental conceptions have resulted from this fascinating
and many fundamental conceptions have resulted from this fascinating
phase of embryologieal research.
phase of embryologieal research.
Line 713: Line 654:


a. Reduction. It may be stated as a general law that every species of
a. Reduction. It may be stated as a general law that every species of
organism is characterized by a definite number of chromosomes, and,
organism is characterized by a definite number of chromosomes, and,
REDUCTION 13
REDUCTION 13


with a few exceptions which are not in contradiction to a full and ade-
with a few exceptions which are not in contradiction to a full and adequate statement of the law, this number occurs in all the cells throughout the bodies of all the members of a particular species. This characteristic number is spoken of as the somatic or diploid number. In the
quate statement of the law, this number occurs in all the cells through-
out the bodies of all the members of a particular species. This charac-
teristic number is spoken of as the somatic or diploid number. In the
history of the germ cells all the divisions of the multiplication period
history of the germ cells all the divisions of the multiplication period
are found to have this characteristic number. During the maturation
are found to have this characteristic number. During the maturation
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In those cases in which the (lijfcrences between reductional and somatic
In those cases in which the (lijfcrences between reductional and somatic
mitoses are most clearly recognizable (that is, in those cases in which
mitoses are most clearly recognizable (that is, in those cases in which
tctrads are formed), we may say that the explanation lies in two out-
tctrads are formed), we may say that the explanation lies in two outstanding facts, namely, the peculiar prophase of the first division with
standing facts, namely, the peculiar prophase of the first division with
its synaptic pairing of homologous chromosomes, and the entire absence
its synaptic pairing of homologous chromosomes, and the entire absence
of a prophase to the second division. The case of Ascaris, the round-
of a prophase to the second division. The case of Ascaris, the roundworm, is one of the best known, and it may serve as an illustration of
worm, is one of the best known, and it may serve as an illustration of
these processes. The somatic number of chromosomes in the common
these processes. The somatic number of chromosomes in the common
Ascaris is four. These are not looked upon as four separate and unrelated
Ascaris is four. These are not looked upon as four separate and unrelated
Line 745: Line 681:
it is very probable that this is always the case. The members of a pair
it is very probable that this is always the case. The members of a pair
are spoken of as homologous chromosomes. Thus each individual derived
are spoken of as homologous chromosomes. Thus each individual derived
from a fertilized egg contains in each of its cells two full sets of homolo-
from a fertilized egg contains in each of its cells two full sets of homologous chromosomes. This fact is to be contrasted with the well-substantiated observation that the germ eells contain but a single set of chromosomes owing to the process of reduction. It will be recalled that a typical
gous chromosomes. This fact is to be contrasted with the well-substanti-
ated observation that the germ eells contain but a single set of chromo-
somes owing to the process of reduction. It will be recalled that a typical
mitotic division, whether in a germ cell or a somatic cell, involves in the
mitotic division, whether in a germ cell or a somatic cell, involves in the
prophase a condition which is really the climax of the entire set of
prophase a condition which is really the climax of the entire set of
mitotic events, namely the splitting of the spireme thread which is to
mitotic events, namely the splitting of the spireme thread which is to
condense to form the metaphase chromosomes. For this reason the meta-
condense to form the metaphase chromosomes. For this reason the metaphase chromosome may be looked upon as consisting of two halves, or
phase chromosome may be looked upon as consisting of two halves, or
chromatids, even if this condition sometimes is not easily seen under
chromatids, even if this condition sometimes is not easily seen under
the microscope. That is to say, the ordinary chromosome is a. bivalent
the microscope. That is to say, the ordinary chromosome is a. bivalent
one, a dyad. With these facts in mind we are now ready to inquire into
one, a dyad. With these facts in mind we are now ready to inquire into
the nature of synapsis.
the nature of synapsis.
FIG. 5. Fertilization and cleavage of Ascaris. (Redrawn from Kellicott after Bovcri.)
fiG. 5. Fertilization and cleavage of Ascaris. (Redrawn from Kellicott after Bovcri.)


A, epermntozoon entering the egg as the second maturation division is taking plan-.
A, epermntozoon entering the egg as the second maturation division is taking plan-.
Line 770: Line 702:


h‘ h’ h‘ h‘
h‘ h’ h‘ h‘
FIG. 6. Diagram of tctr-ad formation and subsequent ro(lu('lion. (Suggested by diagrams
fiG. 6. Diagram of tctr-ad formation and subsequent ro(lu('lion. (Suggested by diagrams
from Sharp.)
from Sharp.)


a. chromosome conditions in spernmtogoniu and at beginning: of first maturation pro-
a. chromosome conditions in spernmtogoniu and at beginning: of first maturation prophuse; I). synopsis in prophnse of first maturation prophnsc (first spernw.tot_vte), 0, tctrad-5
phuse; I). synopsis in prophnse of first maturation prophnsc (first spernw.tot_vte), 0, tctrad-5
ready for the division; d. metaphnse of first niaturmitm division; 0. unaphuse of d; f.
ready for the division; d. metaphnse of first niaturmitm division; 0. unaphuse of d; f.
second spcrmntocytes produced by the division of e; g, division of second spermutocytes;
second spcrmntocytes produced by the division of e; g, division of second spermutocytes;
Line 791: Line 722:
bodies.
bodies.


As a result of synapsis it appears that there are in each first spermato-
As a result of synapsis it appears that there are in each first spermatocyte or oocyte the reduced number of chromosomes in the form of
cyte or oocyte the reduced number of chromosomes in the form of
tetrads, or quadrivalent chromosomes. Each tetrad consists of four
tetrads, or quadrivalent chromosomes. Each tetrad consists of four
chromatids, aa/bb’, two from each of the homologous mates, A and B.
chromatids, aa/bb’, two from each of the homologous mates, A and B.
If, in the succeeding metaphases and anaphases, the bivalent chromo-
If, in the succeeding metaphases and anaphases, the bivalent chromosomes (dyads) which are the result of the division of the tetrad are
somes (dyads) which are the result of the division of the tetrad are
each composed of two chromatids derived from the same one of the
each composed of two chromatids derived from the same one of the
constituent synaptic mates, that is, a and a’ in one chromosome and
constituent synaptic mates, that is, a and a’ in one chromosome and
Line 804: Line 733:
equivalent half chromosomes would necessarily be separated as in any
equivalent half chromosomes would necessarily be separated as in any
ordinary mitosis. That is, the bivalent aa’ is now divided into a and a’
ordinary mitosis. That is, the bivalent aa’ is now divided into a and a’
and bb’ into b and b’, and the maturation with the consequent distribu-
and bb’ into b and b’, and the maturation with the consequent distribution of the four parts of the tetrad to the four germ cells is completed.
tion of the four parts of the tetrad to the four germ cells is completed.
If, on the other hand, the bivalent chromosomes resulting from the
If, on the other hand, the bivalent chromosomes resulting from the
division of the tetrads consist of half of each synaptic mate, that is
division of the tetrads consist of half of each synaptic mate, that is
a and b in one and a’ and b’ (or of course a and b’ or a’ and b may be
a and b in one and a’ and b’ (or of course a and b’ or a’ and b may be
linked together), then the first division is equational. The second divi-
linked together), then the first division is equational. The second division would then be reductional and as in the previous case would result
sion would then be reductional and as in the previous case would result
in the distribution of the four component parts of the tetrad to the four
in the distribution of the four component parts of the tetrad to the four
matured germ cells.
matured germ cells.
Line 819: Line 746:
large number of cases, however, in which actual tetrads are not formed
large number of cases, however, in which actual tetrads are not formed
owing to the failure of the usual split of the spireme to appear during
owing to the failure of the usual split of the spireme to appear during
the early stages of the first division. In this case the first division is
the early stages of the first division. In this case the first division is
always reductional; there is a pause between the first and second
always reductional; there is a pause between the first and second
divisions during which the chromosomes undergo seine reorganization;
divisions during which the chromosomes undergo seine reorganization;
and the splitting which was delayed takes place. It is evident, therefore,
and the splitting which was delayed takes place. It is evident, therefore,
that precisely the same result is achieved in the two cases, whether or
that precisely the same result is achieved in the two cases, whether or
not tetrad formation occurs. That is, there are formed from each sper-
not tetrad formation occurs. That is, there are formed from each spermatocyte or ooeyte of the first order four cells, each with half the number
matocyte or ooeyte of the first order four cells, each with half the number
of chromosomes characteristic of the species. These four cells are mature
of chromosomes characteristic of the species. These four cells are mature
spermatozoa or one functional egg and three polocytes or polar bodies.
spermatozoa or one functional egg and three polocytes or polar bodies.
Line 858: Line 784:
Wierzejski on Physa, of Boveri on Ascarzs, and of many others. In most
Wierzejski on Physa, of Boveri on Ascarzs, and of many others. In most
animals the entire sperm enters the egg, but there are many others, as
animals the entire sperm enters the egg, but there are many others, as
in the sea—urchin and the staifish, in which the tail or at least most of it
in the sea—urchin and the staifish, in which the tail or at least most of it
remains outside. The important elements of the sperm that enter the
remains outside. The important elements of the sperm that enter the
egg and have a function in fertilization are the head which is equivalent
egg and have a function in fertilization are the head which is equivalent
Line 867: Line 793:
of much discussion in connection with fertilization. The sperm enters
of much discussion in connection with fertilization. The sperm enters
rather largely through the activity of the cortical layer of the egg and
rather largely through the activity of the cortical layer of the egg and
by a. fairly definite path makes its way toward the egg pronucleus.
by a. fairly definite path makes its way toward the egg pronucleus.
Immediately upon entrance, however, it rotates so that the middle piece
Immediately upon entrance, however, it rotates so that the middle piece
18 THE GERM-CELL CYCLE
18 THE GERM-CELL CYCLE
Line 884: Line 810:
   
   


FIG 15. Steps in fertilization of the sea ur(-hm, Tow1mc'u.stcs (Redrawn from (‘oiiklin
fiG 15. Steps in fertilization of the sea ur(-hm, Tow1mc'u.stcs (Redrawn from (‘oiiklin
after Wilson )
after Wilson )


Line 902: Line 828:
the egg before either polar body has been extruded; in some cases it may
the egg before either polar body has been extruded; in some cases it may
be before the germinal vesicle has been broken down, in others while the
be before the germinal vesicle has been broken down, in others while the
first maturation mitosis is in the metaphase stage. Nematodes, fiat-
first maturation mitosis is in the metaphase stage. Nematodes, fiatworms, molluscs, some annelids and crustaceans belong to the Ascaris
worms, molluscs, some annelids and crustaceans belong to the Ascaris
type. There are of course intermediate stages between these two extremes.
type. There are of course intermediate stages between these two extremes.


Line 910: Line 835:
and a cleavage spindle is formed between them. There is seldom an actual
and a cleavage spindle is formed between them. There is seldom an actual
fusion of the pronuclei as such; rather they lie side by side upon the
fusion of the pronuclei as such; rather they lie side by side upon the
developing first cleavage spindle, and at the end of this first division
developing first cleavage spindle, and at the end of this first division
the chromosomes of the components are intermingled and are no longer
the chromosomes of the components are intermingled and are no longer
to be distinguished as from the two parents.
to be distinguished as from the two parents.
Line 927: Line 852:


Of the four stages of embryonic development, cleavage, germ-layer
Of the four stages of embryonic development, cleavage, germ-layer
formation, period of development of organs, and of histological differ-
formation, period of development of organs, and of histological differentiation, the period of cleavage is the most constantly recognizable and
entiation, the period of cleavage is the most constantly recognizable and
the most distinct. It consists of a succession of cell divisions taking
the most distinct. It consists of a succession of cell divisions taking
place in a very regular manner and having for their purpose the distribu-
place in a very regular manner and having for their purpose the distribution of the egg protoplasm into a great many single cells. Every organism
tion of the egg protoplasm into a great many single cells. Every organism
above the protozoa consists of many cells, and every one starts as a
above the protozoa consists of many cells, and every one starts as a
single-celled egg. The first problem of development for the fertilized egg,
single-celled egg. The first problem of development for the fertilized egg,
therefore, is that of the regular distribution of its substance in such a
therefore, is that of the regular distribution of its substance in such a
manner that the organs of the later stages may normally arise from the
manner that the organs of the later stages may normally arise from the
appropriate material. Since divisions follow one another with consid-
appropriate material. Since divisions follow one another with considerable rapidity during cleavage the daughter cells never have time to
erable rapidity during cleavage the daughter cells never have time to
grow to the size of the mother cell. The cleavage cells or blastomeres
grow to the size of the mother cell. The cleavage cells or blastomeres
normally divide into two cells each, thus setting up a normal rhythm
normally divide into two cells each, thus setting up a normal rhythm
Line 978: Line 900:
@@€B
@@€B


Fro. 9. The progress of the first cleavages of the snail, Planorbis, showing the man-
Fro. 9. The progress of the first cleavages of the snail, Planorbis, showing the manner in which the furrows out through forming two spherical blastomcres. which then
ner in which the furrows out through forming two spherical blastomcres. which then
draw together, substituting :1. plane of contact for the point of contact.
draw together, substituting :1. plane of contact for the point of contact.


Line 985: Line 906:
four regions, namely, a clear protoplasmic cap at the animal pole, a
four regions, namely, a clear protoplasmic cap at the animal pole, a
darker area at the vegetative, and in between two crescents, one yellow
darker area at the vegetative, and in between two crescents, one yellow
and one light gray. There are thus localized certain organ-forming sub-
and one light gray. There are thus localized certain organ-forming sub22 EGG AND CLEAVAGE TYPES
22 EGG AND CLEAVAGE TYPES


stances in four different regions, and these will give rise to very different
stances in four different regions, and these will give rise to very different
Line 995: Line 915:
whole. This statement is true only in the sense that the egg commonly
whole. This statement is true only in the sense that the egg commonly
shows little evidence of histological differentiation, and the same is at
shows little evidence of histological differentiation, and the same is at
least superficially true of the early blastomercs. That the resemblance
least superficially true of the early blastomercs. That the resemblance
is only superficial, however, is also borne out by the nuclei of certain
is only superficial, however, is also borne out by the nuclei of certain
forms. In Ascaris one of the two nuclei of the 2—cell stage undergoes a
forms. In Ascaris one of the two nuclei of the 2—cell stage undergoes a
process known as chromatin diminution, becomes smaller, and stains
process known as chromatin diminution, becomes smaller, and stains
Line 1,007: Line 927:
the blastomeres arrange themselves at the periphery of the mass and
the blastomeres arrange themselves at the periphery of the mass and
leave a cavity at the center, known variously as a cleavage cavity,
leave a cavity at the center, known variously as a cleavage cavity,
segmentation cavity, blastocoele, or primary body cavity. It is filled
segmentation cavity, blastocoele, or primary body cavity. It is filled
with fluid or with a gelatinous secretion. In eggs containing large
with fluid or with a gelatinous secretion. In eggs containing large
amounts of yolk, however, the cavity is crowded out of the center and
amounts of yolk, however, the cavity is crowded out of the center and
Line 1,014: Line 934:
involves the entire surface or is limited to a small area of it.
involves the entire surface or is limited to a small area of it.


Cleavage may be said to begin with the formation of the first seg-
Cleavage may be said to begin with the formation of the first segmentation spindle. This is a more accurate statement than that it follows
mentation spindle. This is a more accurate statement than that it follows
fertilization, for in the case of eggs which develop parthenogenetically
fertilization, for in the case of eggs which develop parthenogenetically
there is of course no fertilization. It is more difficult to say when it
there is of course no fertilization. It is more difficult to say when it
Line 1,022: Line 941:
reached with the establishment of a definite size relation between
reached with the establishment of a definite size relation between
nucleus and cytoplasm (the nucleo-cytoplasmic ratio), the particular
nucleus and cytoplasm (the nucleo-cytoplasmic ratio), the particular
ratio being that which is normal for that particular stage of that par-
ratio being that which is normal for that particular stage of that particular species. It is of course to be noted that where differentiations
ticular species. It is of course to be noted that where differentiations
due to yolk, etc., are present there cannot be a single nucleo—cytoplasmic
due to yolk, etc., are present there cannot be a single nucleo—cytoplasmic
ratio for an entire embryo. It is perhaps better to say that cleavage is
ratio for an entire embryo. It is perhaps better to say that cleavage is
Line 1,032: Line 950:
phenomena. that three distinct kinds of processes are involved in the
phenomena. that three distinct kinds of processes are involved in the
transformation of the egg into a larva. These are cell division, growth,
transformation of the egg into a larva. These are cell division, growth,
and difi‘erentia.tion—processes which are not only distinct, but to a
and difi‘erentia.tion—processes which are not only distinct, but to a
certain extent antagonistic, the last two never taking place at the same
certain extent antagonistic, the last two never taking place at the same
CLASSIFICATION OF EGG TYPES 23
CLASSIfiCATION OF EGG TYPES 23


time with the first, and only to a minor extent together. (Differentiation
time with the first, and only to a minor extent together. (Differentiation
Line 1,058: Line 976:


It should also be made clear that a classification of cleavage types has
It should also be made clear that a classification of cleavage types has
nothing of the evolutionary significance which the systematic grouping
nothing of the evolutionary significance which the systematic grouping
of animals has, nor can it be made a basis for systematic classification.
of animals has, nor can it be made a basis for systematic classification.
Although cleavage types are in general stable and are coextensive with
Although cleavage types are in general stable and are coextensive with
certain animal groups, yet there are very notable departures in this
certain animal groups, yet there are very notable departures in this
Line 1,066: Line 984:
the scorpions cleave differently from others of their class, and that
the scorpions cleave differently from others of their class, and that
many other exceptions also exist. Indeed, there are instances in which
many other exceptions also exist. Indeed, there are instances in which
nearly related species have different methods of cleavage, and the ex-
nearly related species have different methods of cleavage, and the extreme modification of this sort is perhaps seen where two types of
treme modification of this sort is perhaps seen where two types of
cleavage occur in the very same species. An example of this last case
cleavage occur in the very same species. An example of this last case
is seen in Polyphemus oculus, whose summer eggs undergo regular holo-
is seen in Polyphemus oculus, whose summer eggs undergo regular holoblastie cleavage, whereas in the winter eggs a type of Ineroblastic cleavage occurs which strongly suggests conditions found in the superficial
blastie cleavage, whereas in the winter eggs a type of Ineroblastic cleav-
age occurs which strongly suggests conditions found in the superficial
cleavage of some insect eggs. These are, of course, extreme cases which
cleavage of some insect eggs. These are, of course, extreme cases which
merely serve to show how variable cleavage forms may be, doubtless
merely serve to show how variable cleavage forms may be, doubtless
as adaptive responses to the conditions of development, without having
as adaptive responses to the conditions of development, without having
any special phylogenetic or taxonomic significance.
any special phylogenetic or taxonomic significance.


1. Classification of Egg Types
1. Classification of Egg Types


On the basis of their structure, particularly as modified by the amount
On the basis of their structure, particularly as modified by the amount
Line 1,091: Line 1,006:
Telolecz'thal’eggs have a clear axial structure, the protoplasm at the
Telolecz'thal’eggs have a clear axial structure, the protoplasm at the
animal pole containing very little yolk, while the vegetative half of the
animal pole containing very little yolk, while the vegetative half of the
egg is rich in yolk. The frog egg may be taken as an example. The blasto-
egg is rich in yolk. The frog egg may be taken as an example. The blastomeres at the vegetal pole, therefore, are distinctly larger by reason of
meres at the vegetal pole, therefore, are distinctly larger by reason of
their large yolk content, and the cleavage cavity is pushed toward the
their large yolk content, and the cleavage cavity is pushed toward the
animal pole. Such eggs necessarily have unequal cleavage, if the furrows
animal pole. Such eggs necessarily have unequal cleavage, if the furrows
Line 1,099: Line 1,013:
In another type of telolecithal eggs the accumulation of yolk is so
In another type of telolecithal eggs the accumulation of yolk is so
great that it cannot undergo cleavage. The protoplasm is thus limited
great that it cannot undergo cleavage. The protoplasm is thus limited
by the yolk to a small disc at one pole of the egg while the yolk fills
by the yolk to a small disc at one pole of the egg while the yolk fills
the rest of the space. The eggs of birds and of teleost fishes furnish
the rest of the space. The eggs of birds and of teleost fishes furnish
excellent examples. When cleavage takes place it cuts through the disc
excellent examples. When cleavage takes place it cuts through the disc
only, and is therefore discoidal.
only, and is therefore discoidal.
Line 1,107: Line 1,021:
entire egg cleaves, although unequally; and meroblastic, in which only
entire egg cleaves, although unequally; and meroblastic, in which only
part of the egg mass can be divided, and that by either discoidal or
part of the egg mass can be divided, and that by either discoidal or
superficial cleavage. The terms “partial” and “total” cleavage also
superficial cleavage. The terms “partial” and “total” cleavage also
apply to these types. Between these two types there are of course inter-
apply to these types. Between these two types there are of course intermediate conditions shown by various eggs. These two extremes lead to
mediate conditions shown by various eggs. These two extremes lead to
two types of embryo formation; in the holoblastic egg the entire egg
two types of embryo formation; in the holoblastic egg the entire egg
goes to form the embryo body, but in the meroblastic type the germ disc
goes to form the embryo body, but in the meroblastic type the germ disc
Line 1,118: Line 1,031:
cytoplasmic area is located at the center of the egg surrounded by the
cytoplasmic area is located at the center of the egg surrounded by the
yolk. A protoplasmic layer, however, covers the surface and is connected
yolk. A protoplasmic layer, however, covers the surface and is connected
to the central mass by fine plasmic threads. Some centrolecithal eggs
to the central mass by fine plasmic threads. Some centrolecithal eggs
are so definitely oriented that the position in which they are laid indi-
are so definitely oriented that the position in which they are laid indicates exactly the axes of the future embryo, but in general the primary
cates exactly the axes of the future embryo, but in general the primary
axes are not well developed in eggs of this type, although bilaterality is
axes are not well developed in eggs of this type, although bilaterality is
to be noted. Cleavage begins by the plasma island in the center multi-
to be noted. Cleavage begins by the plasma island in the center multiplying through several nuclear divisions, thus forming a syncytium.
plying through several nuclear divisions, thus forming a syncytium.
These “blastomeres” now move radially toward the periphery and unite
These “blastomeres” now move radially toward the periphery and unite
with the plasma layer which is at once cut up into cytoplasmic areas
with the plasma layer which is at once cut up into cytoplasmic areas
of similar size, each supplied with a nucleus. The central yolk does not
of similar size, each supplied with a nucleus. The central yolk does not
divide, or if division starts it is incomplete. This constitutes superficial
divide, or if division starts it is incomplete. This constitutes superficial
cleavage, the blastoderm forming about the yolk which fills entirely the
cleavage, the blastoderm forming about the yolk which fills entirely the
cleavage cavity (if one might use that expression).
cleavage cavity (if one might use that expression).
CLASSIFICATION OF CLEAVAGE TYPES 25
CLASSIfiCATION OF CLEAVAGE TYPES 25


2. Classification of Cleavage Types
2. Classification of Cleavage Types


Dependent upon the amount of yolk they contain, the first divisions
Dependent upon the amount of yolk they contain, the first divisions
of eggs are total or partial. Eggs having total cleavage are said to be
of eggs are total or partial. Eggs having total cleavage are said to be
holoblastic; those having partial cleavage are meroblastic. It is also cus-
holoblastic; those having partial cleavage are meroblastic. It is also customary to classify types upon the basis of the planes of symmetry which
tomary to classify types upon the basis of the planes of symmetry which


EGG GERM C LEAVAG E
EGG GERM C LEAVAG E
Line 1,160: Line 1,070:
Nemertcans
Nemertcans


[4, Spiral Annelids and mol-
[4, Spiral Annelids and moll11.~cs(ox<'(-pt(~(-pl1'l‘eloleci1lml alopods)
l11.~cs(ox<'(-pt(~(-pl1-
'l‘eloleci1lml alopods)


Scorpion
Scorpion
Line 1,184: Line 1,092:
Arthropoda (except
Arthropoda (except
scorpions)
scorpions)
Controlecitlml Superficial U}. Superficial Someotherscattered
Controlecitlml Superficial U}. Superficial Someotherscattered
' forms among coe-
' forms among coelenterates
lenterates
26 EGG AND CLEAVAGE TYPES
26 EGG AND CLEAVAGE TYPES


Line 1,195: Line 1,102:
of the spindle"in the first divisions turns in a spiral with reference to
of the spindle"in the first divisions turns in a spiral with reference to
the egg axis. These four cleavage types are holoblastic. Meroblastic eggs
the egg axis. These four cleavage types are holoblastic. Meroblastic eggs
may be divided into superficial and discoidal. In the former case the
may be divided into superficial and discoidal. In the former case the
blastodisc forms around the outside of the egg but involves practically
blastodisc forms around the outside of the egg but involves practically
the entire surface whereas in the latter only a small disc undergoes
the entire surface whereas in the latter only a small disc undergoes
Line 1,202: Line 1,109:
groups to which they belong» We shall consider these types in order.
groups to which they belong» We shall consider these types in order.


3. Classification on the Basis of Predelineation
3. Classification on the Basis of Predelineation


Before considering the details of these different modes of cleavage it
Before considering the details of these different modes of cleavage it
is desirable to mention certain qualities of eggs by which they are related
is desirable to mention certain qualities of eggs by which they are related
to the later developing stages. With reference to the degree of pre-
to the later developing stages. With reference to the degree of predelineation shown, Conklin has recognized two types of eggs as follows:
delineation shown, Conklin has recognized two types of eggs as follows:


a. Eggs with Determinative Cleavage. The best examples are the eggs
a. Eggs with Determinative Cleavage. The best examples are the eggs
of annelids, mo1‘uscs (except the cephalopods), and the ascidians. In
of annelids, mo1‘uscs (except the cephalopods), and the ascidians. In
eggs of these groups after fertilization, but before cleavage, there can
eggs of these groups after fertilization, but before cleavage, there can
be recognized in the one-cell stages regions or definite areas in the egg
be recognized in the one-cell stages regions or definite areas in the egg
protoplasm, the organ-forming regions of His. These regions are dis-
protoplasm, the organ-forming regions of His. These regions are distinguishable in various eggs by different means, among which are differences in yolk content, presence or absence of pigment, clear or granular condition of the cytoplasm, and the presence of very fine granules
tinguishable in various eggs by different means, among which are dif-
ferences in yolk content, presence or absence of pigment, clear or gran-
ular condition of the cytoplasm, and the presence of very fine granules
which can be demonstrated by definite staining methods. The centrifuge
which can be demonstrated by definite staining methods. The centrifuge
has also proved useful in detecting different substances in the egg which
has also proved useful in detecting different substances in the egg which
as cleavage advances become segregated into different blastorneres. (Cf.
as cleavage advances become segregated into different blastorneres. (Cf.
the work of Lyon, Lillie, Conklin, etc.) The study of the cell lineage of
the work of Lyon, Lillie, Conklin, etc.) The study of the cell lineage of
such an egg shows that these blastomeres are the beginnings of definite
such an egg shows that these blastomeres are the beginnings of definite
organs of the embryo. In other words the egg substances which are
organs of the embryo. In other words the egg substances which are
thus localized into regions are determined for the production of definite
thus localized into regions are determined for the production of definite
organs of the later stages. During the progress of the investigations
organs of the later stages. During the progress of the investigations
which established the determinative character of certain eggs there was
which established the determinative character of certain eggs there was
a great deal of discussion, and even controversy, as to whether blaste-
a great deal of discussion, and even controversy, as to whether blastemeres were totipotent, that is, interchangeable, or constituted a mosaic
meres were totipotent, that is, interchangeable, or constituted a mosaic
work, each being capable of taking only its own special place. We now
work, each being capable of taking only its own special place. We now
understand that eggs which have determinative cleavage have an opera-
understand that eggs which have determinative cleavage have an operative mechanism of great precision, and that correspondingly they have lost
tive mechanism of great precision, and that correspondingly they have lost
much of their power of regulation. Because of their content of organforming substances they are apparently destined for a particular fate,
much of their power of regulation. Because of their content of organ-
forming substances they are apparently destined for a particular fate,
EGGS WITH IN DETERMINATE CLEAVAGE 27
EGGS WITH IN DETERMINATE CLEAVAGE 27


Line 1,242: Line 1,142:
type differentiation sets in only relatively late after the embryo consists
type differentiation sets in only relatively late after the embryo consists
of many cells. In the preceding case the marks of differentiation are
of many cells. In the preceding case the marks of differentiation are
recognizable from the very first. In indeterminative eggs, there are no
recognizable from the very first. In indeterminative eggs, there are no
orgamforming regions, little histological differentiation is found, and
orgamforming regions, little histological differentiation is found, and
the blastomeres appear to be alike. Such eggs are simple in structure
the blastomeres appear to be alike. Such eggs are simple in structure
and are accompanied by high capacity for regulation. Examples are:
and are accompanied by high capacity for regulation. Examples are:
vertebrates, some insects, most arthropods, cephalopods, most eehino-
vertebrates, some insects, most arthropods, cephalopods, most eehinoderms. In them the power of regulation is much greater than in the
derms. In them the power of regulation is much greater than in the
determinative type, and there is much evidence to indicate that the fate
determinative type, and there is much evidence to indicate that the fate
of a blastomere is often a function of its position, or that the blastomeres
of a blastomere is often a function of its position, or that the blastomeres
Line 1,257: Line 1,156:


Among the more important accounts of the subjects contained in this chapter
Among the more important accounts of the subjects contained in this chapter
are the following: Korsehelt and Heider, Conklin. Morgan in “Experimental Embry-
are the following: Korsehelt and Heider, Conklin. Morgan in “Experimental Embryology,” Cowdry’s “General Cytology” (especially the article by Conklin on "Cellular
ology,” Cowdry’s “General Cytology” (especially the article by Conklin on "Cellular
Difierentiation”). These works are cited in full in the bibliography on page 406.
Difierentiation”). These works are cited in full in the bibliography on page 406.




Line 1,266: Line 1,164:
I. RADIAL CLEAVAGE
I. RADIAL CLEAVAGE


The eggs of the Porifera, of all the coelenterates, except the cteno-
The eggs of the Porifera, of all the coelenterates, except the ctenophores, and of the echinoderrns have radial cleavage. Formerly amphioxus was given as a type of this class, but it has been shown that the
phores, and of the echinoderrns have radial cleavage. Formerly amphi-
oxus was given as a type of this class, but it has been shown that the
older accounts were in error, and that its cleavage is really bilateral.
older accounts were in error, and that its cleavage is really bilateral.


Line 1,274: Line 1,170:
83%?
83%?


Flu. 10. The vleiivage of sea cucumber Synapta dig/Lluta. (Redrawn from horsehclt
flu. 10. The vleiivage of sea cucumber Synapta dig/Lluta. (Redrawn from horsehclt
and Heider after Selcnka.)
and Heider after Selcnka.)


Line 1,288: Line 1,184:
RADIAL CLEAVAGE 29
RADIAL CLEAVAGE 29


succeed each other in regular alternation dividing the egg first meridion-
succeed each other in regular alternation dividing the egg first meridionally and then equatorially into equal blastomeres. It very nearly cor—
ally and then equatorially into equal blastomeres. It very nearly cor—
responds to the Sachs’ principle of the alternation at right angles of
responds to the Sachs’ principle of the alternation at right angles of
successive planes of cell division. The first furrow is meridional and
successive planes of cell division. The first furrow is meridional and
divides the egg equally. The second furrow is also meridional and
divides the egg equally. The second furrow is also meridional and


1 It: 11 Continuation of Fig 10 32-, 64-, and 128-cell st Lges of S:/napta dmztata
1 It: 11 Continuation of fig 10 32-, 64-, and 128-cell st Lges of S:/napta dmztata


divides each of the first two blastomeres equally. The third furrow is
divides each of the first two blastomeres equally. The third furrow is
equatorial and the blastomeres are equal, making eight cells arranged
equatorial and the blastomeres are equal, making eight cells arranged
in two rows about the two poles. By this time a tiny cavity is discover-
in two rows about the two poles. By this time a tiny cavity is discoverable at the center of the mass which is to become the cleavage cavity or
able at the center of the mass which is to become the cleavage cavity or
blastocoele. The furrows of the next cleavage are meridional but at an
blastocoele. The furrows of the next cleavage are meridional but at an
angle of 45 degrees to the first and second. The furrows of the fifth are
angle of 45 degrees to the first and second. The furrows of the fifth are
again latitudinal, dividing all the blastomeres equally. Subsequently the
again latitudinal, dividing all the blastomeres equally. Subsequently the
divisions keep their regular alternation for a period, forming a blastula
divisions keep their regular alternation for a period, forming a blastula
Line 1,311: Line 1,205:
coeloblastula) is formed.
coeloblastula) is formed.


The cleavage of many jellyfishes, though in general radial, undergoes
The cleavage of many jellyfishes, though in general radial, undergoes
many modifications due to yolk distribution, loose arrangement of cells,
many modifications due to yolk distribution, loose arrangement of cells,
and to other factors.
and to other factors.


Radial cleavage undergoes some interesting modifications in some of
Radial cleavage undergoes some interesting modifications in some of
the sea-urchins, notably Strongylocentrotus lividus, as shown by Boveri
the sea-urchins, notably Strongylocentrotus lividus, as shown by Boveri
(1901). In this form cleavage is unequal and differential. The egg is of a
(1901). In this form cleavage is unequal and differential. The egg is of a
Line 1,336: Line 1,230:
the remainder being in the four blastomeres of the vegetal half of the
the remainder being in the four blastomeres of the vegetal half of the
egg. Now follows a peculiar differential cleavage, the upper four cells
egg. Now follows a peculiar differential cleavage, the upper four cells
dividing meridionally while the lower four are unequally divided lati-
dividing meridionally while the lower four are unequally divided latitudinally. This results in the immediate segregation of the pigment-free
tudinally. This results in the immediate segregation of the pigment-free
cap into four vegetative cells, the micromeres. The descendants of these
cap into four vegetative cells, the micromeres. The descendants of these
are later to form the primary mesoderm.
are later to form the primary mesoderm.
Line 1,343: Line 1,236:
In producing the next stage (32 cells) the eight cells of the animal half
In producing the next stage (32 cells) the eight cells of the animal half
(mesomeres) divide equally and latitudinally producing two wreaths of
(mesomeres) divide equally and latitudinally producing two wreaths of
eight cells each. The four larger pigmented macromcres divide meridion-
eight cells each. The four larger pigmented macromcres divide meridionally, and the four micromeres of the unpigmented cap latitudina.lly and
ally, and the four micromeres of the unpigmented cap latitudina.lly and
unequally. Subsequent divisions tend to equalize the size differences
unequally. Subsequent divisions tend to equalize the size differences
and the blastula is regular and consists of equal—sized cells, but from the
and the blastula is regular and consists of equal—sized cells, but from the
Line 1,351: Line 1,243:
from the macromeres come the endoderm and secondary mesoderm;
from the macromeres come the endoderm and secondary mesoderm;
and the primary mesoderm is from the micromeres.
and the primary mesoderm is from the micromeres.
FIG 1! (‘tonvage of sea.-urchm Strormylorerwrotm (Rcdnuvn from Korschelt and
fiG 1! (‘tonvage of sea.-urchm Strormylorerwrotm (Rcdnuvn from Korschelt and
Hmder after Boven )
Hmder after Boven )


Line 1,364: Line 1,256:
  3 F
  3 F


FIG. 13. Cleavage of Baron. (Rcdruwn from Korsclu-It and Heidcr after Zoigler.)
fiG. 13. Cleavage of Baron. (Rcdruwn from Korsclu-It and Heidcr after Zoigler.)


A. second division. The vegetative pole is the upper, as in other figure showing lateral
A. second division. The vegetative pole is the upper, as in other figure showing lateral
view; B. 4-cell stage; C, 8-cell stage from animal pole, as, median plane; bl), transverse
view; B. 4-cell stage; C, 8-cell stage from animal pole, as, median plane; bl), transverse
plane; D. same from lateral view; E, F, 16—cell stages from animal pole and from side View
plane; D. same from lateral view; E, F, 16—cell stages from animal pole and from side View
Line 1,372: Line 1,264:


that they constitute a remarkable exception to the general rules is their
that they constitute a remarkable exception to the general rules is their
greatest interest. Although the peculiarities of these forms early stimu-
greatest interest. Although the peculiarities of these forms early stimulated a great deal of investigation, Ziegler’s findings (1898) form the
lated a great deal of investigation, Ziegler’s findings (1898) form the
basis of our present understanding of this type of development.
basis of our present understanding of this type of development.
DISYMMETRICAL CLEAVAGE 33
DISYMMETRICAL CLEAVAGE 33
Line 1,379: Line 1,270:
The eggs of ctenophores have an ectoplasmic surface layer and an
The eggs of ctenophores have an ectoplasmic surface layer and an
inner vaeuolated yolk mass; the nucleus lies in the ectoplasm near the
inner vaeuolated yolk mass; the nucleus lies in the ectoplasm near the
vegetative pole of the egg where the polar bodies are given off (Hat-
vegetative pole of the egg where the polar bodies are given off (Hatschek). In no other case in the animal kingdom is this type of egg organization found. The first and second cleavage furrows begin at the vegetative pole, advancing meridionally to the animal pole, dividing the
schek). In no other case in the animal kingdom is this type of egg organ-
ization found. The first and second cleavage furrows begin at the vege-
tative pole, advancing meridionally to the animal pole, dividing the
egg equally. The first furrow corresponds to the median plane of the
egg equally. The first furrow corresponds to the median plane of the
adult and the second to a plane connecting the two long tentacles;
adult and the second to a plane connecting the two long tentacles;
Line 1,392: Line 1,280:
   
   


Fm. 14. A, continuation of Fig. 13. 40~('ell stage of Iftrut; B, g.-1-«it|ul.r of ('ulluum4L
Fm. 14. A, continuation of fig. 13. 40~('ell stage of Iftrut; B, g.-1-«it|ul.r of ('ulluum4L
bialnta. (After Metelmlkoff.)
bialnta. (After Metelmlkoff.)


Line 1,402: Line 1,290:
thus divided symmetrically in two directions, but is elongated in the
thus divided symmetrically in two directions, but is elongated in the
tentacle plane, thus giving the impression that there are two centers of
tentacle plane, thus giving the impression that there are two centers of
symmetry, one in each half, right and left, of the embryo. This impres-
symmetry, one in each half, right and left, of the embryo. This impression is accentuated in the next stage in which eight micromeres in two
sion is accentuated in the next stage in which eight micromeres in two
distinct groups are given off on the concave side (animal half) of the
distinct groups are given off on the concave side (animal half) of the
embryo. The 32-cell stage is reached as each of the eight macromeres
embryo. The 32-cell stage is reached as each of the eight macromeres
Line 1,423: Line 1,310:
no part at all, for the large maeromeres that are the primordia of the
no part at all, for the large maeromeres that are the primordia of the
endoderni are simply overgrown by the micromeres. This process is
endoderni are simply overgrown by the micromeres. This process is
known as epiboly. The epibolic gastrula of Callianira is shown in Fig. 14B.
known as epiboly. The epibolic gastrula of Callianira is shown in fig. 14B.
For further details in the development of ctenophores the student is
For further details in the development of ctenophores the student is
referred to the descriptions of Ziegler, Metchnikoff, and others.
referred to the descriptions of Ziegler, Metchnikoff, and others.
Line 1,440: Line 1,327:
In the extreme cases discoidal cleavage results, which is thus related to
In the extreme cases discoidal cleavage results, which is thus related to
the bilateral types. On the other hand it will later appear that the
the bilateral types. On the other hand it will later appear that the
discoidal type is also related to the superficial type.
discoidal type is also related to the superficial type.


1 . Amphioxus
1 . Amphioxus


As a first type amphioxus may be chosen. It was formerly the custom
As a first type amphioxus may be chosen. It was formerly the custom
to class amphioxus as of the radial type. This is perhaps to be ascribed
to class amphioxus as of the radial type. This is perhaps to be ascribed
to the fact that there is some variability in the behavior of different eggs.
to the fact that there is some variability in the behavior of different eggs.
Line 1,454: Line 1,341:


The egg of amphioxus is clearly bilateral in structure before cleavage.
The egg of amphioxus is clearly bilateral in structure before cleavage.
The animal pole is marked by the second polar body, the first being
The animal pole is marked by the second polar body, the first being
given off before the formation of the vitelline membrane and so lost.
given off before the formation of the vitelline membrane and so lost.
It is said that the animal pole is the point of attachment of the oocyte to
It is said that the animal pole is the point of attachment of the oocyte to
Line 1,465: Line 1,352:
cytoplasm, in which the nucleus lies, although part of this mass extends
cytoplasm, in which the nucleus lies, although part of this mass extends
a little into the posterior half on the ventral side; most of the cytoplasm
a little into the posterior half on the ventral side; most of the cytoplasm
of the posterior half of the egg is well filled with yolk globules. Yolk gran-
of the posterior half of the egg is well filled with yolk globules. Yolk granules also are found in the animal half outside the clear cytoplasmic area.
ules also are found in the animal half outside the clear cytoplasmic area.
The distinction of yolk-free and yolk-laden halves of the egg is indicative
The distinction of yolk-free and yolk-laden halves of the egg is indicative
of its bilateral symmetry. The telolecithal character of the egg is peculiar
of its bilateral symmetry. The telolecithal character of the egg is peculiar
Line 1,496: Line 1,382:
right to left.
right to left.


From this stage on, development becomes irregular, and character-
From this stage on, development becomes irregular, and characteristic differentlations appear. The typical coeloblastula characteristic of
istic differentlations appear. The typical coeloblastula characteristic of


P10. 16 Cleavage of amphioxus (Redrawn from Korschelt and Herder, after
P10. 16 Cleavage of amphioxus (Redrawn from Korschelt and Herder, after
Line 1,540: Line 1,425:


probably the most complete. These eggs have typical determinative
probably the most complete. These eggs have typical determinative
cleavage, with definite orrgamforming regions which are recognizable by
cleavage, with definite orrgamforming regions which are recognizable by
«color difference of the cytoplasm.
«color difference of the cytoplasm.


The newly extruded egg surrounded by a layer of test has a conical
The newly extruded egg surrounded by a layer of test has a conical
layer of texoplasm in which is uniformly distributed a yellow pigment.
layer of texoplasm in which is uniformly distributed a yellow pigment.
Soon after fertilization the polar bodies are given off and peculiar rear-
Soon after fertilization the polar bodies are given off and peculiar rearrangements of substance take place. About five minutes after fertiliza
rangements of substance take place. About five minutes after fertiliza-
 
    
    


F
F


FIG. 15. The egg of Cynthia partzta. (After Conklm.)
fiG. 15. The egg of Cynthia partzta. (After Conklm.)


A. unfertilized em: with germinal vesicle, central gray yolk 111.158, peripheral yellow
A. unfertilized em: with germinal vesicle, central gray yolk 111.158, peripheral yellow
protoplasm, and test cells; B, five minutes after fertilization showing streaming of yellow
protoplasm, and test cells; B, five minutes after fertilization showing streaming of yellow
protoplasm to vegetative pole; (‘, streaming of yellow protoplasm nearly completed,
protoplasm to vegetative pole; (‘, streaming of yellow protoplasm nearly completed,
clear protoplasm lies beneath it and is visible at its upper edge. On the top of the cm:
clear protoplasm lies beneath it and is visible at its upper edge. On the top of the cm:
the germinal vesicle is still seen; D, the light creseentic area at the vegetative pole repre-
the germinal vesicle is still seen; D, the light creseentic area at the vegetative pole represents the male pronueleus; the unstippled area is the gray central yolk mass of A; E,
sents the male pronueleus; the unstippled area is the gray central yolk mass of A; E,
polyspermic egg: F. formation of yellow crescent (heavily stippled) with the light gray
polyspermic egg: F. formation of yellow crescent (heavily stippled) with the light gray
trescent above it.
trescent above it.


tion the yellow pigment, mesoplasm, may be seen streaming toward the
tion the yellow pigment, mesoplasm, may be seen streaming toward the
vegetal pole, leaving behind the gray yolk mass, endoplasm, which fills
vegetal pole, leaving behind the gray yolk mass, endoplasm, which fills
most of the cytoplasm of the egg. The yellow mesoplasm arranges itself
most of the cytoplasm of the egg. The yellow mesoplasm arranges itself
in a crescent in the posterior half and will, later in development, give rise
in a crescent in the posterior half and will, later in development, give rise
Line 1,575: Line 1,457:


the animal pole. It IS the neurochordal anlage (or fundainent from which
the animal pole. It IS the neurochordal anlage (or fundainent from which
will arise the neural canal and notochord). The animal pole is sui-
will arise the neural canal and notochord). The animal pole is suiirounded by ectoplasm from which ectoderm arises, and the vegetative
irounded by ectoplasm from which ectoderm arises, and the vegetative
Iby endoplasm producing endoderm.
Iby endoplasm producing endoderm.


The first division, a meridional one, divides the egg and likewise each
The first division, a meridional one, divides the egg and likewise each
of the oigan-foiming rogiorns into «two equal halves Since tliere is but a
of the oigan-foiming rogiorns into «two equal halves Since tliere is but a


FIG 10 A, continuation of Fig 18 B, showing aggregriiion of test cells over the cres-
fiG 10 A, continuation of fig 18 B, showing aggregriiion of test cells over the crescent and the protrusion of the ehorion, (‘, 2-cell stage with formative substances outlined
cent and the protrusion of the ehorion, (‘, 2-cell stage with formative substances outlined
Uniform stipples, volk, light stipples, clear protoplisni eiilarged and extended toward
Uniform stipples, volk, light stipples, clear protoplisni eiilarged and extended toward
the animal pole, grouped stipples, yellow crescent m Lterial
the animal pole, grouped stipples, yellow crescent m Lterial
Line 1,589: Line 1,469:
single plane which can do this it is evident that the cleavage is bilateral
single plane which can do this it is evident that the cleavage is bilateral
in character. The separation of the egg substance into organ—forming
in character. The separation of the egg substance into organ—forming
regions, which had started during the first cleavage, is completed now,
regions, which had started during the first cleavage, is completed now,
although it must be recognized that it is never as sharp as the boundaries
although it must be recognized that it is never as sharp as the boundaries
of the regions shown in_the usual diagrams. It is not possible, however,
of the regions shown in_the usual diagrams. It is not possible, however,
Line 1,606: Line 1,486:
In each case the right blastomere is indicated by underlining the letter
In each case the right blastomere is indicated by underlining the letter


FIG. 20. Cleavage of Cynthia (Redmwn from Korschclt and H0|dOf, after Conklm )
fiG. 20. Cleavage of Cynthia (Redmwn from Korschclt and H0|dOf, after Conklm )


A. 4-cell stage from left side, B, from animal pole, C‘, 8-coll stage from left side, I), from
A. 4-cell stage from left side, B, from animal pole, C‘, 8-coll stage from left side, I), from
animal pole.
animal pole.


as 51} or E‘. The exponent 3 indicates that this is the third cell genera-
as 51} or E‘. The exponent 3 indicates that this is the third cell generation, counting the single-celled egg as 1. The division of A3 results in two
tion, counting the single-celled egg as 1. The division of A3 results in two
blastomeres which are designated A‘ 1 and A4 2. The exponent 4 indicates
blastomeres which are designated A‘ 1 and A4 2. The exponent 4 indicates
the fourth cell generation, and the 1 or 2 after the period shows that it
the fourth cell generation, and the 1 or 2 after the period shows that it
Line 1,639: Line 1,518:


A B C
A B C
FIG. ‘.21. Later stages of ('ymhia cleavage. (Redrawn from Korschelt and Heider, after
fiG. ‘.21. Later stages of ('ymhia cleavage. (Redrawn from Korschelt and Heider, after
Conklin.)
Conklin.)


Line 1,656: Line 1,535:
From here on all the cells of the animal half produce only eetoderm
From here on all the cells of the animal half produce only eetoderm
cells. The cells of the vegetative half are more diversely differentiated.
cells. The cells of the vegetative half are more diversely differentiated.
B“-7 and Q“-7 consist only of yellow protoplasm and are purely meso-
B“-7 and Q“-7 consist only of yellow protoplasm and are purely mesodermal; A”, A“, and B“ with their mates of the right side are almost
dermal; A”, A“, and B“ with their mates of the right side are almost
purely endodermal. The neurochordal cells A“ and A“ lie next to them
purely endodermal. The neurochordal cells A“ and A“ lie next to them
anteriorly, and the crescentie mesoderm anlage, B”, B”, and B“,
anteriorly, and the crescentie mesoderm anlage, B”, B”, and B“,
Line 1,668: Line 1,546:
42 H()L()BLAS'l‘IC TYPES OF CLII«‘.AV.A'(:I«:
42 H()L()BLAS'l‘IC TYPES OF CLII«‘.AV.A'(:I«:


are segregated into definite cells from wvlficln arcise the organs of the
are segregated into definite cells from wvlficln arcise the organs of the
lafterfembryo in the characteristic ascidian manner.
lafterfembryo in the characteristic ascidian manner.


Line 1,713: Line 1,591:
3. Vertebrates
3. Vertebrates


The cleavage of the vertebrates is not usually of a determinative char-
The cleavage of the vertebrates is not usually of a determinative character as is that of the ascidians, and there are many variations in the
acter as is that of the ascidians, and there are many variations in the
characters it presents throughout the different groups. In general, however, they may all be referred to the bilateral type or derived from it,
characters it presents throughout the different groups. In general, how-
although the very considerable amounts of yolk present in the teloVER'1‘EBRA'l‘ES 43
ever, they may all be referred to the bilateral type or derived from it,
although the very considerable amounts of yolk present in the telo-
VER'1‘EBRA'l‘ES 43


lecithal eggs bring about important modifications in the modes of
lecithal eggs bring about important modifications in the modes of
cleavage. This account leaves out of consideration the cleavage of
cleavage. This account leaves out of consideration the cleavage of
mammals which is modified in an extreme manner in spite of the lack
mammals which is modified in an extreme manner in spite of the lack
eofiyolk. Several groups of vertebrates have discoidal cleavage; this type,
eofiyolk. Several groups of vertebrates have discoidal cleavage; this type,


FIG. ‘.32. Cleavage of the frog egg. A, B. C, D, 2-. 4-. 8-. 32—eell stages; E. lutor cleavage
fiG. ‘.32. Cleavage of the frog egg. A, B. C, D, 2-. 4-. 8-. 32—eell stages; E. lutor cleavage
stage: 1“. dorsal lip of blastopore; G. circular blastoporc.
stage: 1“. dorsal lip of blastopore; G. circular blastoporc.


Line 1,738: Line 1,613:


brown or blackish pigment distinguishes the animal from the vegetative
brown or blackish pigment distinguishes the animal from the vegetative
portions of the egg. About the vegetative pole extending perhaps one-
portions of the egg. About the vegetative pole extending perhaps onethird upwards is a white region which contains the material that will
third upwards is a white region which contains the material that will
later go to form the endoderm.
later go to form the endoderm.


Line 1,749: Line 1,623:
   
   


FIG 23 Cleavage of the frog egg seen from the animal or pigmented pole A. B, C. 4-,
fiG 23 Cleavage of the frog egg seen from the animal or pigmented pole A. B, C. 4-,
8-, 32-cell stages
8-, 32-cell stages


In the frog there is considerable variation as to the relations of the
In the frog there is considerable variation as to the relations of the
cleavage planes. Brachet found in 48 per cent of the cases which he
cleavage planes. Brachet found in 48 per cent of the cases which he
observed that the first cleavage plane and the median plane coincided;
observed that the first cleavage plane and the median plane coincided;
in another 20 per cent the deviation was not more than 20 degrees.
in another 20 per cent the deviation was not more than 20 degrees.
However, the bilaterality of the egg may often be shown to be indepen-
However, the bilaterality of the egg may often be shown to be independent of the cleavage figures. In certain amphibian eggs it has been shown
dent of the cleavage figures. In certain amphibian eggs it has been shown
that there is present in both fertilized and unfertilized eggs a bilateral
that there is present in both fertilized and unfertilized eggs a bilateral
arrangement of part of the egg substance, the so-called “gray crescent,”
arrangement of part of the egg substance, the so-called “gray crescent,”
Line 1,763: Line 1,636:
portion, recalling the condition in ascidians.
portion, recalling the condition in ascidians.


The first cleavage divides the egg meridionally, the formation of the
The first cleavage divides the egg meridionally, the formation of the
VER’l‘EBRA'l‘ES 45
VER’l‘EBRA'l‘ES 45


Line 1,774: Line 1,647:
much more numerous. In the fifth and sixth cleavages only the small
much more numerous. In the fifth and sixth cleavages only the small


FIG. 24. Sections through blastulue up to the beginning of gastrulation in the frog“;
fiG. 24. Sections through blastulue up to the beginning of gastrulation in the frog“;
egg. (B, (‘, D, after Ziegler) These show the clmracter of the octoderm and endoderm
egg. (B, (‘, D, after Ziegler) These show the clmracter of the octoderm and endoderm
cells, the nature of the blastoeoelc, and the first sign of gastrular invagmation.
cells, the nature of the blastoeoelc, and the first sign of gastrular invagmation.


upper cirelets of cells are divided and even in those disturbances in the
upper cirelets of cells are divided and even in those disturbances in the
Line 1,789: Line 1,662:
46 HOLOBLASTIC TYPES OF CLEAVAGE
46 HOLOBLASTIC TYPES OF CLEAVAGE


extended laterally, but in places it is reduced to a mere slit as develop-
extended laterally, but in places it is reduced to a mere slit as development proceeds. When the fully formed blastula is reached in the frog, a
ment proceeds. When the fully formed blastula is reached in the frog, a
difference, which is characteristic between vertebrates and invertebrates,
difference, which is characteristic between vertebrates and invertebrates,
becomes apparent in that the wall consists of many cells. In the inverte-
becomes apparent in that the wall consists of many cells. In the invertebrates the octoderm and later the endoderm consist of a single layer of
brates the octoderm and later the endoderm consist of a single layer of
columnar or cuboidal epithelium, but in the vertebrates these germ
columnar or cuboidal epithelium, but in the vertebrates these germ
layers are of several cells in thickness and many of the cells do not lie
layers are of several cells in thickness and many of the cells do not lie
Line 1,805: Line 1,676:
in agreement with the Ascaris type.
in agreement with the Ascaris type.


The egg is small and practically yolk—free, and no evidences of differ-
The egg is small and practically yolk—free, and no evidences of differentiation are visible in the uncleaved egg, nor of relation between cleavage planes and polar bodies, but as soon as the 4-cell condition is reached
entiation are visible in the uncleaved egg, nor of relation between cleav-
age planes and polar bodies, but as soon as the 4-cell condition is reached
the orientation is complete. In addition, however, to the differentiation
the orientation is complete. In addition, however, to the differentiation
which is expressed in the. orientation of the 4-cell stage, another mark
which is expressed in the. orientation of the 4-cell stage, another mark
of differentiation is evident in the nuclear processes. This is the chro-
of differentiation is evident in the nuclear processes. This is the chromatin diminution which occurs in the cells which are somatic in character, and is lacking in the prospective germ cell line, that is, in P1, P2,
matin diminution which occurs in the cells which are somatic in char-
acter, and is lacking in the prospective germ cell line, that is, in P1, P2,
P3, P4, and G and G1.
P3, P4, and G and G1.


The first cleavage plane results in the formation of two cells somewhat
The first cleavage plane results in the formation of two cells somewhat
unequal. Of these the larger is designated as S1 01' AB and the smaller
unequal. Of these the larger is designated as S1 01' AB and the smaller
as P1. S, is shown by its subsequent development to contain only mate-
as P1. S, is shown by its subsequent development to contain only material which is to be distributed to somatic cells, while the P1 contains
rial which is to be distributed to somatic cells, while the P1 contains
materials which will contribute to both soma and germ plasm. The
materials which will contribute to both soma and germ plasm. The
next cleavage planes are not parallel to each other, for the spindle of
next cleavage planes are not parallel to each other, for the spindle of
the AB cell lies parallel to the first division plane, but that of the P1
the AB cell lies parallel to the first division plane, but that of the P1
cell is perpendicular to it. Thus there arises a T-shaped figure, the top
cell is perpendicular to it. Thus there arises a T-shaped figure, the top
being formed by the cells A and B and the stem at first by P1, which
being formed by the cells A and B and the stem at first by P1, which
divides more slowly than the S1 cell, and later by the derivatives, cells
divides more slowly than the S1 cell, and later by the derivatives, cells
S2 and Pa. Subsequently the P2 cell shifts posteriorly so that it comes
S2 and Pa. Subsequently the P2 cell shifts posteriorly so that it comes
to lie in contact with both S2 and B, forming a rhomboidal figure.
to lie in contact with both S2 and B, forming a rhomboidal figure.


Now the bilateral character of the embryo becomes apparent. The
Now the bilateral character of the embryo becomes apparent. The
Line 1,834: Line 1,700:
divides into a on the right side and 0: on the left, and B into b and 6.
divides into a on the right side and 0: on the left, and B into b and 6.
The embryo for a brief time, therefore, is in a 6-celled condition, but
The embryo for a brief time, therefore, is in a 6-celled condition, but
the division of the two ventral cells follows shortly, the planes of divi-
the division of the two ventral cells follows shortly, the planes of diviNEMATODES 47
NEMATODES 47


sion lying perpendicular to the median plane. The 8-cell stage, therefore,
sion lying perpendicular to the median plane. The 8-cell stage, therefore,
consists of 9. plate of four dorsal ectomeres (two right and two left) and
consists of 9. plate of four dorsal ectomeres (two right and two left) and


Flu. 2.3. (‘leuvage of Ascaris ntcgalocephala. (Rt.-drawn from Korschelt and Heider after
flu. 2.3. (‘leuvage of Ascaris ntcgalocephala. (Rt.-drawn from Korschelt and Heider after
Bovcri.)
Bovcri.)


Line 1,851: Line 1,716:
8. row of four ventral cells slightly curved. S2 (EM St) divides into M St
8. row of four ventral cells slightly curved. S2 (EM St) divides into M St
and E, the former being the anlage of mesoderm and stomodaeum and
and E, the former being the anlage of mesoderm and stomodaeum and
the latter that of the primitive endoderm. P2 divides into S3, an ecto-
the latter that of the primitive endoderm. P2 divides into S3, an ecto48 HOLOBLASTIC TYPES OF CLEAVAGE
48 HOLOBLASTIC TYPES OF CLEAVAGE


mesoderm cell, and P3, a continuation of the germ line. In this 8-cell
mesoderm cell, and P3, a continuation of the germ line. In this 8-cell
Line 1,862: Line 1,726:
occurs a process known as chromatin diminution by means of which
occurs a process known as chromatin diminution by means of which


Flu. 26. Continuation of Fig. 25.
flu. 26. Continuation of fig. 25.


A. 6-cell stage. Blastomcres A and B divided into a and a. and b and Li; B. 7-cell stage
A. 6-cell stage. Blastomcres A and B divided into a and a. and b and Li; B. 7-cell stage
Line 1,869: Line 1,733:


the thickened ends of the chromosomes are left behind in the cytoplasm
the thickened ends of the chromosomes are left behind in the cytoplasm
as the telophases of the cleavage divisions take place. Chromatin dimi-
as the telophases of the cleavage divisions take place. Chromatin diminution never occurs in those blastomeres which are antecedent to the
nution never occurs in those blastomeres which are antecedent to the
germ cells of the later stages; but every blastomere which will produce
germ cells of the later stages; but every blastomere which will produce
only somatic cells goes through the process of chromatin diminution
only somatic cells goes through the process of chromatin diminution
Line 1,930: Line 1,793:
CELL LINEAGE OF ASCAEIS FROM DESCRIPTIONS OF ZUR HTRASSEN AND BOVERI
CELL LINEAGE OF ASCAEIS FROM DESCRIPTIONS OF ZUR HTRASSEN AND BOVERI


line continues for five cell generations, at the end of which time no
line continues for five cell generations, at the end of which time no
further somatic cells are produced from this line and the cells rest from
further somatic cells are produced from this line and the cells rest from
further division until the organism has reached a considerable degree
further division until the organism has reached a considerable degree
Line 1,937: Line 1,800:
of maturity. The distinction which is made possible by following through
of maturity. The distinction which is made possible by following through
the chromatin diminution between germ plasm and soma in these early
the chromatin diminution between germ plasm and soma in these early
blastomeres of Ascaris has been of great theoretical significance and
blastomeres of Ascaris has been of great theoretical significance and
often referred to as evidence in support of the theory of germinal con-
often referred to as evidence in support of the theory of germinal continuity. In this connection it is further discussed in Part Two, Chapter I.
tinuity. In this connection it is further discussed in Part Two, Chapter I.
The process will be more clearly understood by referring to that discussion and also to the table showing the cleavage of Ascaris which
The process will be more clearly understood by referring to that dis-
cussion and also to the table showing the cleavage of Ascaris which
appears herewith.
appears herewith.


Line 1,950: Line 1,811:
and its development is not fully understood. It is to a certain extent
and its development is not fully understood. It is to a certain extent
intermediate between the bilateral and the spiral types. The retifers
intermediate between the bilateral and the spiral types. The retifers
have no cleavage cavity or gastrula cavity. (That is, they have stereo-
have no cleavage cavity or gastrula cavity. (That is, they have stereoblastulae and stereogastrulae.) The resemblance between the developmental conditions of annelids and rnolluscs and of the rotifers is perhaps
blastulae and stereogastrulae.) The resemblance between the develop-
mental conditions of annelids and rnolluscs and of the rotifers is perhaps
not so surprising in view of the fact that all these groups pass through
not so surprising in view of the fact that all these groups pass through
larval stages which are_ morphologically trochophores.
larval stages which are_ morphologically trochophores.


Although the character of the cleavage of rotifers is sufiieiently bi-
Although the character of the cleavage of rotifers is sufiieiently bilateral to be placed with other forms of this type, the peculiarities are
lateral to be placed with other forms of this type, the peculiarities are
such that it seems unnecessary to follow out the details for these forms.
such that it seems unnecessary to follow out the details for these forms.


Line 1,964: Line 1,822:
Spiral cleavage is characteristic of polyelads, nemerteans, polychaetes
Spiral cleavage is characteristic of polyelads, nemerteans, polychaetes
and many molluscs. Eggs which cleave spirally are with few exceptions
and many molluscs. Eggs which cleave spirally are with few exceptions
well filled with yolk and therefore segment unequally. Frequently the
well filled with yolk and therefore segment unequally. Frequently the
inequality is so great that only a small cap of cells comprising the ecto-
inequality is so great that only a small cap of cells comprising the ectoderm lies on the large endodermal cells with a consequent more or less
derm lies on the large endodermal cells with a consequent more or less
complete reduction of the cleavage cavity. This condition also results
complete reduction of the cleavage cavity. This condition also results
in a much modified type of gastrulation from that which is character-
in a much modified type of gastrulation from that which is characteristic of holoblastic eggs.
istic of holoblastic eggs.


Nevertheless it is not difficult to derive the spiral type of cleavage
Nevertheless it is not difficult to derive the spiral type of cleavage
Line 1,978: Line 1,834:
with each other what is known as a polar furrow, as do B and D at the
with each other what is known as a polar furrow, as do B and D at the
vegetal pole. But the polar furrows at the two poles are perpendicular
vegetal pole. But the polar furrows at the two poles are perpendicular
to each other. The departure from the radial type becomes clearly dis-
to each other. The departure from the radial type becomes clearly distinguished in the third cleavage, owing to an oblique shift in spindle
tinguished in the third cleavage, owing to an oblique shift in spindle
direction so that when viewed from the animal pole the upper end of
direction so that when viewed from the animal pole the upper end of
SPIRAL CLEAVAG E 5 1
SPIRAL CLEAVAG E 5 1
Line 1,994: Line 1,849:
   
   


FIG. 27. (‘nmp:mLti\'o diugrzuns of radial and spiral cle:tvn.ge. (Redrawn from Korsehelt
fiG. 27. (‘nmp:mLti\'o diugrzuns of radial and spiral cle:tvn.ge. (Redrawn from Korsehelt
and Helder.)
and Helder.)


A, mdinl type; B, spiral type in third cleavage; C, D, rudial and the spiral type respec-
A, mdinl type; B, spiral type in third cleavage; C, D, rudial and the spiral type respectively in fourth cleavage.
tively in fourth cleavage.


position with the lower (Fig. 30 c, e). The upper quartette of cells,
position with the lower (fig. 30 c, e). The upper quartette of cells,
called ectomeres, appears to be given off spirally from the lower endo-
called ectomeres, appears to be given off spirally from the lower endomeres, although of course speaking strictly it is not correct to think of
meres, although of course speaking strictly it is not correct to think of
these cells in this manner, for both quartettes are composed merely of
these cells in this manner, for both quartettes are composed merely of
the daughter cells of the preceding 4-cell stage. This third cleavage is
the daughter cells of the preceding 4-cell stage. This third cleavage is
Line 2,010: Line 1,863:


The fourth cleavage ‘spindles are now formed in accordance with the
The fourth cleavage ‘spindles are now formed in accordance with the
general tendency expressed by the so-called alternation rule that suc-
general tendency expressed by the so-called alternation rule that suc52 HOLOBLASTIC TYPES OF CLEAVAGE
52 HOLOBLASTIC TYPES OF CLEAVAGE


cessive cleavage planes tend to intersect each other at right angles. The
cessive cleavage planes tend to intersect each other at right angles. The
spindles, therefore, take up such positions that the next divisions are laco-
spindles, therefore, take up such positions that the next divisions are laco
 
@®
@®
@@
@@


FIG. 28. (‘ontinuutinn of Fig. 27. Polar views.
fiG. 28. (‘ontinuutinn of fig. 27. Polar views.


A, 13. 8- and 113-0011 stages rarlinl type; (3, I), third and fourth cleavages, spiral typo;
A, 13. 8- and 113-0011 stages rarlinl type; (3, I), third and fourth cleavages, spiral typo;
E. 1". 8- and 16-cell stages spiral typo.
E. 1". 8- and 16-cell stages spiral typo.


tropic, that is in the direction of left-handed spirals. This alternation con-
tropic, that is in the direction of left-handed spirals. This alternation continues in regular order until four quartettes have been produced, and meanwhile each of the cells divides according to the same general laws of
tinues in regular order until four quartettes have been produced, and mean-
while each of the cells divides according to the same general laws of
E
E


FIG. 29. Cleavage of Crcpzdula. (Redrawn from (‘onklin.)
fiG. 29. Cleavage of Crcpzdula. (Redrawn from (‘onklin.)


A. resting stage after the first cleavage; blastomeres flattening against each other and
A. resting stage after the first cleavage; blastomeres flattening against each other and
nuclei. asters, and protoplasmic area rotated dexiotropically; B, anaphase of the second
nuclei. asters, and protoplasmic area rotated dexiotropically; B, anaphase of the second
cleavage. The shift which will result in the formation of a polar furrow just beneath the
cleavage. The shift which will result in the formation of a polar furrow just beneath the
Line 2,039: Line 1,888:
54 HOLOBLASTIC TYPES Oli‘ CLEAVAGE
54 HOLOBLASTIC TYPES Oli‘ CLEAVAGE


cleavage. Since the blastomeres of spirally cleaving eggs are always un-
cleavage. Since the blastomeres of spirally cleaving eggs are always unequal, differences occurring even within a quartette as well as between
equal, differences occurring even within a quartette as well as between
different quartettes, it follows that the cleavages cannot long remain
different quartettes, it follows that the cleavages cannot long remain
entirely regular, for differentiation is rapidly taking place.
entirely regular, for differentiation is rapidly taking place.


Owing to the fact that spiral cleavage is one of the most markedly
Owing to the fact that spiral cleavage is one of the most markedly
determinative in character, this form presents an unusually good ex-
determinative in character, this form presents an unusually good example for the study of cell lineage. To bring out the relationships between
ample for the study of cell lineage. To bring out the relationships between
cells it is found to be necessary to have a definite terminology and nomenclature for the blastomeres of eggs of this type. The system adopted by
cells it is found to be necessary to have a definite terminology and nomen-
clature for the blastomeres of eggs of this type. The system adopted by
Conklin for expressing the relationships in the case of Crepidula is now
Conklin for expressing the relationships in the case of Crepidula is now
in general use. Certain special cells should be given special names, but
in general use. Certain special cells should be given special names, but
Line 2,055: Line 1,901:
previously introduced by Wilson to describe the cell lineage of Nereis.
previously introduced by Wilson to describe the cell lineage of Nereis.


In the nomenclature used in Crepidula Conklin designated the quar-
In the nomenclature used in Crepidula Conklin designated the quartettes of cells by coefficients: “e.g., the first quartette of micromeres
tettes of cells by coefficients: “e.g., the first quartette of micromeres
and all their derivatives are designated by the coefficient 1 (la, ld,
and all their derivatives are designated by the coefficient 1 (la, ld,
la‘-2, 1c”, etc.), the second quartette and its progeny by the coefficient
la‘-2, 1c”, etc.), the second quartette and its progeny by the coefficient
Line 2,065: Line 1,910:
because the distinctions afford the basis for tracing the cell lineage in
because the distinctions afford the basis for tracing the cell lineage in
the more advanced stages. The coefficients designating the quartettes
the more advanced stages. The coefficients designating the quartettes
are retained in all subsequent stages and the further cell lineage indi-
are retained in all subsequent stages and the further cell lineage indicated by exponents. The cell la divides to form la‘ and la“. Then further
cated by exponents. The cell la divides to form la‘ and la“. Then further
exponents are added for each new cell generation always retaining the
exponents are added for each new cell generation always retaining the
complete designation of the parent cell. The cell la“ produces la?‘ and
complete designation of the parent cell. The cell la“ produces la?‘ and
Line 2,077: Line 1,921:
similarly in the other quadrants. Each successive macromere receives
similarly in the other quadrants. Each successive macromere receives
a new coeflicient as it divides into a new macromere and a micromere;
a new coeflicient as it divides into a new macromere and a micromere;
thus 1A produces 2A and 2a; 2A in turn 3A and 3a. Numerical coeffi-
thus 1A produces 2A and 2a; 2A in turn 3A and 3a. Numerical coefficients are used to designate successive quartettes, while the exponents
cients are used to designate successive quartettes, while the exponents
indicate the products of their division. Cleavage is dexiotropic, or
indicate the products of their division. Cleavage is dexiotropic, or
oblique to the right, if the spindle direction is turned clockwise from the
oblique to the right, if the spindle direction is turned clockwise from the
axis of the egg, and laeotropic when turned to the left.
axis of the egg, and laeotropic when turned to the left.


By reference to the accompanying table the relationships of the blasto-
By reference to the accompanying table the relationships of the blastofiG. 30. first cleavage of Crezridula plana. (After Conklin.)
FIG. 30. First cleavage of Crezridula plana. (After Conklin.)


A, approach of sperm and egg pronuclei; B, nuclei in contact, asters and centrosomcs
A, approach of sperm and egg pronuclei; B, nuclei in contact, asters and centrosomcs
Line 2,090: Line 1,932:
two cleavage centrosomes; chromosomes aggregating on the spindle; other granules dis—
two cleavage centrosomes; chromosomes aggregating on the spindle; other granules dis—
solving. Sphere substance increased in size and radiating into the cytoplasm; D, prophase
solving. Sphere substance increased in size and radiating into the cytoplasm; D, prophase
of the first cleavage. Chromatin granules assuming their relation to the spindle fibers;
of the first cleavage. Chromatin granules assuming their relation to the spindle fibers;
E, metaphase of the first cleavage; F, telophase of the first cleavage; spindle axis bending.
E, metaphase of the first cleavage; F, telophase of the first cleavage; spindle axis bending.
Nuclei of left cell partially divided indicating origin of upper part from egg pronucleus
Nuclei of left cell partially divided indicating origin of upper part from egg pronucleus
from female and lower from-the male.
from female and lower from-the male.
Line 2,100: Line 1,942:


In general the 8-cell stage of an egg with spiral cleavage consists of
In general the 8-cell stage of an egg with spiral cleavage consists of
four micromeres, 1a, 1b, 1c, 1d about the animal pole, and four macro-
four micromeres, 1a, 1b, 1c, 1d about the animal pole, and four macromeres, 1A, 1B, 1C, ID, at the vegetative pole. In most cases the third
meres, 1A, 1B, 1C, ID, at the vegetative pole. In most cases the third
cleavage is dexiotropic. The 16-cell stage is reached by a aeotropic
cleavage is dexiotropic. The 16-cell stage is reached by a aeotropic
division and consists of the quartettes of micromeres, la‘,1b‘,lc’,1d‘,
division and consists of the quartettes of micromeres, la‘,1b‘,lc’,1d‘,
Line 2,107: Line 1,948:
There is an intermediate condition in eggs having spiral cleavage in
There is an intermediate condition in eggs having spiral cleavage in
which there are actually twelve cells only, for the second quartette,
which there are actually twelve cells only, for the second quartette,
2a to 2d, is budded off before the division of the first, 1a to 1d, is com-
2a to 2d, is budded off before the division of the first, 1a to 1d, is completed. There is a similar lack of regularity of division in other stages,
pleted. There is a similar lack of regularity of division in other stages,
some quartettes dividing while others hold back even to the extent that
some quartettes dividing while others hold back even to the extent that
some cells may be an entire cell generation behind others. In the transl-
some cells may be an entire cell generation behind others. In the transl
 
A B
A B
Fm. 31. Cleavage of Trochus. (Redmwn from Korsehelt and Heider, after Robert.)
Fm. 31. Cleavage of Trochus. (Redmwn from Korsehelt and Heider, after Robert.)
Line 2,121: Line 1,960:


The division producing the 32-cell stage is usually a dexiotropic one.
The division producing the 32-cell stage is usually a dexiotropic one.
The cells of the first quartette receive their second exponent, la‘ becom-
The cells of the first quartette receive their second exponent, la‘ becoming la" and la”; those of the second quartette their first, 2a‘ and 2a’;
ing la" and la”; those of the second quartette their first, 2a‘ and 2a’;
and the four macromeres divide, producing 3A and 3a (using the A
and the four macromeres divide, producing 3A and 3a (using the A
quadrant as a sample). There are now sixteen descendants of the first
quadrant as a sample). There are now sixteen descendants of the first
Line 2,129: Line 1,967:
The 32-cell stage brings to the spiral type of cleavage a certain degree
The 32-cell stage brings to the spiral type of cleavage a certain degree
of completeness, for three successive divisions have produced three
of completeness, for three successive divisions have produced three
quartettes of ectomeres that represent chiefly ectoderm-forming cells,
quartettes of ectomeres that represent chiefly ectoderm-forming cells,
although larval mesenehyme is also produced from some of the deriva-
although larval mesenehyme is also produced from some of the derivatives of the second quartette. The four macromeres subsequently produce two more quartettes of micromeres and are in general endodermforming cells. An exception is found in the cell 4d in the higher forms
tives of the second quartette. The four macromeres subsequently pro-
duce two more quartettes of micromeres and are in general endoderm-
forming cells. An exception is found in the cell 4d in the higher forms
having spiral cleavage, for it is the parent cell of the mesoderm.
having spiral cleavage, for it is the parent cell of the mesoderm.
SPIRAL CLEAVAGE 57
SPIRAL CLEAVAGE 57
Line 2,145: Line 1,980:


Spiral cleavage, as already indicated, occurs in several of the great
Spiral cleavage, as already indicated, occurs in several of the great
divisions of the animal kingdom. It first appears in the polyclads. Our
divisions of the animal kingdom. It first appears in the polyclads. Our
knowledge of the cleavage of this group is based especially upon the
knowledge of the cleavage of this group is based especially upon the


Line 2,157: Line 1,992:


study of Discocoelis by Lang, of Leploplana by Wilson and of Pltmocera
study of Discocoelis by Lang, of Leploplana by Wilson and of Pltmocera
by Surface. Cleavage in these forms follows the general scheme as previ-
by Surface. Cleavage in these forms follows the general scheme as previously given for all of its main features. There are variations due to
ously given for all of its main features. There are variations due to
differences in the size of the blastomeres and other such factors, but the
differences in the size of the blastomeres and other such factors, but the
general plan as described is entirely applicable here. There are certain
general plan as described is entirely applicable here. There are certain
features in the development of these forms which suggest a relationship
features in the development of these forms which suggest a relationship
to the cleavage of the other flatworms, but there are a great many points
to the cleavage of the other flatworms, but there are a great many points
of agreement between the method of cleavage of polyclads on one side
of agreement between the method of cleavage of polyclads on one side
and that of the annelids and inolluscs on the other, and it has been held
and that of the annelids and inolluscs on the other, and it has been held
Line 2,168: Line 2,002:
58 HOLOBLASTIC TYPES OF CLEAVAGE
58 HOLOBLASTIC TYPES OF CLEAVAGE


to the early development of these forms. The points on which the agree-
to the early development of these forms. The points on which the agreement is observed are sufficiently important that they seem to indicate
ment is observed are sufficiently important that they seem to indicate
more than a mere adaptive coincidence on the part of the previous types
more than a mere adaptive coincidence on the part of the previous types
of the two groups. The formation of three ectomere quartettes which
of the two groups. The formation of three ectomere quartettes which
Line 2,182: Line 2,015:
and indeed they are almost diagrammatic in the regularity which they
and indeed they are almost diagrammatic in the regularity which they
show. The studies of Coe on Micrura, of C. B. Wilson on Cerebratulus
show. The studies of Coe on Micrura, of C. B. Wilson on Cerebratulus
lacteus, and of Zeleny on Cerebratulus marginalis are sufficient to estab-
lacteus, and of Zeleny on Cerebratulus marginalis are sufficient to establish the important features of cleavage in this type. The work on these
lish the important features of cleavage in this type. The work on these
forms as well as upon others of this group is so similar to that described
forms as well as upon others of this group is so similar to that described
for other cases that it does not seem necessary to consider it in detail
for other cases that it does not seem necessary to consider it in detail
although it is important and of excellent character.
although it is important and of excellent character.


Spiral cleavage is especially developed among the polychaetous an-
Spiral cleavage is especially developed among the polychaetous annelids. Of special importance are the studies of E. B. Wilson on Nerezls-,
nelids. Of special importance are the studies of E. B. Wilson on Nerezls-,
of Child on Arenicola, as well as the observations of Mead, Treadwell,
of Child on Arenicola, as well as the observations of Mead, Treadwell,
Nelson, Torrey, and Gerould on other forms of polychaetes. The later
Nelson, Torrey, and Gerould on other forms of polychaetes. The later
stages have been made more clear by the work of Woltcreck on Poly-
stages have been made more clear by the work of Woltcreck on Polygordius. The cleavage of Arenicola, which leads to the development of
gordius. The cleavage of Arenicola, which leads to the development of
the trochophore larvae in its fundamental features, corresponds to that
the trochophore larvae in its fundamental features, corresponds to that
of the general type already described. The cleavage axis running from
of the general type already described. The cleavage axis running from
animal to vegetative pole corresponds to the chief axis of the troeho-
animal to vegetative pole corresponds to the chief axis of the troehophore larva, and although the first cleavages present slight differences
phore larva, and although the first cleavages present slight differences
in order and in the angles they make with the egg axis the result is the
in order and in the angles they make with the egg axis the result is the
same as in the general type, for by the time of the 8- and 16-cell stages
same as in the general type, for by the time of the 8- and 16-cell stages
the normal relationships have been returned although there are certain
the normal relationships have been returned although there are certain
marks of size differentiation among the various blastomeres. The dif-
marks of size differentiation among the various blastomeres. The differences which exist between the cell lineage of Arenicola and that of the
ferences which exist between the cell lineage of Arenicola and that of the
type form are minor differences only. There are, however, some special
type form are minor differences only. There are, however, some special
features about the cleavage of the annelids which deserve mention. In
features about the cleavage of the annelids which deserve mention. In
the animal half of the egg there presently develop certain configurations
the animal half of the egg there presently develop certain configurations
which are especially useful in homologizing the blastomeres of these
which are especially useful in homologizing the blastomeres of these
forms with those of the very similarly cleaving eggs of the gastropod
forms with those of the very similarly cleaving eggs of the gastropod
Line 2,212: Line 2,040:
chief characteristic of the embryo for the stages immediately following
chief characteristic of the embryo for the stages immediately following
the 64-091] condition. As will be seen by consulting the accompanying
the 64-091] condition. As will be seen by consulting the accompanying
FIG 33 ('le.nu.go stage of Anmcula cnstata (RC-drawn from Korichelt and Helder,
fiG 33 ('le.nu.go stage of Anmcula cnstata (RC-drawn from Korichelt and Helder,
after (‘hxld )
after (‘hxld )


A, 1)-coll stage, B, 4-coll stage C, “Hell stage I), 16-coll stage Pnmary trochoblasts
A, 1)-coll stage, B, 4-coll stage C, “Hell stage I), 16-coll stage Pnmary trochoblasts
are stxppled, E, the apu-nl stun culls la"-Id“ are dwldmg to produce m F the apical
are stxppled, E, the apu-nl stun culls la"-Id“ are dwldmg to produce m F the apical
rosette cells 19.1”-ld'“ and the stem cells of the cross 1a“‘-Id“? The primary trocho-
rosette cells 19.1”-ld'“ and the stem cells of the cross 1a“‘-Id“? The primary trochoblasts are la"-Id" and 121”-Id”
blasts are la"-Id" and 121”-Id”
60 HOLOBLASTIC TYPES OF CLEAVAGE
60 HOLOBLASTIC TYPES OF CLEAVAGE


figure there are in each quadrant apical rosette cells, stem cells of the
figure there are in each quadrant apical rosette cells, stem cells of the
cross and intermediate cells. These cells when the four quadrants are
cross and intermediate cells. These cells when the four quadrants are
considered together form a very definite picture of a cross, and not only
considered together form a very definite picture of a cross, and not only
are the cells themselves homologous with the similar condition found in
are the cells themselves homologous with the similar condition found in
the gastropods but there is a decided similarity in their arrangement, as
the gastropods but there is a decided similarity in their arrangement, as
will be seen by comparing Fig. 33 for Arenicola with the similar figure of
will be seen by comparing fig. 33 for Arenicola with the similar figure of
Crepidula (Fig. 29).
Crepidula (fig. 29).


The first appearance of the mesoderm in Arenicola is from the cell 4d
The first appearance of the mesoderm in Arenicola is from the cell 4d
Line 2,236: Line 2,063:
development of this group that call forth the admiration of the observer
development of this group that call forth the admiration of the observer
to the precision of the developmental mechanism. This is determinative
to the precision of the developmental mechanism. This is determinative
cleavage at its best and the specialist in this field of embryology finds a
cleavage at its best and the specialist in this field of embryology finds a
great deal here to interest him.
great deal here to interest him.


The cleavage of the Oligochaeta and the Hirudinca with certain modi-
The cleavage of the Oligochaeta and the Hirudinca with certain modifications shows the general agreement with the type just discussed.
fications shows the general agreement with the type just discussed.
These differences are correlated with the differences in the mode of
These differences are correlated with the differences in the mode of
existence between the water-living polychaetes and the other more
existence between the water-living polychaetes and the other more
specialized classes of annelids. In one of these forms, Clepsine, a leech,
specialized classes of annelids. In one of these forms, Clepsine, a leech,
the first study of cell lineage was made by Whitman in 1878.
the first study of cell lineage was made by Whitman in 1878.


As already indicated, the most important studies of the spiral type of
As already indicated, the most important studies of the spiral type of
Line 2,256: Line 2,082:
of this class. Conklin on Crepidula, Robert on Trochus are especially
of this class. Conklin on Crepidula, Robert on Trochus are especially
important contributions to our knowledge of the development of the
important contributions to our knowledge of the development of the
Prosobranchia, as is the work of Heymons on Umbrella, Casteel on Fiona
Prosobranchia, as is the work of Heymons on Umbrella, Casteel on fiona
for the Opisthobranchia, and Holmes on Planorbis and Wierzejski on
for the Opisthobranchia, and Holmes on Planorbis and Wierzejski on
Physa for the Pulmonata. Many other forms have been studied, but
Physa for the Pulmonata. Many other forms have been studied, but
these are examples of the various conditions found here. It may be
these are examples of the various conditions found here. It may be
noted that the cleavage of Planorbis and of Physa may be readily fol-
noted that the cleavage of Planorbis and of Physa may be readily followed in the laboratory, at least during very early stages, and they
lowed in the laboratory, at least during very early stages, and they
present perhaps the best opportunities for a student to observe this
present perhaps the best opportunities for a student to observe this
type of development.
type of development.


Spiral cleavage in the molluscs conforms to the type and indeed might
Spiral cleavage in the molluscs conforms to the type and indeed might
serve as the type, as may be seen from the table summarizing the devel-
serve as the type, as may be seen from the table summarizing the develSPIRAL CLEAVAGE 61
SPIRAL CLEAVAGE 61


opment of Crepidula. The importance of the homologies existing be-
opment of Crepidula. The importance of the homologies existing between the blastomeres of the annelids and of the molluscs have already
tween the blastomeres of the annelids and of the molluscs have already
been pointed out and need not again be referred to. Certain other
been pointed out and need not again be referred to. Certain other
interesting features, however, should be noted. One of these is the pres-
interesting features, however, should be noted. One of these is the presence of the yolk lobe described by a number of investigators in heavily
ence of the yolk lobe described by a number of investigators in heavily
yolk-laden Inollusc eggs. A similar structure has been described also in
yolk-laden Inollusc eggs. A similar structure has been described also in
some annelids. Here there appears at the vegetative pole in each of the
some annelids. Here there appears at the vegetative pole in each of the
first few cleavages a lobe Inore or less clearly marked but never com-
first few cleavages a lobe Inore or less clearly marked but never completely cut off from one of the blastomercs. It is known as the yolk
pletely cut off from one of the blastomercs. It is known as the yolk
lobe and is of varying size in different animals. Before each succeeding
lobe and is of varying size in different animals. Before each succeeding
cleavage it unites again with its blastomere, only to present itself in the
cleavage it unites again with its blastomere, only to present itself in the
interim before the next cleavage. Finally it becomes completely united
interim before the next cleavage. finally it becomes completely united
with the cell D and development proceeds. Experiments have been per-
with the cell D and development proceeds. Experiments have been performed in which this lobe has been cut off with the result that the
formed in which this lobe has been cut off with the result that the
larvae lack the ectoderm of the posterior portion of the body. Another
larvae lack the ectoderm of the posterior portion of the body. Another
interesting phenomenon observed in some cases of spiral cleavage con-
interesting phenomenon observed in some cases of spiral cleavage concerns the relation between the symmetry of the adult and that of the
cerns the relation between the symmetry of the adult and that of the
embryo. Crampton pointed out as a result of studying the cleavage of
embryo. Crampton pointed out as a result of studying the cleavage of
Physa that the reversed spiral of the shell of this snail is not a matter
Physa that the reversed spiral of the shell of this snail is not a matter
of adult life only but is so definitely impressed upon the nature of the
of adult life only but is so definitely impressed upon the nature of the
species that the direction of the cleavage planes from the third division
species that the direction of the cleavage planes from the third division
011 is exactly reversed from what is seen in eggs in which there is a shell
011 is exactly reversed from what is seen in eggs in which there is a shell
Line 2,294: Line 2,113:


The later stages in the cell lineage of spirally cleaving eggs lead us to
The later stages in the cell lineage of spirally cleaving eggs lead us to
a consideration of the methods of gastrulation and of mesoderm forma-
a consideration of the methods of gastrulation and of mesoderm formation and as such seem more properly to be considered in the chaptels
tion and as such seem more properly to be considered in the chaptels
which deal with these matters.
which deal with these matters.


Line 2,302: Line 2,120:
Among the more important accounts of the subjects contained in this chapter
Among the more important accounts of the subjects contained in this chapter
are the following: Echinoderms: Korsehelt and Heider, Selenka, Boveri, Plough,
are the following: Echinoderms: Korsehelt and Heider, Selenka, Boveri, Plough,
Morgan (Experimental Embryology); Ctenophores: Ziegler, Metchnikoff; Amphi-
Morgan (Experimental Embryology); Ctenophores: Ziegler, Metchnikoff; Amphioxus: Cerfontaine, Hatschek; Ascidians: Conklin, Chabry, Castle, Drieseh; Frog:
oxus: Cerfontaine, Hatschek; Ascidians: Conklin, Chabry, Castle, Drieseh; Frog:
Brachet, Morgan; Ascaris: Boveri; Spiral types: Conklin, Holmes, Wilson, Child,
Brachet, Morgan; Ascaris: Boveri; Spiral types: Conklin, Holmes, Wilson, Child,
Lillie, Robert, Coe, Lang, Surface, Whitman, Metealf, Casteel, Wierzejski, Cramp-
Lillie, Robert, Coe, Lang, Surface, Whitman, Metealf, Casteel, Wierzejski, Crampton. These works are cited in full in the bibliography on page 406.
ton. These works are cited in full in the bibliography on page 406.




===Chapter V Meroblastic Types of Cleavage===
===Chapter V Meroblastic Types of Cleavage===


I . SUPERFICIAL CLEAVAGE
I . SUPERfiCIAL CLEAVAGE


Superficial cleavage is found to occur most extensively among the
Superficial cleavage is found to occur most extensively among the
arthropod classes and indeed by many it is supposed to be coextensive
arthropod classes and indeed by many it is supposed to be coextensive
with this phylum of animals. There are, however, some other cases
with this phylum of animals. There are, however, some other cases
which may be properly spoken of as superficial cleavage. Among these
which may be properly spoken of as superficial cleavage. Among these
latter are the eggs of some eoelenterates which are heavily laden with
latter are the eggs of some eoelenterates which are heavily laden with
yolk, for example, Renilla, hydrocorals and Alcyonium. In addition it
yolk, for example, Renilla, hydrocorals and Alcyonium. In addition it
Line 2,322: Line 2,138:


Furthermore, it is by no means true that all arthropods undergo
Furthermore, it is by no means true that all arthropods undergo
superficial cleavage. Among the Crustacea there are many cases of total
superficial cleavage. Among the Crustacea there are many cases of total
cleavage in holoblastic eggs, and at the other extreme of the phylum
cleavage in holoblastic eggs, and at the other extreme of the phylum
the scorpions have discoidal cleavage. Examples of holoblastic cleavage
the scorpions have discoidal cleavage. Examples of holoblastic cleavage
Line 2,329: Line 2,145:
examples include cases in which cleavage is very nearly equal and in
examples include cases in which cleavage is very nearly equal and in
others, as the cirripeds, distinctly unequal. One illuminating study has
others, as the cirripeds, distinctly unequal. One illuminating study has
been made on the cleavage of the barnacle Lepas, which suggests rela-
been made on the cleavage of the barnacle Lepas, which suggests relationship to the annelid type and even has certain characteristics of the
tionship to the annelid type and even has certain characteristics of the
rotifers. In view of the generally assumed fact that the arthropods are
rotifers. In view of the generally assumed fact that the arthropods are
derived from annelid ancestry, the case of Lepas as studied by Bigelow
derived from annelid ancestry, the case of Lepas as studied by Bigelow
Line 2,336: Line 2,151:


With the exceptions of the forms mentioned the arthropods have
With the exceptions of the forms mentioned the arthropods have
superficial cleavage. It will be observed that the diversity of this
superficial cleavage. It will be observed that the diversity of this
phylum is so great that many different conditions of cleavage are found
phylum is so great that many different conditions of cleavage are found
here and even among the cases of superficial cleavage there will be seen
here and even among the cases of superficial cleavage there will be seen
to be a great variety. To such an extent is this true that we cannot
to be a great variety. To such an extent is this true that we cannot
describe as typical of superficially cleaving eggs any one particular
describe as typical of superficially cleaving eggs any one particular
form, and, although we may classify superficial cleavage into subdivi-
form, and, although we may classify superficial cleavage into subdivisions, these are by no means separated from each other sharply but
sions, these are by no means separated from each other sharply but
gradations exist between them. Superficial cleavage is characteristic of
gradations exist between them. Superficial cleavage is characteristic of
eggs which are centrolecithal in character; eggs of the centrolecithal
eggs which are centrolecithal in character; eggs of the centrolecithal
type are derived from forms having total and in most cases equal cleav-
type are derived from forms having total and in most cases equal cleavage, while on the other hand they lead to an extreme type of superficial cleavage which is so different from the usual arthropod eg as to
age, while on the other hand they lead to an extreme type of super-
ficial cleavage which is so different from the usual arthropod eg as to


62
62
SUPERFICIAL CLEAVAGE 63
SUPERfiCIAL CLEAVAGE 63


be classified with eggs having discoidal cleavage rather than superficial.
be classified with eggs having discoidal cleavage rather than superficial.
Reference is made to the eggs of the scorpion which are without question
Reference is made to the eggs of the scorpion which are without question
derived from the extreme superficial type but which as a result of
derived from the extreme superficial type but which as a result of
parallel convergence resemble most clearly the discoidal type of verte-
parallel convergence resemble most clearly the discoidal type of vertebrates. In eentrolecithal eggs the cleavage nucleus is usually at the
brates. In eentrolecithal eggs the cleavage nucleus is usually at the
center of the egg and is surrounded by the mass of yolk spherules and
center of the egg and is surrounded by the mass of yolk spherules and
fat droplets. Penetrating this mass in every part is a network of cyto-
fat droplets. Penetrating this mass in every part is a network of cytoplasm which is continuous with the central cytoplasmic portion around
plasm which is continuous with the central cytoplasmic portion around
the nucleus and also with a very thin superficial cytoplasmic layer on
the nucleus and also with a very thin superficial cytoplasmic layer on
the outside of the egg. This latter layer is in some cases so delicate as
the outside of the egg. This latter layer is in some cases so delicate as
to be difficult to make out, whereas in other cases it is clearly visible.
to be difficult to make out, whereas in other cases it is clearly visible.
Line 2,370: Line 2,180:
many other egg types.
many other egg types.


As a first type of superficial cleavage we may take up one of the
As a first type of superficial cleavage we may take up one of the
insects, for in this form it is especially clearly developed. The well-known
insects, for in this form it is especially clearly developed. The well-known
figures of the cleavage of Hydrophilus suggest the early course of this
figures of the cleavage of Hydrophilus suggest the early course of this
type of development. The cleavage nucleus lying at the center of the egg
type of development. The cleavage nucleus lying at the center of the egg
in the midst of its plasma island divides into 2, 4, 8. 16 nuclei, each
in the midst of its plasma island divides into 2, 4, 8. 16 nuclei, each
surrounded by a small portion of cytoplasm and each somewhat sepa-
surrounded by a small portion of cytoplasm and each somewhat separated from the others in the form of amoeboid or star-shaped areas.
rated from the others in the form of amoeboid or star-shaped areas.
Actually all are in communication through the plasma. network that
Actually all are in communication through the plasma. network that
penetrates the yolk mass. At this stage and for some time later the egg
penetrates the yolk mass. At this stage and for some time later the egg
Line 2,385: Line 2,194:
these cleavage cells come to form a layer within the yolk which by one
these cleavage cells come to form a layer within the yolk which by one
continued division tends to approach the periphery of the egg. At length
continued division tends to approach the periphery of the egg. At length
they unite with the superficial cytoplasmic layer in Hg/drophilus near
they unite with the superficial cytoplasmic layer in Hg/drophilus near
the middle of the egg first and at the ends only some time later. Then
the middle of the egg first and at the ends only some time later. Then
cytoplasmic boundaries become visible and the cleavage is truly super-
cytoplasmic boundaries become visible and the cleavage is truly superficial, although of course only partial, since the divisions do not extend
ficial, although of course only partial, since the divisions do not extend
through the yolk mass.
through the yolk mass.


Line 2,394: Line 2,202:
not take part in the formation of the blastoderm but remain in the yolk
not take part in the formation of the blastoderm but remain in the yolk
while the others pass to the surface. They take on special functions for
while the others pass to the surface. They take on special functions for
the assimilation of the yolk substance and become known as the mello-
the assimilation of the yolk substance and become known as the mellophages. In some cases incomplete cell boundaries seem to be formed
phages. In some cases incomplete cell boundaries seem to be formed
fiG. 34. Blasboderm formation in the water beetle Hydrophilus. (Redruwn from Korschelt
FIG. 34. Blasboderm formation in the water beetle Hydrophilus. (Redruwn from Korschelt
and Heidcr. after Heider.)
and Heidcr. after Heider.)


b, blastoderm cells; 0, “cleavage cells"; p, peripheral layer of protoplasm; y, yolk.
b, blastoderm cells; 0, “cleavage cells"; p, peripheral layer of protoplasm; y, yolk.
CLEAVAGE AT FIRST TOTAL BUT LATER SUPERFICIAL 65
CLEAVAGE AT fiRST TOTAL BUT LATER SUPERfiCIAL 65


around these vitellophages, giving rise to the so-called secondary yolk
around these vitellophages, giving rise to the so-called secondary yolk
cleavage. The vitellophages are to be regarded as endoderm, and for
cleavage. The vitellophages are to be regarded as endoderm, and for
that reason some investigators have described superficial cleavage as
that reason some investigators have described superficial cleavage as
leading directly to the formation of a gastrula-like stage since two kinds
leading directly to the formation of a gastrula-like stage since two kinds
of cells, ectoderm and endoderm, are formed about the same time.
of cells, ectoderm and endoderm, are formed about the same time.
This view has not been widely adopted.
This view has not been widely adopted.


Superficial cleavage usually results in the formation of blastomeres
Superficial cleavage usually results in the formation of blastomeres
of equal size and cleavage is indcterminativc.* Inequalities appear very
of equal size and cleavage is indcterminativc.* Inequalities appear very
early in some forms, however, and there are many variations from the
early in some forms, however, and there are many variations from the
Line 2,417: Line 2,224:
from the spiders and from tl1e insects, by certain characteristic features;
from the spiders and from tl1e insects, by certain characteristic features;
but these differences do not lend themselves to accuracy of statement
but these differences do not lend themselves to accuracy of statement
nor form a satisfactory basis for classification. It is wiser therefore to
nor form a satisfactory basis for classification. It is wiser therefore to
classify the superficial cleavage under the following heads: Group 1.
classify the superficial cleavage under the following heads: Group 1.
Cleavage at first total but later superficial. Group 2. Cleavage purely
Cleavage at first total but later superficial. Group 2. Cleavage purely
superficial. Both of these groups in their turn may be divided into two
superficial. Both of these groups in their turn may be divided into two
subdivisions in one of which the blastoderm forms on all sides simulta-
subdivisions in one of which the blastoderm forms on all sides simultaneously and in the other on the ventral side precociously.
neously and in the other on the ventral side precociously.


1. Cleavage at First Total but Later Superficial
1. Cleavage at first Total but Later Superficial


This type of cleavage, which is typical of many crustaceans, begins
This type of cleavage, which is typical of many crustaceans, begins
with the division of the plasma island into 2, 4, and perhaps 8 blaste-
with the division of the plasma island into 2, 4, and perhaps 8 blastemcres about which all cell boundaries are cut off at once. (‘leavage
mcres about which all cell boundaries are cut off at once. (‘leavage
during this period of the development and for some successive cell
during this period of the development and for some successive cell
divisions thereafter is total and approximately equal. Presently there
divisions thereafter is total and approximately equal. Presently there
comes a time when the furrows at the surface are unable to cut entirely
comes a time when the furrows at the surface are unable to cut entirely
through the egg, or if they do the yolk masses at the center must fuse
through the egg, or if they do the yolk masses at the center must fuse
together and cleavage becomes superficial with a cellular region sharply
together and cleavage becomes superficial with a cellular region sharply
separated from the yolk mass. The blastula consists of a layer of super-
separated from the yolk mass. The blastula consists of a layer of superficial cells of cq11al size and an inner yolk mass replacing the cleavage
ficial cells of cq11al size and an inner yolk mass replacing the cleavage
cavity. In many cases there is a (listinction between the central-lying
cavity. In many cases there is a (listinction between the central-lying
yolk mass and the yolk which formed the inner end of the blastomcre.
yolk mass and the yolk which formed the inner end of the blastomcre.
They were left incomplete by the failure of the furrows to penetrate to
They were left incomplete by the failure of the furrows to penetrate to
the center of the egg. These inner ends are spoken of as the yolk pyra-
the center of the egg. These inner ends are spoken of as the yolk pyra
 
* Nevertheless, experiments on the egg of the house fly, M usca domestica, made
* Nevertheless, experiments on the egg of the house fly, M usca domestica, made
by Reith (1925) show for this animal (and make it probable for others having this
by Reith (1925) show for this animal (and make it probable for others having this
type of cleavage) that the egg is highly determinative. The embryo is fore-shadowed
type of cleavage) that the egg is highly determinative. The embryo is fore-shadowed
in the cytoplasm of the egg and the regions are clearly organized in relation to their
in the cytoplasm of the egg and the regions are clearly organized in relation to their
future destiny. Add to this.the very definite nuclear determination which the experi-
future destiny. Add to this.the very definite nuclear determination which the experiments on the genetics of Drosophila have demonstrated, and it is clear that the
ments on the genetics of Drosophila have demonstrated, and it is clear that the
eggs of Dipteru can by no means he called indeterminative.
eggs of Dipteru can by no means he called indeterminative.
66 MEROBLASTIC TYPES OF CLEAVAGE
66 MEROBLASTIC TYPES OF CLEAVAGE


mids (sometimes as Rathke’s yolk pyramids). The significance of these
mids (sometimes as Rathke’s yolk pyramids). The significance of these
structures is not entirely clear but their appearance is characteristic.
structures is not entirely clear but their appearance is characteristic.
This type of cleavage easily suggests a transition from the holoblastic
This type of cleavage easily suggests a transition from the holoblastic
eggs of other Crustacea to the form in which cleavage is purely super.
eggs of other Crustacea to the form in which cleavage is purely super.
ficial. This type of cleavage, as already pointed out, occurs in two
ficial. This type of cleavage, as already pointed out, occurs in two
subdivisions :
subdivisions :


FIG. 35. Cleavage of Macrutoma vulgaris. (Redmwn from Korsehelt and Heider, after
fiG. 35. Cleavage of Macrutoma vulgaris. (Redmwn from Korsehelt and Heider, after
Uzel.)
Uzel.)


Line 2,465: Line 2,267:
having fused.
having fused.


a. Eggs in which the superficial cleavage leads to blastoderni forma-
a. Eggs in which the superficial cleavage leads to blastoderni formation simultaneously all over the egg. To this subdivision belong the eggs
tion simultaneously all over the egg. To this subdivision belong the eggs
of those free-living copepods which are not holoblastic, some parasitic
of those free-living copepods which are not holoblastic, some parasitic
copepods, the ostraeods, spiders, and some isolated forms in various
copepods, the ostraeods, spiders, and some isolated forms in various
Line 2,473: Line 2,274:
b. Eggs in which the blastoderm develops early on the ventral side, a
b. Eggs in which the blastoderm develops early on the ventral side, a
condition which foretells the position of the forming germ streak. The
condition which foretells the position of the forming germ streak. The
EGGS WITH PURELY SUPERFICIAL CLEAVAGE 67
EGGS WITH PURELY SUPERfiCIAL CLEAVAGE 67


dccapods in part come under this subdivision as do some of the amphi-
dccapods in part come under this subdivision as do some of the amphipods as well as other scattering forms.
pods as well as other scattering forms.


2. Eggs with Purely Superficial Cleavage
2. Eggs with Purely Superficial Cleavage


Eggs which come under this subdivision carry still farther those
Eggs which come under this subdivision carry still farther those
tendencies which are beginning to be expressed in the previous group.
tendencies which are beginning to be expressed in the previous group.


FIG. 36. Cleavage of the crab Dromfa. (Redrawn from Korschelt and Heider. after Cane.)
fiG. 36. Cleavage of the crab Dromfa. (Redrawn from Korschelt and Heider. after Cane.)
Successive stages showing “cleavage cells," the yolk pyramids, and the blastoderm.
Successive stages showing “cleavage cells," the yolk pyramids, and the blastoderm.


Line 2,490: Line 2,290:
nucleus with its surrounding plasmic layer divides several times but no
nucleus with its surrounding plasmic layer divides several times but no
cell boundaries are formed by the separate areas. The only indication
cell boundaries are formed by the separate areas. The only indication
of division now to be seen is the occasional presence of superficial furrows
of division now to be seen is the occasional presence of superficial furrows
68 MEROBLASTIC TYPES OF CLEAVAGE
68 MEROBLASTIC TYPES OF CLEAVAGE


Line 2,496: Line 2,296:
they approach the surface and furrows become more pronounced.
they approach the surface and furrows become more pronounced.
The result is a blastoderm with the cell boundaries cutting in to the
The result is a blastoderm with the cell boundaries cutting in to the
yolk although not completely delimiting definite cell bodies from it
yolk although not completely delimiting definite cell bodies from it
until a. later stage when the blastoderm takes on the form of the definite
until a. later stage when the blastoderm takes on the form of the definite
layer. Cleavage of this type occurs among the Crustacea commonly,
layer. Cleavage of this type occurs among the Crustacea commonly,
although it is much more widespread in the Malacostraca than in the
although it is much more widespread in the Malacostraca than in the
Line 2,508: Line 2,308:
that many variations will be found, although in general the description
that many variations will be found, although in general the description
of Ilyrlrophilus as already given is quite applicable. There are cases in
of Ilyrlrophilus as already given is quite applicable. There are cases in
which the superficial plasma layer is so thin as to be almost absent and
which the superficial plasma layer is so thin as to be almost absent and
other cases in which it is Very definitely marked and these varying
other cases in which it is Very definitely marked and these varying
conditions have an effect upon the appearance of the blastoderm. There
conditions have an effect upon the appearance of the blastoderm. There
is also variation in the extent to which the blastoderm is formed over the
is also variation in the extent to which the blastoderm is formed over the
surface of the egg. This latter feature is the basis for the further classifi-
surface of the egg. This latter feature is the basis for the further classification of these eggs into two types as in the previous group.
cation of these eggs into two types as in the previous group.


:1. Eggs which have simultaneous formations of the blastoderm all
:1. Eggs which have simultaneous formations of the blastoderm all
over the egg. Most of the cases of purely superficial cleavage come here,
over the egg. Most of the cases of purely superficial cleavage come here,
specifically the Cladocera, most decapods, the myriapods, most insects
specifically the Cladocera, most decapods, the myriapods, most insects
and many other scattered forms.
and many other scattered forms.


b. Eggs with precocious development of the blastoderm on the ventral
b. Eggs with precocious development of the blastoderm on the ventral
side. Here belong Ncbalia, the schizopods, the Cumaceae, the isopods,
side. Here belong Ncbalia, the schizopods, the Cumaceae, the isopods,
and some decapods,including the lobster. The restriction of the blaste-
and some decapods,including the lobster. The restriction of the blastederm to a small portion of the surface of the egg is so marked in some of
derm to a small portion of the surface of the egg is so marked in some of
these forms that it was formerly the practice of some investigators to
these forms that it was formerly the practice of some investigators to
regard these as cases of diseoidal cleavage. We do not at the present time,
regard these as cases of diseoidal cleavage. We do not at the present time,
however, so regard them. Nevertheless this subdivision of superficial
however, so regard them. Nevertheless this subdivision of superficial
cleavage clearly leads to the conditions found in the scorpions as an
cleavage clearly leads to the conditions found in the scorpions as an
extreme case, and these latter forms are commonly included with the
extreme case, and these latter forms are commonly included with the
Line 2,538: Line 2,336:
in two separate invertebrate classes, the cephalopods and the scorpions.
in two separate invertebrate classes, the cephalopods and the scorpions.
This distribution suggests what is found to be the case, namely that
This distribution suggests what is found to be the case, namely that
FIG. 37. Cleavage of (”am7mdz'a staphulinus. (Rcdrawn from Korschelt and Heider,
fiG. 37. Cleavage of (”am7mdz'a staphulinus. (Rcdrawn from Korschelt and Heider,
after Uzel.)
after Uzel.)


Line 2,554: Line 2,352:
discoidal cleavage except the scorpions in which the discoidal type is
discoidal cleavage except the scorpions in which the discoidal type is
derived, as may be inferred from the preceding discussion (page 68)
derived, as may be inferred from the preceding discussion (page 68)
from the extreme case of purely superficial cleavage. Only a small portion
from the extreme case of purely superficial cleavage. Only a small portion
of the egg surface is involved in the formation of the embryo body in the
of the egg surface is involved in the formation of the embryo body in the
superficial forms mentioned.
superficial forms mentioned.


It is evident that not much in common is to be expected in the ele-
It is evident that not much in common is to be expected in the elemental features of these two characteristic modes of discoidal cleavage.
mental features of these two characteristic modes of discoidal cleavage.


@@
@@
Line 2,565: Line 2,362:
A B C
A B C


FIG. 38. Germ disc of the scorpion Euscorpius carpathicus. Polar views. (Redrawn from
fiG. 38. Germ disc of the scorpion Euscorpius carpathicus. Polar views. (Redrawn from
Korschelt and Heider, after Brauer.)
Korschelt and Heider, after Brauer.)


It was formerly said that discoidal cleavage occurs also in some crus-
It was formerly said that discoidal cleavage occurs also in some crustaceans but it seems wiser to regard these as within the limits of superficial cleavage than as examples of the true discoidal type. Because of
taceans but it seems wiser to regard these as within the limits of super-
ficial cleavage than as examples of the true discoidal type. Because of
the separate origin of these cleavage types it will be convenient to begin
the separate origin of these cleavage types it will be convenient to begin
this discussion with the cleavage of the scorpion.
this discussion with the cleavage of the scorpion.
Line 2,581: Line 2,376:
portion is limited to a disc-shaped area which corresponds to the point
portion is limited to a disc-shaped area which corresponds to the point
of attachment within the egg follicle. With the exception of perhaps a
of attachment within the egg follicle. With the exception of perhaps a
very thin filament over the surface of the egg no other protoplasmic
very thin filament over the surface of the egg no other protoplasmic
portion can be demonstrated. Segmentation is limited to the proto-
portion can be demonstrated. Segmentation is limited to the protoplasmic disc which divides with fair regularity. About the third or
plasmic disc which divides with fair regularity. About the third or
fourth cleavage there is oftentimes what seems superficially to be a
fourth cleavage there is oftentimes what seems superficially to be a
bilateral arrangement of the blastomeres, but the appearance is only
bilateral arrangement of the blastomeres, but the appearance is only
superficial for the cleavages from here on become quite irregular. The
superficial for the cleavages from here on become quite irregular. The
SCORPIO NS 71
SCORPIO NS 71


result of cleavage is a round or oval blastodisc consisting of at first but
result of cleavage is a round or oval blastodisc consisting of at first but
a single layer of cells. The single-celled condition does not remain long
a single layer of cells. The single-celled condition does not remain long
because a number of cells wander down below the surface from a defi-
because a number of cells wander down below the surface from a definitely recognizable white speck. This speck is important in determining
nitely recognizable white speck. This speck is important in determining
the plane of symmetry and the hinder end of the embryo. The first cells
the plane of symmetry and the hinder end of the embryo. The first cells
which wander in are transformed into yolk cells and although they
which wander in are transformed into yolk cells and although they
Line 2,602: Line 2,395:
   
   


FIG '3‘) Set tions of stages similar to lig .58, and of two liter stages.
fiG '3‘) Set tions of stages similar to lig .58, and of two liter stages.


A, immature germinal vesicle, B, early cleavage, C‘, l)l‘1‘lt()(l(‘l‘II1 formed, D, beginning
A, immature germinal vesicle, B, early cleavage, C‘, l)l‘1‘lt()(l(‘l‘II1 formed, D, beginning
Line 2,613: Line 2,406:


Mesoderm arises from a division of cctoderm cells near those which
Mesoderm arises from a division of cctoderm cells near those which
are to produce genital cells. The subsequent development of the blaste-
are to produce genital cells. The subsequent development of the blastedisc shows the formation of a segmented germ streak which gradually
disc shows the formation of a segmented germ streak which gradually
develops into the typical body form of the scorpion and which grows
develops into the typical body form of the scorpion and which grows
finally to include entirely the yolk in the middle region of the gut. The
finally to include entirely the yolk in the middle region of the gut. The
forming embryo is suggestive of certain stages in the later development
forming embryo is suggestive of certain stages in the later development
of eggs having superficial cleavage but it is likewise very similar in a
of eggs having superficial cleavage but it is likewise very similar in a
number of particulars to the conditions found in vertebrate embryos
number of particulars to the conditions found in vertebrate embryos
72 MEROBLASTIC TYPES OF CLEAVAGE
72 MEROBLASTIC TYPES OF CLEAVAGE


which develop by diseoidal clcivage. There are clearly produced in
which develop by diseoidal clcivage. There are clearly produced in
these different groups similarities which are purely embryonic and there-
these different groups similarities which are purely embryonic and therefore transitory; they have no evolutionary significance.
fore transitory; they have no evolutionary significance.


2. Cephalopods
2. Cephalopods
Line 2,630: Line 2,421:
The cleavage of cephalopod eggs differs in many particulars from that
The cleavage of cephalopod eggs differs in many particulars from that
of other molluscs and also from the forms within the groups having
of other molluscs and also from the forms within the groups having
discoidal cleavage. The differences seem to be in keeping with the pecu-
discoidal cleavage. The differences seem to be in keeping with the peculiarities of egg structure, which are pronounced.
liarities of egg structure, which are pronounced.


The eggs are laid in large numbers, usually together, and the mass
The eggs are laid in large numbers, usually together, and the mass
may assume various forms. There is always a protective covering which
may assume various forms. There is always a protective covering which
is the means of attaching the mass of spawn. In Sepia the eggs are dis-
is the means of attaching the mass of spawn. In Sepia the eggs are dis
 
av
av


Line 2,642: Line 2,431:


A v B C
A v B C
FIG. 40. Eggs of the squid Loligo pmlii. (Redmwn from Korsehelt and Heider, after
fiG. 40. Eggs of the squid Loligo pmlii. (Redmwn from Korsehelt and Heider, after
Watase.)
Watase.)


Line 2,649: Line 2,438:
crete and each is in its own capsule. In Loligo many are laid together in
crete and each is in its own capsule. In Loligo many are laid together in
a gelatinous tube and numerous tubes are attached in one mass, known
a gelatinous tube and numerous tubes are attached in one mass, known
to the sailors as “dead men’s fingers.” Fertilization follows after various
to the sailors as “dead men’s fingers.” Fertilization follows after various
peculiar types of copulation in which spermatozoa are transferrerl in
peculiar types of copulation in which spermatozoa are transferrerl in
spermatophores; fertilization is internal in some groups, and external in
spermatophores; fertilization is internal in some groups, and external in
others, of which the squids mentioned are examples.
others, of which the squids mentioned are examples.


The eggs themselves are relatively large for marine eggs and all con-
The eggs themselves are relatively large for marine eggs and all contain very much yolk. The development of the squids, particularly of
tain very much yolk. The development of the squids, particularly of
Sepia and of Loligo, are best known and will be used from here on as
Sepia and of Loligo, are best known and will be used from here on as
examples of this form of development. Sepia eggs have the size of ordi-
examples of this form of development. Sepia eggs have the size of ordinary peas, whereas those of Loligo are much smaller, but even they are
nary peas, whereas those of Loligo are much smaller, but even they are
larger than the eggs of most marine molluscs.
larger than the eggs of most marine molluscs.


Cephalopod eggs have been studied by numerous investigators, but
Cephalopod eggs have been studied by numerous investigators, but
our knowledge of the cleavage depends chiefly upon the work of Vialleton
our knowledge of the cleavage depends chiefly upon the work of Vialleton
on Sepia ofiicinalis and of Watase on Loligo pealii. The eggs of Loligo,
on Sepia ofiicinalis and of Watase on Loligo pealii. The eggs of Loligo,
at the time they are ready for cleavage, are somewhat oblong in shape,
at the time they are ready for cleavage, are somewhat oblong in shape,
CEPHALOPODS 73
CEPHALOPODS 73


one end being more pointed than the ot.her. The egg consists of a mass
one end being more pointed than the ot.her. The egg consists of a mass
of fine granules of food yolk surrounded entirely by a thin protoplasmic
of fine granules of food yolk surrounded entirely by a thin protoplasmic
layer. This layer is thicker at the pointed end of the egg where the germ
layer. This layer is thicker at the pointed end of the egg where the germ
disc will form. Thus this egg represents an extreme telolecithal type and
disc will form. Thus this egg represents an extreme telolecithal type and
is a perfect example of meroblastic cleavage.
is a perfect example of meroblastic cleavage.


The uncleaved egg from surface study alone gives evidence of bilat-
The uncleaved egg from surface study alone gives evidence of bilateral symmetry which bears a definite relation to the subsequent history
eral symmetry which bears a definite relation to the subsequent history
of the embryo, and it is possible to distinguish an anterior border from
of the embryo, and it is possible to distinguish an anterior border from
a posterior as well as right from left sides of the organism. The germ
a posterior as well as right from left sides of the organism. The germ
Line 2,681: Line 2,467:
   
   


FIG. 41. Germ disc of the squid Sepia 0j7'i(‘inaIi.~r. (Redrawn from Korsehelt and Heider,
fiG. 41. Germ disc of the squid Sepia 0j7'i(‘inaIi.~r. (Redrawn from Korsehelt and Heider,
after Vialleton.)
after Vialleton.)


Line 2,702: Line 2,488:
deeply, dividing the entire protoplasmic cap at this point, but toward
deeply, dividing the entire protoplasmic cap at this point, but toward
the edges of the disc it becomes shallower until it is a mere groove and
the edges of the disc it becomes shallower until it is a mere groove and
finally disappears entirely. The successive cleavages behave in a similar
finally disappears entirely. The successive cleavages behave in a similar
manner. Thus cleavage is incomplete even with respect to the proto-
manner. Thus cleavage is incomplete even with respect to the protoplasmic layer. ,The second furrow is at right angles to the first, and like
plasmic layer. ,The second furrow is at right angles to the first, and like
it, fades away into the thin protoplasm. The later furrows which extend
it, fades away into the thin protoplasm. The later furrows which extend
outward likewise fade away and the cells thus formed are incompletely
outward likewise fade away and the cells thus formed are incompletely
Line 2,717: Line 2,502:


_r ”‘o,w"{§y,_ 01¢)‘: 501,1‘-xv «.91?
_r ”‘o,w"{§y,_ 01¢)‘: 501,1‘-xv «.91?
-I. - v-
-I. - v
 
‘,Q°.. _v'5 6
‘,Q°.. _v'5 6
b
b
Line 2,724: Line 2,508:
   
   


Fm 42 Older germ disc of S(’[)’LLl ofiicmalzs from the beginning of germ layer form itu n
Fm 42 Older germ disc of S(’[)’LLl ofiicmalzs from the beginning of germ layer form itu n
The darker cells iiidimte the region where the disc is of several cells in llll( kiiess L itcr
The darker cells iiidimte the region where the disc is of several cells in llll( kiiess L itcr
stage than Fig 41
stage than fig 41


the term blastomere being applied only to those cells which are coni-
the term blastomere being applied only to those cells which are conipletely cut off, while the peripheral ones which have no outer boundary
pletely cut off, while the peripheral ones which have no outer boundary
are spoken of as blastocones.
are spoken of as blastocones.


In the preceding types of cleavage we have seen that the cleavage
In the preceding types of cleavage we have seen that the cleavage
cells have usually received special designations. In the present case,
cells have usually received special designations. In the present case,
on the other hand, it has been found more convenient to indicate a dis-
on the other hand, it has been found more convenient to indicate a distinction between the various cleavage cells by numbering the furrows
tinction between the various cleavage cells by numbering the furrows
which separate them, the first furrow lying in the median plane and
which separate them, the first furrow lying in the median plane and
indicated by the polar body numbered I. The second furrow, II, is at
indicated by the polar body numbered I. The second furrow, II, is at
right angles to it. The third furrow likewise is meridional but it divides
right angles to it. The third furrow likewise is meridional but it divides
Line 2,752: Line 2,534:
   
   


Fit. 4i Se: tioim ilirmigh the edge of the germ (.lls( in suctessiic stagm
fit. 4i Se: tioim ilirmigh the edge of the germ (.lls( in suctessiic stagm
B, corresponds to Fig 42 y, yolk, y 0 , yolk epithelium, e, embryonic cells
B, corresponds to fig 42 y, yolk, y 0 , yolk epithelium, e, embryonic cells


of the disc. By this time the bilaterality which existed in the uneleaved
of the disc. By this time the bilaterality which existed in the uneleaved
egg has become very appaient, each half of the egg consisting of seven
egg has become very appaient, each half of the egg consisting of seven
blastocones and one blastomere. The 32-cell stage is reached partly by
blastocones and one blastomere. The 32-cell stage is reached partly by
nieiidional and partly by transverse furrows. Numbering the blasto-
nieiidional and partly by transverse furrows. Numbering the blastocones of each half of the egg from the anterior side backwards as one
cones of each half of the egg from the anterior side backwards as one
to six, the following divisions occur. Number one divides transversally,
to six, the following divisions occur. Number one divides transversally,
producing a blastoinere and a blastocone. Numbers two and three
producing a blastoinere and a blastocone. Numbers two and three
divide meridionally, each producing two blastocones. Numbers four and
divide meridionally, each producing two blastocones. Numbers four and
five each cut off a blastomere by a transverse division, and number six
five each cut off a blastomere by a transverse division, and number six
divides meridionally. The posterior narrow pair of blastocones again
divides meridionally. The posterior narrow pair of blastocones again
76 MEROBLASTIC TYPES OF CLEAVAGE
76 MEROBLASTIC TYPES OF CLEAVAGE


divide transversally, cutting off blastomeres, and the two first blaste-
divide transversally, cutting off blastomeres, and the two first blastemeres likewise divide. The 32-cell stage thus consists of fourteen blastemeres and eighteen blastocones symmetrically arranged. Thus the center
meres likewise divide. The 32-cell stage thus consists of fourteen blaste-
of the disc comes to be filled up with a compact layer of blastomeres
meres and eighteen blastocones symmetrically arranged. Thus the center
of the disc comes to be filled up with a compact layer of blastomeres
radiating from ‘which are the blastocones.
radiating from ‘which are the blastocones.


Subsequent cleavages bring about a decrease in the size of the blaste-
Subsequent cleavages bring about a decrease in the size of the blastemeres and are responsible for their regular disposition. The germ disc
meres and are responsible for their regular disposition. The germ disc
thus comes to consist of a one—layered plate of polygonal cells with
thus comes to consist of a one—layered plate of polygonal cells with
peripheral blastocones passing over into the mass of formative yolk.
peripheral blastocones passing over into the mass of formative yolk.
Line 2,803: Line 2,581:
and it has been recorded for some Inarsupial eggs. In the opossum,
and it has been recorded for some Inarsupial eggs. In the opossum,
however, according to the accurate and clear description of Hartman,
however, according to the accurate and clear description of Hartman,
cleavage is certainly not disceidal, nor is that of Dasyurus as figured
cleavage is certainly not disceidal, nor is that of Dasyurus as figured
by Hill. Thus it occurs in five classes of vertebrates, and possibly in the
by Hill. Thus it occurs in five classes of vertebrates, and possibly in the
sixth; in seine of these it is the characteristic method and in others it is
sixth; in seine of these it is the characteristic method and in others it is
quite exceptional. This distribution points out, as has been noted previ-
quite exceptional. This distribution points out, as has been noted previously, that there is no taxonomic or phylogenetic significance in the
ously, that there is no taxonomic or phylogenetic significance in the
classification of cleavage types. An inspection of the list as given shows
classification of cleavage types. An inspection of the list as given shows
discoidal cleavage alongside of the holoblastic type in many of these
discoidal cleavage alongside of the holoblastic type in many of these
groups. The myxinoids are discoidal while the lampreys have holoblastic
groups. The myxinoids are discoidal while the lampreys have holoblastic
cleavage in the class Cyclostomata. Among the fishes, elasmobranchs
cleavage in the class Cyclostomata. Among the fishes, elasmobranchs
and teleosts are extremely disceidal, but the dipnoid and the ganoid
and teleosts are extremely disceidal, but the dipnoid and the ganoid
VERTEBRATES 7 7
VERTEBRATES 7 7


fishes are holoblastic in type. The typical amphibian egg is holoblastic,
fishes are holoblastic in type. The typical amphibian egg is holoblastic,
but ‘the Gymnophiona show discoidal cleavage. Instead of having
but ‘the Gymnophiona show discoidal cleavage. Instead of having
taxonomic significance, the distribution of discoidal cleavage is related
taxonomic significance, the distribution of discoidal cleavage is related
entirely to the amount of yolk present in the egg.
entirely to the amount of yolk present in the egg.


The relationship between the holoblastic and ineroblastic types of
The relationship between the holoblastic and ineroblastic types of
cleavage will be best understood by recalling the cleavage of the frog
cleavage will be best understood by recalling the cleavage of the frog
egg (Figs. 22 and 26). From the condition found in the frog egg we may
egg (figs. 22 and 26). From the condition found in the frog egg we may
pass by a consideration of the cleavage of /icipenser, the sturgeon, Amia,
pass by a consideration of the cleavage of /icipenser, the sturgeon, Amia,
the bowfin, and Lepidosteus, the gar pike, to those found in the tcleost
the bowfin, and Lepidosteus, the gar pike, to those found in the tcleost
egg. That is, we pass from the telolecithal egg of the amphibian or
egg. That is, we pass from the telolecithal egg of the amphibian or
lamprey by increasing degrees of separation of yolk and protoplasmic
lamprey by increasing degrees of separation of yolk and protoplasmic
Line 2,836: Line 2,613:
(l{e(lr'.u\'n from Ziegler, after Whiunan and E_v(-leshymer.)
(l{e(lr'.u\'n from Ziegler, after Whiunan and E_v(-leshymer.)


The cleavages of the lamprey and of the frog show remarkable simi-
The cleavages of the lamprey and of the frog show remarkable similarity. In both there is a large proportion of yolk, but it is still suffieiently separated into spherules for the cytoplasm to cut cntirelv
larity. In both there is a large proportion of yolk, but it is still suffi-
through it. Cleavage is total and unequal, the first two furrows being
eiently separated into spherules for the cytoplasm to cut cntirelv
through it. Cleavage is total and unequal, the first two furrows being
meridional and separating the eggs into four blastomeres. The third
meridional and separating the eggs into four blastomeres. The third
furrow is latitudinal. In Petromyzon the fourth furrows mark the begin-
furrow is latitudinal. In Petromyzon the fourth furrows mark the beginning of irregularities in cleavages whereby the cells of the animal half
ning of irregularities in cleavages whereby the cells of the animal half
cleave more rapidly than the vegetative half, some of the furrows not
cleave more rapidly than the vegetative half, some of the furrows not
being completed until very late.
being completed until very late.


In the sturgeon, according to the description of Dean, the first
In the sturgeon, according to the description of Dean, the first
cleavages separate the blastomeres but do not penetrate deeply into
cleavages separate the blastomeres but do not penetrate deeply into
the yolk. The egg in the late segmentation stages shows a protoplasmic
the yolk. The egg in the late segmentation stages shows a protoplasmic
Line 2,852: Line 2,626:
also occurred and meridional cleavages have separated off marginal cells
also occurred and meridional cleavages have separated off marginal cells
in an irregular manner so that the surface of the yolk half of the egg
in an irregular manner so that the surface of the yolk half of the egg
becomes subdivided into many-sized polygonal cells. While the proto-
becomes subdivided into many-sized polygonal cells. While the protoplasmic cap of small cells constitutes a blastodisc, it does not include
plasmic cap of small cells constitutes a blastodisc, it does not include
all the protoplasmic portion of the egg, as in the case of the true discoidal
all the protoplasmic portion of the egg, as in the case of the true discoidal
78 MEROBLASTIC TYPES OF CLEAVAGE
78 MEROBLASTIC TYPES OF CLEAVAGE


types. The cells adjacent to it are connected with the yolk. The blaste-
types. The cells adjacent to it are connected with the yolk. The blastedisc proper, however, is separated from the yolk by the cleavage cavity,
disc proper, however, is separated from the yolk by the cleavage cavity,
the floor of which consists at first of a few irregular yolk-bearing cells.
the floor of which consists at first of a few irregular yolk-bearing cells.
There is no sharp distinction between these cells and the yolk which
There is no sharp distinction between these cells and the yolk which
they are doubtless helping to elaborate into nutritive supplies for the
they are doubtless helping to elaborate into nutritive supplies for the
growing blastodisc. Obviously the blastula here, which consists of a.
growing blastodisc. Obviously the blastula here, which consists of a.
blastodisc grading into shallow cells covering the yolk mass and sepa-
blastodisc grading into shallow cells covering the yolk mass and separated by the segmentation cavity from the yolk-laden cells beneath it,
rated by the segmentation cavity from the yolk-laden cells beneath it,
has points of marked similarity with the telolecithal type of the lamprey.
has points of marked similarity with the telolecithal type of the lamprey.


   
   


FIG. 45. A, B. cleavage stages of Potromyzon fluviatilis; C, D, cleavage stages of Prim-
fiG. 45. A, B. cleavage stages of Potromyzon fluviatilis; C, D, cleavage stages of Primmyzon. plancri. (Redrawn from Ziegler, from Hatschek.)
myzon. plancri. (Redrawn from Ziegler, from Hatschek.)


The inner yolk-containing cells of the latter are not represented in the
The inner yolk-containing cells of the latter are not represented in the
sturgeon, in the yolk of which no cell boundaries are to be distinguished
sturgeon, in the yolk of which no cell boundaries are to be distinguished
although the outer polygonal cells of the yolk hemisphere possess divid-
although the outer polygonal cells of the yolk hemisphere possess dividing nuclei. The formation of the body of the embryo is more distinctly
ing nuclei. The formation of the body of the embryo is more distinctly
limited to the blastodisc in the case of the sturgeon.
limited to the blastodisc in the case of the sturgeon.


Line 2,884: Line 2,653:
vertical furrows appear near the apical pole and extend downward.
vertical furrows appear near the apical pole and extend downward.
The next cleavage is the meridional one, cutting off thus a group of
The next cleavage is the meridional one, cutting off thus a group of
eight micromeres. At the next division these then divide into a super-
eight micromeres. At the next division these then divide into a superficial and a deeper segment and the macromeres divide by vertical
ficial and a deeper segment and the macromeres divide by vertical
furrows. A new latitudinal furrow cuts off additional micromeres and
furrows. A new latitudinal furrow cuts off additional micromeres and
VERTEBRATES 79
VERTEBRATES 79
Line 2,899: Line 2,667:
B
B


FIG 46 Cleavage of Amza calm (Redrawn from Ziegler, after Whitman and
fiG 46 Cleavage of Amza calm (Redrawn from Ziegler, after Whitman and
Eycleshymer )
Eycleshymer )


Line 2,914: Line 2,682:


very sharply apparent have meroblastic cleavage, in the cases under
very sharply apparent have meroblastic cleavage, in the cases under
consideration here, of the discoidal type. The first group of the verte-
consideration here, of the discoidal type. The first group of the vertebrates in which discoidal cleavage occurs is the Myxinoidae. Of the
brates in which discoidal cleavage occurs is the Myxinoidae. Of the
myxinoids the development of Bdellostoma is best known. It has been
myxinoids the development of Bdellostoma is best known. It has been
studied by a' number of investigators, notably by Doflein and by Dean.
studied by a' number of investigators, notably by Doflein and by Dean.
The egg is quite large, being in the neighborhood of an inch long and
The egg is quite large, being in the neighborhood of an inch long and
shaped something like a banana. It is well filled with dense yolk and the
shaped something like a banana. It is well filled with dense yolk and the
germinal disc is limited to one end. Its cleavage is very similar to that of
germinal disc is limited to one end. Its cleavage is very similar to that of
the bony fishes which are shortly to be described. The first two furrows
the bony fishes which are shortly to be described. The first two furrows
are approximately meridional, but irregularities begin with the direction
are approximately meridional, but irregularities begin with the direction
of the third furrow and very shortly the arrangement of the furrows is
of the third furrow and very shortly the arrangement of the furrows is
Line 2,940: Line 2,707:
Fm 47 Egg of the gm PM the endoderm is separated off and with it
Fm 47 Egg of the gm PM the endoderm is separated off and with it
Iaerndoetcue osemr»: In (leavaLt(' mesoderm. A gastrula cavity is not present.
Iaerndoetcue osemr»: In (leavaLt(' mesoderm. A gastrula cavity is not present.
  £‘°"I°r' "W" Thus there is no definite end to the processes
  £‘°"I°r' "W" Thus there is no definite end to the processes


of cleavage and blastula formation after
of cleavage and blastula formation after
Line 2,950: Line 2,717:


So far as known all selachian eggs are extremely meroblastic and
So far as known all selachian eggs are extremely meroblastic and
have discoidal cleavage. If a member of this group of fishes should be
have discoidal cleavage. If a member of this group of fishes should be
found with small holoblastie eggs, it would be a matter of considerable
found with small holoblastie eggs, it would be a matter of considerable
interest from the standpoint of the gradual adaptations which accomplish
interest from the standpoint of the gradual adaptations which accomplish
those modifications that are secondary to yolk accumulation. Dean has
those modifications that are secondary to yolk accumulation. Dean has
found a condition in the shark, Cestraczon, which suggests the approach
found a condition in the shark, Cestraczon, which suggests the approach
of cleavage to the total, unequal type as described for Amw and Lepr-
of cleavage to the total, unequal type as described for Amw and Leprdosteus. Among the selachians are found genera which are viviparous as
dosteus. Among the selachians are found genera which are viviparous as


well as others which are oviparous. The former include, among others,
well as others which are oviparous. The former include, among others,
Line 2,971: Line 2,737:
   
   


FIG. 48. (‘leav-age stages of Bdelloslcmuz stouti. (Redrawn from Ziegler. after Dean.)
fiG. 48. (‘leav-age stages of Bdelloslcmuz stouti. (Redrawn from Ziegler. after Dean.)
A, B, 0. surface views; D, section through edge of blustoderm showing dorsal lip.
A, B, 0. surface views; D, section through edge of blustoderm showing dorsal lip.


ropy liquid, pale yellowish with perhaps a greenish cast. Our knowledge
ropy liquid, pale yellowish with perhaps a greenish cast. Our knowledge
of the early development of the selachian goes back chiefly to Ruckcrt.
of the early development of the selachian goes back chiefly to Ruckcrt.


In a number of selachians the fertilization process is completed and
In a number of selachians the fertilization process is completed and
the fusion nucleus undergoes two mitoses before any cytoplasmic divi-
the fusion nucleus undergoes two mitoses before any cytoplasmic division is to be seen, although there are exceptions to this condition. The
sion is to be seen, although there are exceptions to this condition. The
first furrow then makes its appearance as a slight groove across the
first furrow then makes its appearance as a slight groove across the
disc and a second follows more or less at right angles to it. It is an interesting deviation from the expected sequence of events that oftentimes
disc and a second follows more or less at right angles to it. It is an inter-
the second furrow corresponds to the first nuclear division. The divisions
esting deviation from the expected sequence of events that oftentimes
the second furrow corresponds to the first nuclear division. The divisions
continue, and by the time the 16-cell stage has been reached the furrows
continue, and by the time the 16-cell stage has been reached the furrows
separating the blastomeres form a network over the surface of the egg.
separating the blastomeres form a network over the surface of the egg.
FIG. 49. Cleavage of A. Torpedo ocellata (16 ce1ls), B, C, Scyllmm canicula. the dog
fiG. 49. Cleavage of A. Torpedo ocellata (16 ce1ls), B, C, Scyllmm canicula. the dog
shark (64 and 145 cells respectively) (Rod:-awn from Zwgler, nftu Ruchert)
shark (64 and 145 cells respectively) (Rod:-awn from Zwgler, nftu Ruchert)
VERTEBRATES 83
VERTEBRATES 83


The direction of the cleavage spindles in the fifth division is such that
The direction of the cleavage spindles in the fifth division is such that
part of the cells are cut off under the others and of the 32 blastomeres,
part of the cells are cut off under the others and of the 32 blastomeres,


one sees at most only 20 to 24. In each case the peripheral divisions do
one sees at most only 20 to 24. In each case the peripheral divisions do


FIG. 50. Sections through 16- 64-cell stages and through hlastoderm at the end of the
fiG. 50. Sections through 16- 64-cell stages and through hlastoderm at the end of the
cleavage period. (Redrawn from Ziegler, after Ruchert.)
cleavage period. (Redrawn from Ziegler, after Ruchert.)


In Fig. C the posterior is toward the right, and tho blastoderm, cleavage cavity,bl.,
In fig. C the posterior is toward the right, and tho blastoderm, cleavage cavity,bl.,
periblast cells, p., and supemumerary spermatozoa, 3., are shown.
periblast cells, p., and supemumerary spermatozoa, 3., are shown.


Line 3,010: Line 2,774:
blastodisc consists of 128 cells, it is said that about 70 of these are at the
blastodisc consists of 128 cells, it is said that about 70 of these are at the
surface. In more advanced stages of cleavage the blastococle appears at
surface. In more advanced stages of cleavage the blastococle appears at
first as a space beneath the growing disc. This completes the formation
first as a space beneath the growing disc. This completes the formation
of the blastula.
of the blastula.


C
C


FIG 51 Comparative diagrams of holoblastic and dlS(‘0ld'll eggs (Redrawn from
fiG 51 Comparative diagrams of holoblastic and dlS(‘0ld'll eggs (Redrawn from
Ziegler, after Boaz )
Ziegler, after Boaz )


Line 3,023: Line 2,787:


During the formation of the blastula there are to be observed around
During the formation of the blastula there are to be observed around
its edge, on the floor of the blastula cavity, nuclei scattered heie and
its edge, on the floor of the blastula cavity, nuclei scattered heie and
there singly or in groups. These differ in appearance from the nuclei of
there singly or in groups. These differ in appearance from the nuclei of
the blastomeres, in that the chromatin is arranged in thicker masses and
the blastomeres, in that the chromatin is arranged in thicker masses and
Line 3,037: Line 2,801:
blastoderm and is continuous with the yolk. They are concerned with the
blastoderm and is continuous with the yolk. They are concerned with the
nutritive changes involved in utilization of the yolk as food material.
nutritive changes involved in utilization of the yolk as food material.
They disappear in the later stages and take no further part in the forma-
They disappear in the later stages and take no further part in the formation of the embryo proper.
tion of the embryo proper.


The homology of the diseoidal type of cleavage as shown by the
The homology of the diseoidal type of cleavage as shown by the
Line 3,046: Line 2,809:
the small-celled animal half of the amphibian egg, a comparison which
the small-celled animal half of the amphibian egg, a comparison which
suggests the reason why the ectoderm of the amphibian is many-celled
suggests the reason why the ectoderm of the amphibian is many-celled
in thickness. In the amphibian egg the floor of the blastocoele is a mass
in thickness. In the amphibian egg the floor of the blastocoele is a mass
of large yolk-filled cells; in selachians it is a layer of sub—blastocoele
of large yolk-filled cells; in selachians it is a layer of sub—blastocoele
endoderm covering the yolk sphere and the scattered periblast nuclei.
endoderm covering the yolk sphere and the scattered periblast nuclei.
The linings or the floor coverings of the blastocoeles in the two cases
The linings or the floor coverings of the blastocoeles in the two cases
are homologous, and periblast plus yolk cells of the selachians is homol-
are homologous, and periblast plus yolk cells of the selachians is homologous to the large, yolk-filled endoderm cells of the amphibian. In the
ogous to the large, yolk-filled endoderm cells of the amphibian. In the
gastrula stage this homology is emphasized by the fact that the gastrular
gastrula stage this homology is emphasized by the fact that the gastrular
invagination takes place at a point which is the morphological equivalent
invagination takes place at a point which is the morphological equivalent
Line 3,059: Line 2,821:
These comparisons serve to point out that there is much less of a
These comparisons serve to point out that there is much less of a
distinction between the cleavage types of holoblastic and meroblastic
distinction between the cleavage types of holoblastic and meroblastic
eggs than seems to be the case upon superficial observation.
eggs than seems to be the case upon superficial observation.


The cleavage of the teleosts has been described for a great many
The cleavage of the teleosts has been described for a great many
Line 3,068: Line 2,830:
the eggs are uniformly small, varying‘ in size from that of a small pea
the eggs are uniformly small, varying‘ in size from that of a small pea
to that of a pinhead. There are a few exceptions to this statement among
to that of a pinhead. There are a few exceptions to this statement among
some fresh-water fishes, and these, together with the sharp segregation
some fresh-water fishes, and these, together with the sharp segregation
of yolk and protoplasm, suggest that in ancestral forms the yolk may
of yolk and protoplasm, suggest that in ancestral forms the yolk may
have been very much larger in quantity and the egg more comparable in
have been very much larger in quantity and the egg more comparable in
size to that of a selachian or of a bird. In most selachians the yolk is
size to that of a selachian or of a bird. In most selachians the yolk is
spherical and the protoplasmic layer which before fertilization shows
spherical and the protoplasmic layer which before fertilization shows
but very slight localization accumulates at one place as a distinct eleva-
but very slight localization accumulates at one place as a distinct elevation, after the entrance of the sperm. During polar body formation and
tion, after the entrance of the sperm. During polar body formation and
cleavage, the protoplasmic portion is sharply distinguished from the
cleavage, the protoplasmic portion is sharply distinguished from the
yolk, but with the growth of the blastodisc the separation becomes less
yolk, but with the growth of the blastodisc the separation becomes less
Line 3,080: Line 2,841:


marked and at length the germ layers completely enclose the yolk mass.
marked and at length the germ layers completely enclose the yolk mass.
The yolk itself is at first in the form of spherules, but at the time of
The yolk itself is at first in the form of spherules, but at the time of
fertilization these run together to form a single spherical mass of glassy
fertilization these run together to form a single spherical mass of glassy
transparency. In many eggs, oil droplets are to be noted within the yolk
transparency. In many eggs, oil droplets are to be noted within the yolk
Line 3,090: Line 2,851:
pb., perxblast.
pb., perxblast.


development. In the great majority of marine fishes the eggs float ai
development. In the great majority of marine fishes the eggs float ai
the surface of the water during their early stages.
the surface of the water during their early stages.


Line 3,096: Line 2,857:
the segmentation of the germinal disc of the teleost egg does not differ
the segmentation of the germinal disc of the teleost egg does not differ
in principle from that of the other types having discoidal cleavage. The
in principle from that of the other types having discoidal cleavage. The
first two furrows are meridional, the first one appearing in the shorter
first two furrows are meridional, the first one appearing in the shorter
diameter of the ellipse, the form assumed by the blastodisc with the
diameter of the ellipse, the form assumed by the blastodisc with the
beginning of cleavage. The third and fourth furrows are vertical, becom-
beginning of cleavage. The third and fourth furrows are vertical, becomVERTEBRATES 87
VERTEBRATES 87


ing arranged so that they are practically parallel to the first and second.
ing arranged so that they are practically parallel to the first and second.
Thus, it is the rule that in the 16~ce1l stage the teleost egg consists of
Thus, it is the rule that in the 16~ce1l stage the teleost egg consists of
four rows of four cells each. In section it is to be noted that the first
four rows of four cells each. In section it is to be noted that the first
furrows do not extend to the yolk, but a continuous basal layer of pro-
furrows do not extend to the yolk, but a continuous basal layer of protoplasm is left between the cleaving blastoderm and the yolk. The
toplasm is left between the cleaving blastoderm and the yolk. The
blastocoele appears at the end of the fourth cleavage by the third and
blastocoele appears at the end of the fourth cleavage by the third and


FIG. 53 Cleavage and formation of the blastoderm of the sea bass, Scrranus strarws
fiG. 53 Cleavage and formation of the blastoderm of the sea bass, Scrranus strarws
(Redrawn from Ziegler, after H B Wilson )
(Redrawn from Ziegler, after H B Wilson )


Line 3,115: Line 2,874:
fourth furrows curving around in their deeper portions to meet the
fourth furrows curving around in their deeper portions to meet the
preceding division planes which were perpendicular to the surface. Thus
preceding division planes which were perpendicular to the surface. Thus
the 32-cell stage consists of a layer of superficial cells and a deeper-lying
the 32-cell stage consists of a layer of superficial cells and a deeper-lying
layer.
layer.


The next division results in the blastoderm becoming three-layered,
The next division results in the blastoderm becoming three-layered,
and in the fourth another layer is added, while at the same time the
and in the fourth another layer is added, while at the same time the
superficial cells also become more numerous. In subsequent stages it
superficial cells also become more numerous. In subsequent stages it
is seen that the cells of the basal portion will divide less rapidly but with
is seen that the cells of the basal portion will divide less rapidly but with
88 MEROBLASTIC TYPES OF CLEAVAGE
88 MEROBLASTIC TYPES OF CLEAVAGE
Line 3,134: Line 2,893:
numerous, are strangely lobed, and present appearances which are unlike
numerous, are strangely lobed, and present appearances which are unlike


FIG. 54. Cleavage of the salmon, Salmo salar. (After Ziegler.)
fiG. 54. Cleavage of the salmon, Salmo salar. (After Ziegler.)
A, 16-cell stage; B, blastula.
A, 16-cell stage; B, blastula.


Line 3,157: Line 2,916:
The eggs of birds and reptiles are very much alike in all fundamental
The eggs of birds and reptiles are very much alike in all fundamental
respects and resemble also those of the elasmobranchs. The amount of
respects and resemble also those of the elasmobranchs. The amount of
yolk present is large and the protoplasm and yolk are distinctly sepa-
yolk present is large and the protoplasm and yolk are distinctly separated from each other, although the segregation is less sharp. The germinal disc is more intimately connected with the yolk and at its edges
rated from each other, although the segregation is less sharp. The ger-
minal disc is more intimately connected with the yolk and at its edges


   
   


FIG. 55. Cross sections through the germ disc of the teleost, Ctenolabrus. (Redrawn from
fiG. 55. Cross sections through the germ disc of the teleost, Ctenolabrus. (Redrawn from
Korschelt and Heider. after Agassiz.)
Korschelt and Heider. after Agassiz.)


gradually passes over into yolk in distinction to the sharp line of separa-
gradually passes over into yolk in distinction to the sharp line of separation noted in the teleosts. The eggs of birds have been studied by many
tion noted in the teleosts. The eggs of birds have been studied by many
investigators and the early stages are quite thoroughly understood.
investigators and the early stages are quite thoroughly understood.
The general procedure is similar to that of elasmobranchs, but the early
The general procedure is similar to that of elasmobranchs, but the early
furrows are more regular, the first two being meridional and at right
furrows are more regular, the first two being meridional and at right
angles to each other. They are then followed by a pair of vertical fur-
angles to each other. They are then followed by a pair of vertical furrows. The irregularities are many, however, and in certain species they
rows. The irregularities are many, however, and in certain species they
occur earlier than in others. In the early cleavage of the chick, for
occur earlier than in others. In the early cleavage of the chick, for
example, Patterson found that the third cleavage furrows may not be
example, Patterson found that the third cleavage furrows may not be
clearly recognizable. Accessory sperms enter the eggs of birds, and the
clearly recognizable. Accessory sperms enter the eggs of birds, and the
phenomenon known as accessory cleavage is due to an attempt at seg-
phenomenon known as accessory cleavage is due to an attempt at segmentation on the part of the yolk in which these accessory sperm nuclei
mentation on the part of the yolk in which these accessory sperm nuclei
90 MEROBLASTIC TYPES OF CLEAVAGE
90 MEROBLASTIC TYPES OF CLEAVAGE


Line 3,189: Line 2,943:
new central cells are constantly cut off and new marginal cells arise
new central cells are constantly cut off and new marginal cells arise
peripherally. With the formation of the central cells, due to horizontal
peripherally. With the formation of the central cells, due to horizontal
cleavages, a space is formed between them and the underlying proto-
cleavages, a space is formed between them and the underlying protoplasm. This space becomes filled with fluid and is the segmentation
plasm. This space becomes filled with fluid and is the segmentation
cavity. In general the processes already described for the formation of
cavity. In general the processes already described for the formation of
discoidal cleavage in the lower vertebrates also apply to that in reptiles
discoidal cleavage in the lower vertebrates also apply to that in reptiles
Line 3,196: Line 2,949:
   
   


FIG. 56. Periblast cells showing many mitoses from a. cleavage stage of Belone. (Redrawn
fiG. 56. Periblast cells showing many mitoses from a. cleavage stage of Belone. (Redrawn
from Ziegler, after Kopsch.)
from Ziegler, after Kopsch.)


Line 3,206: Line 2,959:
In bringing to a close the sections dealing with cleavage it is necessary
In bringing to a close the sections dealing with cleavage it is necessary
to mention certain irregular cleavages which do not fall in any of the
to mention certain irregular cleavages which do not fall in any of the
classes previously discussed, or at least are so modified that their rela-
classes previously discussed, or at least are so modified that their relationships have not yet been certainly made out. The cleavages of some
tionships have not yet been certainly made out. The cleavages of some
sponges and of some coelenteratcs, though undoubtedly fundamentally
sponges and of some coelenteratcs, though undoubtedly fundamentally
radial, present variations from the normal type that are so great as to
radial, present variations from the normal type that are so great as to
be understood only with difficulty. The cleavages of the trematodes
be understood only with difficulty. The cleavages of the trematodes
and cestodes are among the most irregular of all forms. The cleavages of
and cestodes are among the most irregular of all forms. The cleavages of
brachiopods and of bryozoans, although total and equal, do not follow
brachiopods and of bryozoans, although total and equal, do not follow
Line 3,220: Line 2,972:


Among the more important accounts of the subjects contained in this chapter
Among the more important accounts of the subjects contained in this chapter
are the following: Superficial: Brauer, Korschelt and Heider, Bigelow, Heider on
are the following: Superficial: Brauer, Korschelt and Heider, Bigelow, Heider on
Hydrophilus, Cano; Cephalopods: Watase, Vialleton; Vertebrates: Dean, Whitman
Hydrophilus, Cano; Cephalopods: Watase, Vialleton; Vertebrates: Dean, Whitman
and Eycleshymer, H. V. Wilson, Agassiz, Kopsch, Patterson. These works are cited
and Eycleshymer, H. V. Wilson, Agassiz, Kopsch, Patterson. These works are cited
Line 3,231: Line 2,983:
as a hollow spherical embryo consisting of a single layer of cells, and
as a hollow spherical embryo consisting of a single layer of cells, and
indeed the most typical blastulae are so constructed. Actually, however,
indeed the most typical blastulae are so constructed. Actually, however,
there are many different forms of blastulae, of which the hollow, one-
there are many different forms of blastulae, of which the hollow, onelayered type is but a single one, and these different types of blastulae are
layered type is but a single one, and these different types of blastulae are
now to be .considered.
now to be .considered.


Line 3,240: Line 2,991:
yolk present in the egg, a factor which differs widely in the several
yolk present in the egg, a factor which differs widely in the several
groups of animals. For the same reasons it is to be expected that the
groups of animals. For the same reasons it is to be expected that the
different cleavage types will lead to difierent kinds of blastulae, and this
different cleavage types will lead to difierent kinds of blastulae, and this
expectation is borne out. There are seven types of blastulae as follows:
expectation is borne out. There are seven types of blastulae as follows:
coeloblastula, stereoblastula, morula, placula, amphiblastula, superficial
coeloblastula, stereoblastula, morula, placula, amphiblastula, superficial
blastula, and discoblastula.
blastula, and discoblastula.


Line 3,248: Line 2,999:


The simplest type of blastula is that known as a eoeloblastula, the
The simplest type of blastula is that known as a eoeloblastula, the
kind having a cavity at the center. Coeloblastulae may be further sub-
kind having a cavity at the center. Coeloblastulae may be further subdivided, depending upon the size of the segmentation cavity and upon
divided, depending upon the size of the segmentation cavity and upon
the relative sizes of the cells. They include both equal and unequal
the relative sizes of the cells. They include both equal and unequal
blastulae, distinguished as to whether the cells are of uniform size
blastulae, distinguished as to whether the cells are of uniform size
throughout the embryo, and each of these is again of two distinct sub-
throughout the embryo, and each of these is again of two distinct subtypes, depending upon the size of the blastocoele cavity. If the altitude
types, depending upon the size of the blastocoele cavity. If the altitude
of the cells is low so that they resemble a sort of cuboidal epithelium,
of the cells is low so that they resemble a sort of cuboidal epithelium,
then necessarily the cavity is very large, and we have the simplest type,
then necessarily the cavity is very large, and we have the simplest type,
Line 3,284: Line 3,033:
   
   


FIG 57 Blastula of amphioxus. Fm 58 (‘oc[0b1astu1,; of 30,.
fiG 57 Blastula of amphioxus. Fm 58 (‘oc[0b1astu1,; of 30,.
(After C0I‘f0flWm0) mtta (Redrawn from Korsehelt
(After C0I‘f0flWm0) mtta (Redrawn from Korsehelt
and Heider, after Hertwig )
and Heider, after Hertwig )


which rather closely approach the coeloblastula type.) Gastrula forma-
which rather closely approach the coeloblastula type.) Gastrula formation in types having coeloblastulae is usually by invagination; however,
tion in types having coeloblastulae is usually by invagination; however,
the method to be discussed presently, polar ingrowth, sometimes applies
the method to be discussed presently, polar ingrowth, sometimes applies
to this type.
to this type.
Line 3,308: Line 3,056:
STEREOBLASTULA 93
STEREOBLASTULA 93


Therefore we should expect to find it in the polyclads, annelids, molluscs,
Therefore we should expect to find it in the polyclads, annelids, molluscs,
Bryozoa (Fig. 59) and among the holoblastic eggs of vertebrates (Fig. 26).
Bryozoa (fig. 59) and among the holoblastic eggs of vertebrates (fig. 26).
The blastulae of vertebrates can readily be distinguished from the other
The blastulae of vertebrates can readily be distinguished from the other
types, for in them we always find a great many cells in the wall. In the
types, for in them we always find a great many cells in the wall. In the
vertebrates, epithelium is differentiated into many layers of cells. It is as
vertebrates, epithelium is differentiated into many layers of cells. It is as
if this differentiation that is characteristic of adult vertebrates makes
if this differentiation that is characteristic of adult vertebrates makes
Line 3,317: Line 3,065:
consists of many cells, and each germ layer, ectoderm and endoderm, is
consists of many cells, and each germ layer, ectoderm and endoderm, is
several cells thick. This characteristic is clearly seen in the amphibian
several cells thick. This characteristic is clearly seen in the amphibian
type, the frog and salamander, with such modifications as the difference
type, the frog and salamander, with such modifications as the difference
in yolk would involve. Unequal coeloblastulae are derived from unequal
in yolk would involve. Unequal coeloblastulae are derived from unequal


Line 3,325: Line 3,073:
   
   


FIG 59 Unequal eoeloblastula FIG 60 Equal stereoblastula
fiG 59 Unequal eoeloblastula fiG 60 Equal stereoblastula
of Flustrella hzsmda (Redrawn of Lucernaruz (Redrawn from
of flustrella hzsmda (Redrawn of Lucernaruz (Redrawn from
from Korschelt and Herder, after Kcrsehelt and Heider, after
from Korschelt and Herder, after Kcrsehelt and Heider, after
Pace) Bergh)
Pace) Bergh)
Line 3,337: Line 3,085:
The stereoblastula (the term means a solid blastula) is obviously
The stereoblastula (the term means a solid blastula) is obviously
derived from the coeloblastula, and may be equal or unequal, depending
derived from the coeloblastula, and may be equal or unequal, depending
upon whether it is produced from the equal or unequal type of c0elo-
upon whether it is produced from the equal or unequal type of c0eloblastula. If the cleavage cavity in the type of equal coeloblastula with
blastula. If the cleavage cavity in the type of equal coeloblastula with
small blastoeoele continues to be reduced until it vanishes, we have the
small blastoeoele continues to be reduced until it vanishes, we have the
equal type of stereoblastula such as is found in Lucernarza. With increase
equal type of stereoblastula such as is found in Lucernarza. With increase
in volume of cells and decrease in size of blastocoele we get a stereo-
in volume of cells and decrease in size of blastocoele we get a stereoblastula.
blastula.


More common than this, however, is the unequal type of stereoblastula
More common than this, however, is the unequal type of stereoblastula
such as we find in Crepzdula. The unequal stereoblastula is derived
such as we find in Crepzdula. The unequal stereoblastula is derived
through unequal cleavage and may occur either in the spiral types or the
through unequal cleavage and may occur either in the spiral types or the
more extreme of the bilateral types. Gastrulation regularly occurs in this
more extreme of the bilateral types. Gastrulation regularly occurs in this
Line 3,361: Line 3,107:
strictly radial type there is some reason for that description, but we do
strictly radial type there is some reason for that description, but we do
not speak now of a morula stage. However, in some types there are
not speak now of a morula stage. However, in some types there are
formed blastulae which can best be described as morulae or solid blas-
formed blastulae which can best be described as morulae or solid blastulae. In Clava we have an example of the solid blastula which illustrates
tulae. In Clava we have an example of the solid blastula which illustrates
the difference from the stereoblastula type, for inside the morula there
the difference from the stereoblastula type, for inside the morula there
are cells, whereas in the stereoblastula there were no cells which did not
are cells, whereas in the stereoblastula there were no cells which did not
Line 3,368: Line 3,113:
   
   


FIG. 61. Unequal storeoblustulu of Crepidula. (After Conklin.)
fiG. 61. Unequal storeoblustulu of Crepidula. (After Conklin.)


have a boundary at the surface of the egg. Superficially the two are quite
have a boundary at the surface of the egg. Superficially the two are quite
alike, but actually there is an important distinguishing feature. The
alike, but actually there is an important distinguishing feature. The
morula is produced by a characteristic shifting of the spindle position
morula is produced by a characteristic shifting of the spindle position
Line 3,377: Line 3,122:
that the new cleavage plane divides the cell in such a way that part of it
that the new cleavage plane divides the cell in such a way that part of it
touches the surface and part the center of the egg. However, the morula
touches the surface and part the center of the egg. However, the morula
comes about by a shifting of the spindle to a radial rather than a para-
comes about by a shifting of the spindle to a radial rather than a paratangential position, and the result is that some of the daughter cells
tangential position, and the result is that some of the daughter cells
touch the surface and others are only in the interior of the egg. So the
touch the surface and others are only in the interior of the egg. So the
morula, although superficially similar to the stereoblastula, is really a
morula, although superficially similar to the stereoblastula, is really a
distinct and different type. Morulae occur chiefly in coelenterates.
distinct and different type. Morulae occur chiefly in coelenterates.


D. PLACULA
D. PLACULA


The placula presents another kind of modification which has been
The placula presents another kind of modification which has been
produced from the equal coeloblastula. Let us suppose that, instead of
produced from the equal coeloblastula. Let us suppose that, instead of
SUPERFICIAL BLASTULA 95
SUPERfiCIAL BLASTULA 95


the cavity vanishing, the egg is compressed from the animal to the vege-
the cavity vanishing, the egg is compressed from the animal to the vegetative pole. The result would be a flattened blastula consisting of two
tative pole. The result would be a flattened blastula consisting of two
plates of cells. This is the placula and is found especially well developed
plates of cells. This is the placula and is found especially well developed
in the ascidians and to a less extent in the nematodes. The edge of the
in the ascidians and to a less extent in the nematodes. The edge of the
Line 3,400: Line 3,143:
   
   


Tie. 62 Morula of (‘lava 9qua- FIG 63 Placula of Cynthia pamta (After
Tie. 62 Morula of (‘lava 9qua- fiG 63 Placula of Cynthia pamta (After
mam (Redmwn from Korschelt and Conklin)
mam (Redmwn from Korschelt and Conklin)
Heider, after Harm )
Heider, after Harm )


Gastrulation takes place by two different methods, epiboly and the
Gastrulation takes place by two different methods, epiboly and the
sinking in of the flattened plates; that is, it is accomplished by a combi-
sinking in of the flattened plates; that is, it is accomplished by a combination of epiboly and invagination.
nation of epiboly and invagination.


E. AMPHIBLASTULA
E. AMPHIBLASTULA


The amphiblastula of the sponge is of somewhat different type. This
The amphiblastula of the sponge is of somewhat different type. This
structure was first described by Haeckel for the free-swimming larval
structure was first described by Haeckel for the free-swimming larval
stage of calcareous sponges, and hence does not strictly correspond to
stage of calcareous sponges, and hence does not strictly correspond to
other blastulae which we have described. This larval form, however, is
other blastulae which we have described. This larval form, however, is
Line 3,419: Line 3,161:
important although it is necessary to include it.
important although it is necessary to include it.


F. SUPERFICIAL BLASTULA
F. SUPERfiCIAL BLASTULA


The superficial blastula, or periblastula, is characteristic of those
The superficial blastula, or periblastula, is characteristic of those
forms having superficial cleavage, an example of which is the crab,
forms having superficial cleavage, an example of which is the crab,
Dromza (Figs. 36f and 37d). The result of superficial cleavage is the
Dromza (figs. 36f and 37d). The result of superficial cleavage is the
formation of a layer of cells around the inner yolk mass. There is no
formation of a layer of cells around the inner yolk mass. There is no
blastocoele and it is usual to say that the blastocoele is occupied by the
blastocoele and it is usual to say that the blastocoele is occupied by the
Line 3,429: Line 3,171:


yolk mass. But the case is not quite so simple. Actually it will be recalled
yolk mass. But the case is not quite so simple. Actually it will be recalled
that the superficial cleavage resulted in the formation of blastomeres
that the superficial cleavage resulted in the formation of blastomeres
which at first were continuous with the yolk at their inner end. These
which at first were continuous with the yolk at their inner end. These
blastomeres presently are completely out off, a protoplasmic blastomere
blastomeres presently are completely out off, a protoplasmic blastomere
being separated from the yolk-laden inner mass. Their inner ends, or the
being separated from the yolk-laden inner mass. Their inner ends, or the
Line 3,443: Line 3,185:
   
   


FIG 64. Amphiblastula of Sycandra mphanuv (Redrawn from Korschelt and Helder.
fiG 64. Amphiblastula of Sycandra mphanuv (Redrawn from Korschelt and Helder.
after Schulze )
after Schulze )


Line 3,449: Line 3,191:
around these nuclei, a process of division which is often spoken of as the
around these nuclei, a process of division which is often spoken of as the
yolk cleavage. But by some these nuclei are regarded as endoderm.
yolk cleavage. But by some these nuclei are regarded as endoderm.
If this latter VIOW is adopted, there would be no such thing as a super-
If this latter VIOW is adopted, there would be no such thing as a superficial blastula because the embryo would consist mostly of two cell layers,
ficial blastula because the embryo would consist mostly of two cell layers,
the outer being ectoderm, and these internal yolk cells endoderm. This
the outer being ectoderm, and these internal yolk cells endoderm. This
designation of these cells as endoderm has not, however, come into
designation of these cells as endoderm has not, however, come into
general use. Rather we say that the superficial is a true blastula.
general use. Rather we say that the superficial is a true blastula.


G. DISCOBLASTULA
G. DISCOBLASTULA


Finally we have the discoblastula, the end stage of the eggs having dis-
finally we have the discoblastula, the end stage of the eggs having discoidal cleavage. It is derived from the unequal coeloblastula (fig. 52)
coidal cleavage. It is derived from the unequal coeloblastula (Fig. 52)
upon the assumption that the yolk becomes so abundant and so dense as
upon the assumption that the yolk becomes so abundant and so dense as
DISCO BLASTULA 97
DISCO BLASTULA 97
Line 3,465: Line 3,205:
half of the egg. Recalling that discoidal cleavage occurs both in the
half of the egg. Recalling that discoidal cleavage occurs both in the
vertebrates and invertebrates we should say at once that discoblastulae
vertebrates and invertebrates we should say at once that discoblastulae
are of two sorts, the vertebrate type (Fig. 55) and the invertebrate
are of two sorts, the vertebrate type (fig. 55) and the invertebrate
(Fig. 44); the latter consists of the single layer of cells which is found in
(fig. 44); the latter consists of the single layer of cells which is found in
all invertebrates having diseoidal cleavage in contrast to the former
all invertebrates having diseoidal cleavage in contrast to the former
which is of many cells. Usually in all types having discoidal cleavage
which is of many cells. Usually in all types having discoidal cleavage
Line 3,486: Line 3,226:
Among the more important accounts of the subjects contained in this chapter
Among the more important accounts of the subjects contained in this chapter
are the following: Korschelt and Heider, Minehin, Maas, Hertwig, Wilson, Conklin,
are the following: Korschelt and Heider, Minehin, Maas, Hertwig, Wilson, Conklin,
Schultze, Brauer, Whitman and Eyclcshymer, O. Herting, Ziegler, Brooks and Bit-
Schultze, Brauer, Whitman and Eyclcshymer, O. Herting, Ziegler, Brooks and Bittenhaus. These works are cited in full in the bibliography on page 406.
tenhaus. These works are cited in full in the bibliography on page 406.




Line 3,511: Line 3,250:
    
    


FIG 65 Two stages in the gastrula-
fiG 65 Two stages in the gastrulation of Terebratulma septentnonalts (After
tion of Terebratulma septentnonalts (After
Conklm.)
Conklm.)


cells, the next stage in the develop-
cells, the next stage in the development of the embryo is the formation
ment of the embryo is the formation
of a gastrula. The gastrula develops
of a gastrula. The gastrula develops
from the blastula by the differentia-
from the blastula by the differentiation of two layers of cells, an outer
tion of two layers of cells, an outer
or cctodermal layer, and an inner
or cctodermal layer, and an inner
or endodermal layer. From the
or endodermal layer. From the
eetoderm develops the nervous
eetoderm develops the nervous
system and the outer parts of the
system and the outer parts of the
future animal, and from the en-
future animal, and from the endoderm comes the lining of the
doderm comes the lining of the
alimentary canal.
alimentary canal.


There are several different types
There are several different types
of gastrula formation, depending
of gastrula formation, depending
partly on the type of blastula preced-
partly on the type of blastula preceding the gastrula. We shall consider
ing the gastrula. We shall consider
each of these types and describe its
each of these types and describe its
method of formation.
method of formation.
Line 3,539: Line 3,273:
The best-known type of gastrula
The best-known type of gastrula
is the embolie or invaginate gastrula.
is the embolie or invaginate gastrula.
Gastrulae of this kind occur in em-
Gastrulae of this kind occur in embryos with total cleavage, resulting
bryos with total cleavage, resulting
in cells of either equal or slightly
in cells of either equal or slightly
unequal size. The blastula resembles
unequal size. The blastula resembles
Line 3,553: Line 3,286:
EMBOLIC GASTRULATION 99
EMBOLIC GASTRULATION 99


In one part, the vegetative half, the cells are typically larger than else-
In one part, the vegetative half, the cells are typically larger than elsewhere, and sometimes markedly so.
where, and sometimes markedly so.


The first sign of gastrulation is a slight flattening of the vegetative
The first sign of gastrulation is a slight flattening of the vegetative
region. This flattening gradually deepens and the resulting gastrula has
region. This flattening gradually deepens and the resulting gastrula has
the appearance of a rubber ball which has been pushed in at one point
the appearance of a rubber ball which has been pushed in at one point
by pressure with a finger. The inpushing of the cells at the vegetative
by pressure with a finger. The inpushing of the cells at the vegetative
pole continues until this invaginated layer lies close to the cells of the
pole continues until this invaginated layer lies close to the cells of the
outer wall. In this way a two-layered gastrula is formed and two cell
outer wall. In this way a two-layered gastrula is formed and two cell
Line 3,567: Line 3,299:
   
   


FIG. 66. Gastrula of amphioxus. (After Cerfontaine.)
fiG. 66. Gastrula of amphioxus. (After Cerfontaine.)
Oriented with respect to the future embryonic axis.
Oriented with respect to the future embryonic axis.


Line 3,589: Line 3,321:


attempt at migration by the cells of the vegetative half, a process which
attempt at migration by the cells of the vegetative half, a process which
in the last analysis is to be attributed to chemotactic influences. If this
in the last analysis is to be attributed to chemotactic influences. If this
explanation is correct, then the migration of the endodermal cells must
explanation is correct, then the migration of the endodermal cells must
be connected with a change in surface tension at the boundary between
be connected with a change in surface tension at the boundary between
Line 3,601: Line 3,333:
membrane, so that the surface increase of the blastodcrm is possible only
membrane, so that the surface increase of the blastodcrm is possible only
internally. This factor is probably not often effective, for in many cases
internally. This factor is probably not often effective, for in many cases
the egg membrane appears pushed away by the pcrivitelline fluid and the
the egg membrane appears pushed away by the pcrivitelline fluid and the
blastocoele is not an empty cavity but is filled with fluid which would
blastocoele is not an empty cavity but is filled with fluid which would
have to be displaced. (c) The constantly decreasing fluid of the blasto-
have to be displaced. (c) The constantly decreasing fluid of the blastocoele which perhaps exerts a sucking effect on the endodermal plate.
coele which perhaps exerts a sucking effect on the endodermal plate.
We must at the present time regard this factor as of doubtful occurrence and significance.
We must at the present time regard this factor as of doubtful occur-
rence and significance.


The size of that part of the old segmentation cavity or blastocoele
The size of that part of the old segmentation cavity or blastocoele
which remains after gastrulation may be very small, as in amphioxus, or
which remains after gastrulation may be very small, as in amphioxus, or
it may be quite extensive, as in the echinoderms in whose embryos the
it may be quite extensive, as in the echinoderms in whose embryos the
primitive gut is relatively small. The fate of the fluid or gelatinous
primitive gut is relatively small. The fate of the fluid or gelatinous
content of the blastocoele is uncertain; some authors think that it is
content of the blastocoele is uncertain; some authors think that it is
resorbed by the endoderm cells. If this process could be satisfactorily
resorbed by the endoderm cells. If this process could be satisfactorily
Line 3,627: Line 3,357:
placula which then rounds out so that a complete sphere is formed. In
placula which then rounds out so that a complete sphere is formed. In
some cases there is an active increase by epiboly in the ectodermal cells
some cases there is an active increase by epiboly in the ectodermal cells
preceding invagination. This may be one of the causes for the invagina-
preceding invagination. This may be one of the causes for the invagination in placulae, but on the other hand the process may be due to the
tion in placulae, but on the other hand the process may be due to the
same causes that lie back of typical invagination.
same causes that lie back of typical invagination.


Invagination occurs in the following forms: some actinians, some
Invagination occurs in the following forms: some actinians, some
syphopolyps; Sagitta, Pedicellina, brachiopods; Phoronis, nemerteans;
syphopolyps; Sagitta, Pedicellina, brachiopods; Phoronis, nemerteans;
echinoderms; some arthropods, as crayfish, Palimonetes; some insects;
echinoderms; some arthropods, as crayfish, Palimonetes; some insects;
many annelids, as Polygordius, Podarke, Eupomotus; some molluscs, as
many annelids, as Polygordius, Podarke, Eupomotus; some molluscs, as
EPIBOLIC GASTRULATION 101
EPIBOLIC GASTRULATION 101
Line 3,652: Line 3,381:
were approximately equal in size. In many other embryos, however,
were approximately equal in size. In many other embryos, however,


FIG. 67. Gastrulation by epiboly in Crepidula. (After Conklin.)
fiG. 67. Gastrulation by epiboly in Crepidula. (After Conklin.)


there is a great difference in size between the small cells at the upper or
there is a great difference in size between the small cells at the upper or
Line 3,668: Line 3,397:
of the small cells at the animal pole and an overgrowth or migration of
of the small cells at the animal pole and an overgrowth or migration of
these cells down over the larger cells at the vegetative pole. These large
these cells down over the larger cells at the vegetative pole. These large
yolk-filled cells seem to take no active part in the process. The free edge
yolk-filled cells seem to take no active part in the process. The free edge
of the growing cap is called the blastopore, and the protruding yolk-
of the growing cap is called the blastopore, and the protruding yolkfilled cells, the yolk plug. When the overgrowth by the small cells is
filled cells, the yolk plug. When the overgrowth by the small cells is
complete, the blastopore usually closes and the large cells are enclosed.
complete, the blastopore usually closes and the large cells are enclosed.
The small, overgrowing cells are ectodermal and the large yolk cells
The small, overgrowing cells are ectodermal and the large yolk cells
Line 3,694: Line 3,422:
the cells at the animal and vegetative poles.
the cells at the animal and vegetative poles.


Epibolic gastrulation occurs in ctenophores (Fig. 14B), rotifers,
Epibolic gastrulation occurs in ctenophores (fig. 14B), rotifers,
turbellarians, some molluscs, some annelids, and many crustaceans
turbellarians, some molluscs, some annelids, and many crustaceans
including many parasitic copepods.
including many parasitic copepods.
Line 3,718: Line 3,446:
the preceding types.
the preceding types.


The following forms have gastrulation by restricted unipolar ingres-
The following forms have gastrulation by restricted unipolar ingression: some holoblastic Crustacea (some schizopods and Cladocera),
sion: some holoblastic Crustacea (some schizopods and Cladocera),
Ascaris megalocephala and other nematodes, and some molluscs (Patella).
Ascaris megalocephala and other nematodes, and some molluscs (Patella).


Line 3,725: Line 3,452:


In the ciliated blastulae of the coelenterates occurs a second form of
In the ciliated blastulae of the coelenterates occurs a second form of
gastrulation by polar ingrowth. In it there is an elongated, oval or sausage-
gastrulation by polar ingrowth. In it there is an elongated, oval or sausageshaped, free-swimming stage (called
shaped, free-swimming stage (called
a planula) which is really a blastula
a planula) which is really a blastula
with a large blastocoele and with thick-
with a large blastocoele and with thickened cells at the posterior pole. Here
ened cells at the posterior pole. Here
there takes place the migration of cells
there takes place the migration of cells
to a position within the blastula
to a position within the blastula
Line 3,736: Line 3,461:
extends from the pole over the nearby
extends from the pole over the nearby
portion of the embryo. The cells which
portion of the embryo. The cells which
first migrated into the blastocoele lie
first migrated into the blastocoele lie
isolated in the jelly contents but, later,
isolated in the jelly contents but, later,


when migration takes place en masse, Fm. ex. Endoderm formation in ‘the
when migration takes place en masse, Fm. ex. Endoderm formation in ‘the
a plugof cells turns inward from the fgiggigfi 1;;j’;m”“,§,§r;$g;‘“;n';*8',§:§g;';;
a plugof cells turns inward from the fgiggigfi 1;;j’;m”“,§,§r;$g;‘“;n';*8',§:§g;';;
posterior pole and gradually fills the after Patten.)
posterior pole and gradually fills the after Patten.)
 
blastocoele. The migration of cells in-


blastocoele. The migration of cells in
ward is not limited to the vegetative pole, but reaches to neighboring
ward is not limited to the vegetative pole, but reaches to neighboring
parts. There is no interruption in the continuity of cells at the hinder
parts. There is no interruption in the continuity of cells at the hinder
pole, and no gap in the outer superficial cell layer. At the end stage of
pole, and no gap in the outer superficial cell layer. At the end stage of
the gastrulation, there is an embryo with an outer superficial epithelial
the gastrulation, there is an embryo with an outer superficial epithelial
layer and with a solid cell mass filling the interior of the larva. This
layer and with a solid cell mass filling the interior of the larva. This
stage is variously called a stereogastrula or a parenchymella.
stage is variously called a stereogastrula or a parenchymella.


The formation of the gut cavity follows later by dehiscenee. A gradu-
The formation of the gut cavity follows later by dehiscenee. A gradually widening split occurs in the interior of the endoderm cell mass and
ally widening split occurs in the interior of the endoderm cell mass and
later breaks through to the outside, forming the mouth. During this
later breaks through to the outside, forming the mouth. During this
process, the endodermal cells become arranged in a layer.
process, the endodermal cells become arranged in a layer.
Line 3,762: Line 3,485:
process a closed epithelial layer is shifted by infolding to the interior,
process a closed epithelial layer is shifted by infolding to the interior,
and in the ingrowth process the cells of the vegetative half pass inward
and in the ingrowth process the cells of the vegetative half pass inward
as a solid cell mass, later taking on an epithelial character, and develop-
as a solid cell mass, later taking on an epithelial character, and develop104 EN DODERM FORMATION
104 EN DODERM FORMATION


ing a lumen. Metchnikoff concluded that the polar ingression was
ing a lumen. Metchnikoff concluded that the polar ingression was
Line 3,771: Line 3,493:
and gastrulation by polar ingrowth. In many forms, as in Aurelia aurita
and gastrulation by polar ingrowth. In many forms, as in Aurelia aurita


FIG. 69. Endodenn formation by unipolar ingression in the plrmuln of Aequoria accord-
fiG. 69. Endodenn formation by unipolar ingression in the plrmuln of Aequoria according to Claus. (Redruwn from Korschelt and Heider.)
ing to Claus. (Redruwn from Korschelt and Heider.)


and Eupomotus, there are invaginate gastrulae in which the gut lumen
and Eupomotus, there are invaginate gastrulae in which the gut lumen
Line 3,795: Line 3,516:
of cells from several places instead of a single
of cells from several places instead of a single
one on the surface of the blastula. It might
one on the surface of the blastula. It might
be spoken of as apolar ingrowth as distin-
be spoken of as apolar ingrowth as distinguished from that which proceeds from a
guished from that which proceeds from a
single restricted portion of the blastula.
single restricted portion of the blastula.
However, since the processes are so similar
However, since the processes are so similar
to those already described in this section it
to those already described in this section it
seems desirable to assign this type to the
seems desirable to assign this type to the
same division even if it presents some de-
same division even if it presents some departures from the other cases placed here.
partures from the other cases placed here.


Multipolar ingression occurs in coele-
Multipolar ingression occurs in coeleblastulae when cells, few in number at first,
blastulae when cells, few in number at first,
pass inside the embryo from various places
pass inside the embryo from various places
on the surface. The blastocoele is in this
on the surface. The blastocoele is in this
way filled up with endoderm. The resulting
way filled up with endoderm. The resulting
stage is a solidly built mass of cells like a
stage is a solidly built mass of cells like a
morula. It may be called a pseudo-morula,
morula. It may be called a pseudo-morula,
differing from the typical morula in that
differing from the typical morula in that
there is no differentiation of cells in the latter _ Fm. 70. Multipolar ingres-
there is no differentiation of cells in the latter _ Fm. 70. Multipolar ingreswhereas here the endodermal cells, now a ?‘§:d‘?a$:”°;::f:‘§’Zg;;:fl“Z:‘§
whereas here the endodermal cells, now a ?‘§:d‘?a$:”°;::f:‘§’Zg;;:fl“Z:‘§
solid mass, have already arisen by an inward Heider. after Metchnikofi.)
solid mass, have already arisen by an inward Heider. after Metchnikofi.)
movement of some of the outer cells. The
movement of some of the outer cells. The
gut cavity appears later inside the endoderm. Cases of this sort of
gut cavity appears later inside the endoderm. Cases of this sort of
Line 3,828: Line 3,545:
or endodermal layer from the vegetative pole, or from the vegetative
or endodermal layer from the vegetative pole, or from the vegetative
half of the embryo. There is, however, another type of endodermal
half of the embryo. There is, however, another type of endodermal
formation, common in coelenterates, in which there is no polar localiza-
formation, common in coelenterates, in which there is no polar localiza106 ENDODERM FORMATION
106 ENDODERM FORMATION


tion of endoderm-forming cells, for in these the endoderm comes from
tion of endoderm-forming cells, for in these the endoderm comes from
Line 3,835: Line 3,551:
following ways: by migration into the coeloblastula from visible spots
following ways: by migration into the coeloblastula from visible spots
in the embryo, by cutting off from the cell wall of the coeloblastula by
in the embryo, by cutting off from the cell wall of the coeloblastula by
division, or, when the end stage of cleavage is a solid embryo, by his-
division, or, when the end stage of cleavage is a solid embryo, by histological differentiation of an epithelial outer layer from the parenchymous inner mass. There are many types which belong here. It will
tological differentiation of an epithelial outer layer from the paren-
chymous inner mass. There are many types which belong here. It will
be observed that multipolar ingrowth might from some points of view be
be observed that multipolar ingrowth might from some points of view be
included under this heading. The term delamination has been used to
included under this heading. The term delamination has been used to
bring together processes of different kinds and is no longer a definite
bring together processes of different kinds and is no longer a definite
term of definite meaning. Many of the forms intergrade with each other
term of definite meaning. Many of the forms intergrade with each other
through transitional stages. It is best to consider, under the head of
through transitional stages. It is best to consider, under the head of
delamination, all cases of endoderm formation which are not derived
delamination, all cases of endoderm formation which are not derived
Line 3,849: Line 3,563:
Delamination occurs in those forms whose embryos are set free late
Delamination occurs in those forms whose embryos are set free late
in development either from spore sacs or from eggs with membranous
in development either from spore sacs or from eggs with membranous
and gelatinous coverings. Many forms classified here belong to the
and gelatinous coverings. Many forms classified here belong to the
intergrading or mixed type of endoderm formation.
intergrading or mixed type of endoderm formation.


Line 3,855: Line 3,569:


When, in a coeloblastula, paratangential division planes which are
When, in a coeloblastula, paratangential division planes which are
differential in character cut off single cells into the interior of the blasto-
differential in character cut off single cells into the interior of the blastoeoele and these subsequently become arranged into a layer, coeloblastic
eoele and these subsequently become arranged into a layer, coeloblastic
delamination may be said to occur. These inner cells constitute the
delamination may be said to occur. These inner cells constitute the
endoderm and at length fill the blastocoele. By dehiscence within them
endoderm and at length fill the blastocoele. By dehiscence within them
the gut subsequently arises. In many cases of this mixed delamination,
the gut subsequently arises. In many cases of this mixed delamination,
there is a combination of the origin of endoderm by cell division and by
there is a combination of the origin of endoderm by cell division and by
Line 3,869: Line 3,582:
In morula delamination, also called secondary delamination, cleavage
In morula delamination, also called secondary delamination, cleavage
results in the formation of an embryo without a blastocoele, that is, in
results in the formation of an embryo without a blastocoele, that is, in
one solid from the first. Early in cleavage there occur both radial and
one solid from the first. Early in cleavage there occur both radial and
paratangential division planes with no histological differentiation
paratangential division planes with no histological differentiation
resulting between the inner and outer cells. An embryo arising in this
resulting between the inner and outer cells. An embryo arising in this
manner is a true morula in which a cleavage cavity never develops.
manner is a true morula in which a cleavage cavity never develops.
Haeckel thought that the morula, the stage of solid aggregates of blasto-
Haeckel thought that the morula, the stage of solid aggregates of blastomeres, always preceded the blastocoele. But it is now well known that a
meres, always preceded the blastocoele. But it is now well known that a
MORULA DELAMINATION 107
MORULA DELAMINATION 107


blastocoele cavity appears in some forms as early as the 4-cell stage,
blastocoele cavity appears in some forms as early as the 4-cell stage,
and that true morulae, as the above, are formed only in certain cases.
and that true morulae, as the above, are formed only in certain cases.
In multipolar ingrowth and in coeloblastic delamination, the pseudo-
In multipolar ingrowth and in coeloblastic delamination, the pseudo
 
fiG 71. Hydra embryo (Redrawn from Korschelt and Heider. after Brauer)
FIG 71. Hydra embryo (Redrawn from Korschelt and Heider. after Brauer)


A, showing early migration of some endoderm cells inward and the origin of others
A, showing early migration of some endoderm cells inward and the origin of others
by cell division. B, a later stage in which the endoderm fills up the cauty
by cell division. B, a later stage in which the endoderm fills up the cauty


morula follows the blastocoele stage instead of preceding it, differing
morula follows the blastocoele stage instead of preceding it, differing
Line 3,890: Line 3,601:


In morula delamination, differentiation of layers follows the solid
In morula delamination, differentiation of layers follows the solid
stage of undifferentiated cells. In Clava (Fig. 62) the cells at the surface
stage of undifferentiated cells. In Clava (fig. 62) the cells at the surface
108 EN DODERM FORMATION
108 EN DODERM FORMATION


Line 3,899: Line 3,610:
become epithelial. The cells adjoining them lose their yolk content and
become epithelial. The cells adjoining them lose their yolk content and
take positions among the outer endodermal cells. The innermost cells
take positions among the outer endodermal cells. The innermost cells
of the yolk mass finally liquefy and are resorbed, thus giving rise to the
of the yolk mass finally liquefy and are resorbed, thus giving rise to the
gastrula cavity. The formation of a definite endoderm is accomplished,
gastrula cavity. The formation of a definite endoderm is accomplished,
and the planulae, now ciliated, swarm out.
and the planulae, now ciliated, swarm out.


Morula delamination occurs also in
Morula delamination occurs also in


Trachymedusae, Siphonophora, in alcyo-
Trachymedusae, Siphonophora, in alcyonians, Stauromedusae, and Cubomedusae.
nians, Stauromedusae, and Cubomedusae.


3. Syncytial Delamination
3. Syncytial Delamination
Line 3,912: Line 3,622:
Syncytial delamination occurs in those
Syncytial delamination occurs in those
coelenterates whose embryos show a
coelenterates whose embryos show a
similarity to the superficial cleavage of
similarity to the superficial cleavage of
arthropods. In these embryos, only a few
arthropods. In these embryos, only a few
cell boundaries may be seen, and there is
cell boundaries may be seen, and there is
Line 3,918: Line 3,628:
morula stage. The ectoderm becomes
morula stage. The ectoderm becomes


FIG. 72. Endoderm formation separated from the inner mass, which in
fiG. 72. Endoderm formation separated from the inner mass, which in


3;affggaogmgfgjgggigglzfiggg; part forms the endoderm and in part
3;affggaogmgfgjgggigglzfiggg; part forms the endoderm and in part


layers by difierentiation. (Redrawn gradually is used up.
layers by difierentiation. (Redrawn gradually is used up.
‘mm K°“°h°” '”‘d Held” me’ In Turritopsis there is at first total
‘mm K°“°h°” '”‘d Held” me’ In Turritopsis there is at first total
Hum) cleavage, but in later stages the blastomeres
Hum) cleavage, but in later stages the blastomeres
flow together and form a syncytium. In this case the syncytial nuclei
flow together and form a syncytium. In this case the syncytial nuclei
at the surface multiply, cell boundaries cut in and a delicate basement
at the surface multiply, cell boundaries cut in and a delicate basement
membrane is formed. Differentiation of the endoderm comes later,
membrane is formed. Differentiation of the endoderm comes later,
when its cell boundaries begin to appear. The primitive endoderm
when its cell boundaries begin to appear. The primitive endoderm
cells are irregularly disposed, but later, when a split forms inside, repre-
cells are irregularly disposed, but later, when a split forms inside, representing the gut cavity, they are definitely formed into an epithelial layer.
senting the gut cavity, they are definitely formed into an epithelial layer.
In the hydrocorals, according to Hickson, there is no separation into
In the hydrocorals, according to Hickson, there is no separation into
blastomeres and the embryo is a syncytium from the first, recalling the
blastomeres and the embryo is a syncytium from the first, recalling the
cleavage of insects. Nuclear fragmentation of the first cleavage nucleus
cleavage of insects. Nuclear fragmentation of the first cleavage nucleus
has been described in these forms as the source of the nuclei of the
has been described in these forms as the source of the nuclei of the
plasma islands, which arise, according to this account, from regenerating
plasma islands, which arise, according to this account, from regenerating
chromatin particles. About the plasma islands cell boundaries appear,
chromatin particles. About the plasma islands cell boundaries appear,
and later the ectoderm becomes differentiated as a layer and develop-
and later the ectoderm becomes differentiated as a layer and development proceeds.
ment proceeds.


There is considerable doubt as to whether all the cases classified as
There is considerable doubt as to whether all the cases classified as
SYNCYTIAL DELAMINATION 109
SYNCYTIAL DELAMINATION 109


Line 3,946: Line 3,654:
the same material and describe many doubtful processes. Some of their
the same material and describe many doubtful processes. Some of their


FIG 73. Development of Turruopsts. (Redrawn from Korschelt and Helder, after
fiG 73. Development of Turruopsts. (Redrawn from Korschelt and Helder, after
Brooks and Rlttonhouse )
Brooks and Rlttonhouse )


A. morula. B, fusion 01 blastomeres, C, young planula Wltl) definitely formed ectoderm.
A. morula. B, fusion 01 blastomeres, C, young planula Wltl) definitely formed ectoderm.


material may be improperly fixed, and a reinvestigation may furnish
material may be improperly fixed, and a reinvestigation may furnish
more complete knowledge of their development.
more complete knowledge of their development.
Many hydroids probably belong in this group which develops by
Many hydroids probably belong in this group which develops by
Line 3,965: Line 3,673:
discoblastula, a mass of yolk occupies the greater part of the egg and
discoblastula, a mass of yolk occupies the greater part of the egg and


Fm 74. Gastrulation in Petromyzan fluvumlis (Redrawn from Ziegler, after Goette)
Fm 74. Gastrulation in Petromyzan fluvumlis (Redrawn from Ziegler, after Goette)
A, B. beginnings of gastrulation, C, formation of an anlage of the medullary tube.
A, B. beginnings of gastrulation, C, formation of an anlage of the medullary tube.


Line 3,979: Line 3,687:
edge of the embryo is the blastopore.
edge of the embryo is the blastopore.


In order to understand this process of gastrulation thus briefly
In order to understand this process of gastrulation thus briefly
described it will be necessary to take up at greater length the gastru-
described it will be necessary to take up at greater length the gastru
 
|IIIIIIIlIn.,,’
|IIIIIIIlIn.,,’
__....§
__....§
4"""lIIn\:
4"""lIIn\:


FIG. 75. Series of diagrams showing gastrulation. (After Ziegler.)
fiG. 75. Series of diagrams showing gastrulation. (After Ziegler.)


A, B. sections through embryos of an amphibian or a dipnoan in the stage of the cir-
A, B. sections through embryos of an amphibian or a dipnoan in the stage of the circular blastopore; C, gastrula of a hypothetical intermediate between Amphibia and
cular blastopore; C, gastrula of a hypothetical intermediate between Amphibia and
Amniota; D, gastrula of a reptile. y., yolk plug; ec., eetoderm; bl., blastocoele; g.,
Amniota; D, gastrula of a reptile. y., yolk plug; ec., eetoderm; bl., blastocoele; g.,
gastrocoele; m., medullary plate; d.. dorsal lip of the blastopore; s., subgerminal cavity.
gastrocoele; m., medullary plate; d.. dorsal lip of the blastopore; s., subgerminal cavity.


lation of the frog (Figs. 22, 51, and 74-76); although its egg has total,
lation of the frog (figs. 22, 51, and 74-76); although its egg has total,
unequal cleavage and gastrulation is therefore chiefly embolie, the study
unequal cleavage and gastrulation is therefore chiefly embolie, the study
of its egg enables us to interpret much better the conditions in a true
of its egg enables us to interpret much better the conditions in a true
discogastrula. In the lower or vegetative part of the frog’s egg, the white
discogastrula. In the lower or vegetative part of the frog’s egg, the white
Line 4,010: Line 3,716:
ascidians cannot always be made out.
ascidians cannot always be made out.


FIG. 76. Development of embryo of Rana showing closure of blastopore, formation of
fiG. 76. Development of embryo of Rana showing closure of blastopore, formation of
neural folds, and development of body form.
neural folds, and development of body form.


Line 4,029: Line 3,735:
The crescent groove follows the border of the pigment zone as the
The crescent groove follows the border of the pigment zone as the
latter gradually extends over the yolk and represents the dorsal side of
latter gradually extends over the yolk and represents the dorsal side of
the egg. The ventral hp of the blastopore appears later, when invagina-
the egg. The ventral hp of the blastopore appears later, when invagination takes place there, and the blastopore then becomes circular. The
tion takes place there, and the blastopore then becomes circular. The
dorsal lip advances over the yolk more rapidly than does the ventral,
dorsal lip advances over the yolk more rapidly than does the ventral,
probably on account of the greater amount of yolk in the latter region.
probably on account of the greater amount of yolk in the latter region.
Line 4,040: Line 3,745:


. B
. B
Bio 77. Embryos of Rana A at time of first indication of gill slit, B, Just before ap-
Bio 77. Embryos of Rana A at time of first indication of gill slit, B, Just before appearance of external gills at time of hatching
pearance of external gills at time of hatching


ring-shaped blastopore grows together, owing to the greater downgrowth
ring-shaped blastopore grows together, owing to the greater downgrowth
of the dorsal lip, it draws down on the yolk plug and finally becomes a
of the dorsal lip, it draws down on the yolk plug and finally becomes a
small median, slit-like furrow. This process of the growing together of
small median, slit-like furrow. This process of the growing together of
the edges of the blastopore is concrescence We may then regard con-
the edges of the blastopore is concrescence We may then regard concrescence as a third factor in the gastrulation of the frog.
crescence as a third factor in the gastrulation of the frog.


At first the dorsal, and later the ventral, blastopore lips become
At first the dorsal, and later the ventral, blastopore lips become
differentiated with distinct ectodermal and endodermal layers. The cells
differentiated with distinct ectodermal and endodermal layers. The cells
of the yolk mass, which have extended as a plug in the blastopore,
of the yolk mass, which have extended as a plug in the blastopore,
Line 4,064: Line 3,767:
frog. In the former, a protoplasmic disc rests on the top of the yolk
frog. In the former, a protoplasmic disc rests on the top of the yolk
mass, and there is thus a sharp division between protoplasm and yolk,
mass, and there is thus a sharp division between protoplasm and yolk,
instead of a gradual transition as in the frog. The disc—shaped proto-
instead of a gradual transition as in the frog. The disc—shaped protoplasmic mass of the selachian becomes furrowcd by cleavage planes, but
plasmic mass of the selachian becomes furrowcd by cleavage planes, but
the yolk mass remains unsegmented. That part of the endodermal mass
the yolk mass remains unsegmented. That part of the endodermal mass
of the frog which we have called the yolk plug must be represented in the
of the frog which we have called the yolk plug must be represented in the
Line 4,076: Line 3,778:
   
   


FIG. 78. Median section through the gastrula of Torpedo (After Ziegler)
fiG. 78. Median section through the gastrula of Torpedo (After Ziegler)


cells and are called the periblast cells. These periblast nuclei are com-
cells and are called the periblast cells. These periblast nuclei are comparable to the eephalopod blastocones; that is, they are blastomeres not
parable to the eephalopod blastocones; that is, they are blastomeres not
cut off from the yolk mass by cleavage.
cut off from the yolk mass by cleavage.


Line 4,092: Line 3,793:


The first change in the germ disc of the selachian is the formation of
The first change in the germ disc of the selachian is the formation of
an epithelial layer from the superficial cells which become flattened and
an epithelial layer from the superficial cells which become flattened and
broadened. This layer begins to form at the hinder part of the embryo
broadened. This layer begins to form at the hinder part of the embryo
where the cleavage cavity is larger and the germ disc thinner and
where the cleavage cavity is larger and the germ disc thinner and
Line 4,106: Line 3,807:
spreading as an iris-like ingrowth from the edge of the germ disc and of
spreading as an iris-like ingrowth from the edge of the germ disc and of
the growing epithelial endoderm. The invaginated gastrula cavity is at
the growing epithelial endoderm. The invaginated gastrula cavity is at
first crescent shaped, comparable to that of amphibians, but with an
first crescent shaped, comparable to that of amphibians, but with an
axial cavity in addition to the peripheral cavities of the crescent. The
axial cavity in addition to the peripheral cavities of the crescent. The
edge of the entire germ disc may be thought of as a blastopore.
edge of the entire germ disc may be thought of as a blastopore.


FIG 7‘) G1-«itriilitiam of the salmon. Salmo salar; ll. growth of the bl i-itoderm of
fiG 7‘) G1-«itriilitiam of the salmon. Salmo salar; ll. growth of the bl i-itoderm of
the salmon, (‘, emlirvonal shield stage, the germ ring covering one-li ilf of the yolk (After
the salmon, (‘, emlirvonal shield stage, the germ ring covering one-li ilf of the yolk (After
Ziegler )
Ziegler )


The anterior edge of the blastopore becomes extremely active and
The anterior edge of the blastopore becomes extremely active and
begins to grow down over the yolk. Finally it grows entiiely over the
begins to grow down over the yolk. finally it grows entiiely over the
yolk, passing over the vegetative pole, and reappearing behind the
yolk, passing over the vegetative pole, and reappearing behind the
embryo as the ventral lip of the blastopore. The yolk thus becomes
embryo as the ventral lip of the blastopore. The yolk thus becomes
Line 4,124: Line 3,825:
at the posterior edge of the germ disc where invagination bi iiigs about
at the posterior edge of the germ disc where invagination bi iiigs about
the origin of the primitive gut. There is a slight invagination at the
the origin of the primitive gut. There is a slight invagination at the
lateral and anterior edges also, and the yolk is finally enclosed by the
lateral and anterior edges also, and the yolk is finally enclosed by the
blastoderm, the anterior margin becoming the ventral lip of the blaste-
blastoderm, the anterior margin becoming the ventral lip of the blaste1 16 ENDODERM FORMATION
1 16 ENDODERM FORMATION


pore. In the elasmobranchs, teleosts, and also in the myxinoids, there
pore. In the elasmobranchs, teleosts, and also in the myxinoids, there
Line 4,134: Line 3,834:
second, the lateral and anterior margins of the blastoderm gradually
second, the lateral and anterior margins of the blastoderm gradually
cover the yolk. Thus only the dorsal lip takes part in the formation of
cover the yolk. Thus only the dorsal lip takes part in the formation of
the future embryo, while the lateral and ventral lips are entirely extra-
the future embryo, while the lateral and ventral lips are entirely extraembryonic.
embryonic.


c. Reptiles and Birds. In all the vertebrates thus far described, the
c. Reptiles and Birds. In all the vertebrates thus far described, the
Anamnia, the blastoporic lip appears at the edge of the blastoderm. In
Anamnia, the blastoporic lip appears at the edge of the blastoderm. In
the reptiles and birds, which have embryonic membranes and hence
the reptiles and birds, which have embryonic membranes and hence
belong to the Amniota, the blastoporic lip lies wholly within the blasto-
belong to the Amniota, the blastoporic lip lies wholly within the blastoderm. The archenteric cavity is well developed only in primitive forms
derm. The archenteric cavity is well developed only in primitive forms
and is usually represented only by the neurenteric canal. In most cases
and is usually represented only by the neurenteric canal. In most cases


   
   


FIG. 80. Gastrula of pigeon. (After Patterson.)
fiG. 80. Gastrula of pigeon. (After Patterson.)


Thirty-six hours after fertilization. Section through the posterior portion of the blastodisc
Thirty-six hours after fertilization. Section through the posterior portion of the blastodisc
Line 4,155: Line 3,853:


In the chick the blastoderm or germ disc lies on top of the yolk mass,
In the chick the blastoderm or germ disc lies on top of the yolk mass,
as in the fish. The endoderm is formed by an inturning of the germ disc
as in the fish. The endoderm is formed by an inturning of the germ disc
at the posterior margin and by ingrowth from the inturned portion. At
at the posterior margin and by ingrowth from the inturned portion. At
the posterior part of the germ disc the primitive streak is formed by a
the posterior part of the germ disc the primitive streak is formed by a
linear thickening of the upper layer of the blastoderm. The endodermal
linear thickening of the upper layer of the blastoderm. The endodermal
layer in the chick gradually grows around the yolk and the yolk sac is
layer in the chick gradually grows around the yolk and the yolk sac is
thus formed. The ectoderm does not directly cover the yolk sac, how-
thus formed. The ectoderm does not directly cover the yolk sac, however, as here conditions are complicated by the presence of embryonic
ever, as here conditions are complicated by the presence of embryonic
membranes, the amnion, which encloses the embryo, the allantois, and
membranes, the amnion, which encloses the embryo, the allantois, and
the chorion.
the chorion.
Line 4,167: Line 3,864:
In the chick the primitive streak represents the fused lips of the
In the chick the primitive streak represents the fused lips of the
margin of invagination and therefore is to be considered as the closing
margin of invagination and therefore is to be considered as the closing
blastopore. In the primitive streak the germ layers are fused, the differ-
blastopore. In the primitive streak the germ layers are fused, the differentiated part of the embryo being formed in front of it, the anus at the
entiated part of the embryo being formed in front of it, the anus at the
posterior end, and the neurenteric canal at the anterior end. We must
posterior end, and the neurenteric canal at the anterior end. We must
o
o
Line 4,177: Line 3,873:


i J
i J
FIG 81 Dlagram to Illustrate dxfierence between the blastopores of Annmnm and Ammcte.
fiG 81 Dlagram to Illustrate dxfierence between the blastopores of Annmnm and Ammcte.
(After Jenklnson )
(After Jenklnson )


a—c Closure of blastopore 1n frog or sxmxlar form Stlppled reglon 1s the blastoderm.
a—c Closure of blastopore 1n frog or sxmxlar form Stlppled reglon 1s the blastoderm.
The edge of the blnstoderm represents the edges of the blastopore d-—f Ventral hp of blusto-
The edge of the blnstoderm represents the edges of the blastopore d-—f Ventral hp of blustopore xs absent m such a. form as Lemdoszren The heavy solld lxne represents the portlon
pore xs absent m such a. form as Lemdoszren The heavy solld lxne represents the portlon
whmh forms the lips of the blastopore g, h Only a. small part at the postenor end becomes
whmh forms the lips of the blastopore g, h Only a. small part at the postenor end becomes
the blastopore as In the Gymnophlona. The yolk remams uncovered 1. J The condxtlon
the blastopore as In the Gymnophlona. The yolk remams uncovered 1. J The condxtlon
Line 4,196: Line 3,891:
In the reptiles there IS a so-called embryonic shield at the posterior
In the reptiles there IS a so-called embryonic shield at the posterior
end of the blastoderm. This IS a circular or oval area of columnar cells
end of the blastoderm. This IS a circular or oval area of columnar cells
resting upon a lower layer and surrounded by a region of flattened cells.
resting upon a lower layer and surrounded by a region of flattened cells.


   
   
Line 4,206: Line 3,901:
B C
B C


FIG 82 Bali'our’s diagrams showing homology between bliistopore and the primitive
fiG 82 Bali'our’s diagrams showing homology between bliistopore and the primitive
streak (After Ziegler )
streak (After Ziegler )


Line 4,225: Line 3,920:
The comparison of the Anamnia and Amniota can best be understood
The comparison of the Anamnia and Amniota can best be understood
by observing the development of the gymnophionan egg. Here the
by observing the development of the gymnophionan egg. Here the
blastoderm is an oval layer of columnar cells resting upon a partly seg-
blastoderm is an oval layer of columnar cells resting upon a partly segmented yolk. Only a part of the edge of the blastoderm at its posterior
mented yolk. Only a part of the edge of the blastoderm at its posterior
end is converted into a blastoporic lip which is at first dorsal. Later the
end is converted into a blastoporic lip which is at first dorsal. Later the
lateral lips turn back around a small part of the yolk, and then join to
lateral lips turn back around a small part of the yolk, and then join to
Line 4,232: Line 3,926:
part in the formation of the blastopore. In this form the yolk remains
part in the formation of the blastopore. In this form the yolk remains
uncovered. We have seen that, in other Anamnia, the ventral lip develops
uncovered. We have seen that, in other Anamnia, the ventral lip develops
from the anterior edge of the blastoderm and the yolk is necessarily cov-
from the anterior edge of the blastoderm and the yolk is necessarily covered where_the blastopore closes.
ered where_the blastopore closes.


The embryonic shield of the Amniota must be represented, in the
The embryonic shield of the Amniota must be represented, in the
Line 4,239: Line 3,932:
together with the lower layer with which it is connected at the primitive
together with the lower layer with which it is connected at the primitive
plate, must be represented by the yolk cells or nucleated yolk. It seems
plate, must be represented by the yolk cells or nucleated yolk. It seems
natural to suppose that in the transition from forms like the Gymno-
natural to suppose that in the transition from forms like the Gymnophiona to the higher vertebrates, as the yolk material in the egg increased
phiona to the higher vertebrates, as the yolk material in the egg increased
in amount, segmentation has become restricted, not to the blastoderm
in amount, segmentation has become restricted, not to the blastoderm
alone as in the fishes, but to the blastoderm and those adjacent and
alone as in the fishes, but to the blastoderm and those adjacent and
subjacent cells which in the Gymnophiona are partly segmented from
subjacent cells which in the Gymnophiona are partly segmented from
the yolk.
the yolk.
Line 4,258: Line 3,950:
to this type, regardless of whether it is an invertebrate or a vertebrate egg.
to this type, regardless of whether it is an invertebrate or a vertebrate egg.


The scorpion egg (Fig. 39) is rich in yolk and the cleavage of the egg is
The scorpion egg (fig. 39) is rich in yolk and the cleavage of the egg is
discoidal. In young stages there is found a small, one-layered cap on the
discoidal. In young stages there is found a small, one-layered cap on the
yolk. The blastoderm spreads gradually from this point and advances
yolk. The blastoderm spreads gradually from this point and advances
over the yolk. Scorpion eggs, since they have cleavage of this type, are
over the yolk. Scorpion eggs, since they have cleavage of this type, are
comparable to eggs in which there is superficial cleavage with early
comparable to eggs in which there is superficial cleavage with early
formation of the blastodisc on one portion of the egg only. The scorpion
formation of the blastodisc on one portion of the egg only. The scorpion
condition is probably an extreme case and is to be traced back to the
condition is probably an extreme case and is to be traced back to the
Line 4,268: Line 3,960:


type which is widespread among the arachnids. The scorpion egg,
type which is widespread among the arachnids. The scorpion egg,
therefore, represents a modification of the type common to its group
therefore, represents a modification of the type common to its group
(as is also indicated by its viviparous mode of development).
(as is also indicated by its viviparous mode of development).


Line 4,274: Line 3,966:
disc which lie next to the yolk and form a regular epithelium. The
disc which lie next to the yolk and form a regular epithelium. The
irregular cells which remain between the outer layer or ectoderm and the
irregular cells which remain between the outer layer or ectoderm and the
inner or endodermal layer become arranged into two symmetrical meso-
inner or endodermal layer become arranged into two symmetrical mesodermal bands.
dermal bands.


It will be seen at once that in the scorpions, as in the myxinoids, the
It will be seen at once that in the scorpions, as in the myxinoids, the
Line 4,297: Line 3,988:
the first cleavage cells and later the outer cells of the disc, the blastocones,
the first cleavage cells and later the outer cells of the disc, the blastocones,
are not cut off from the peripheral protoplasm. The germ disc spreads
are not cut off from the peripheral protoplasm. The germ disc spreads
out and increases in size, at first chiefly at the expense of the formative
out and increases in size, at first chiefly at the expense of the formative
yolk with which the blastocones are connected. The germ disc, one cell
yolk with which the blastocones are connected. The germ disc, one cell
in thickness and covering only a small part of the egg, becomes thick-
in thickness and covering only a small part of the egg, becomes thickened at the periphery as it spreads. When the cleavage cells have
ened at the periphery as it spreads. When the cleavage cells have
increased to a considerable number the peripheral blastocones become
increased to a considerable number the peripheral blastocones become
detached from the germ disc. These cells, according to Vialleton, wander
detached from the germ disc. These cells, according to Vialleton, wander
Line 4,312: Line 4,002:


While the yolk epithelium is forming and the edge of the germ disc
While the yolk epithelium is forming and the edge of the germ disc
is becoming thickened, the outer cells of the disc increase rapidly (Fig.
is becoming thickened, the outer cells of the disc increase rapidly (fig.
44). This outer layer extends gradually over the whole egg (and thus
44). This outer layer extends gradually over the whole egg (and thus
CEPHALOPODS 121
CEPHALOPODS 121
Line 4,319: Line 4,009:
two layers, the ectoderm and the yolk epithelium, are soon followed by
two layers, the ectoderm and the yolk epithelium, are soon followed by
a third or middle layer, which also covers the yolk. There are thus two
a third or middle layer, which also covers the yolk. There are thus two
definite regions in the egg at this time, the germ disc which forms the
definite regions in the egg at this time, the germ disc which forms the
embryonic rudiment, and the yolk sac composed of three layers.
embryonic rudiment, and the yolk sac composed of three layers.


Line 4,348: Line 4,038:
seen, next to the yolk, an epithelial plate of only a few cells. It is the
seen, next to the yolk, an epithelial plate of only a few cells. It is the
first indication of the enteron. It soon increases in size and becomes
first indication of the enteron. It soon increases in size and becomes
sac like, finally separating from the yolk. The yolk epithelium, pre-
sac like, finally separating from the yolk. The yolk epithelium, previously lacking at this point, now grows under the enteron. The origin
viously lacking at this point, now grows under the enteron. The origin
of the endodermal plate thus described is probably from the thickened
of the endodermal plate thus described is probably from the thickened
peripheral mass at the edge of the germ disc which evidently represents
peripheral mass at the edge of the germ disc which evidently represents
meso-endoderm. The whole process is thus to be regarded as a much
meso-endoderm. The whole process is thus to be regarded as a much
modified invagination, and the edge of the germ disc is the blastopore
modified invagination, and the edge of the germ disc is the blastopore
filled by the large yolk plug, which also fills the whole enteric cavity.
filled by the large yolk plug, which also fills the whole enteric cavity.


BIBLIOGRAPHIC NOTE
BIBLIOGRAPHIC NOTE
Line 4,365: Line 4,054:


Mesoderm is the layer between the outer epidermis and the midgut
Mesoderm is the layer between the outer epidermis and the midgut
epithelium. It produces the muscles, coelome, and the structures belong-
epithelium. It produces the muscles, coelome, and the structures belonging to the coelome, all the body and intestinal musculature, the gonads,
ing to the coelome, all the body and intestinal musculature, the gonads,
the kidneys (except the Malpighian vessels) and the anlagen of connective tissue and blood vessels.
the kidneys (except the Malpighian vessels) and the anlagen of con-
nective tissue and blood vessels.


The concept mesoderm lacks a genetic unity throughout the animal
The concept mesoderm lacks a genetic unity throughout the animal
Line 4,375: Line 4,062:
of genetic unity of mesoderm, the anlagen of mesodermal structures
of genetic unity of mesoderm, the anlagen of mesodermal structures
have a common origin in single great groups of the rnetazoa. There is a
have a common origin in single great groups of the rnetazoa. There is a
definite homology in the mesoderm of all forms with a spiral type of
definite homology in the mesoderm of all forms with a spiral type of
cleavage, as turbellarians, nemertines, molluscs, annelids, and also the
cleavage, as turbellarians, nemertines, molluscs, annelids, and also the
arthropods. The mesoderm of all these forms is endodermal, arising
arthropods. The mesoderm of all these forms is endodermal, arising
from the endoderm, and therefore the anlagen of the mesoderm bands
from the endoderm, and therefore the anlagen of the mesoderm bands
are in genetic unity. It is also true that the ectomesoderm or mesoderm
are in genetic unity. It is also true that the ectomesoderm or mesoderm
arising from the ectoderm of many forms is homologous. It is further-
arising from the ectoderm of many forms is homologous. It is furthermore probable that the enterocoeles of echinoderms, Enteropneusta,
more probable that the enterocoeles of echinoderms, Enteropneusta,
and chordates are of common origin.
and chordates are of common origin.


Line 4,391: Line 4,077:
first the eetomesoderm.
first the eetomesoderm.


Ectomesoderm arises from the primary ectoderm and usually pro-
Ectomesoderm arises from the primary ectoderm and usually produces mesenchymatous muscle cells and connective tissue. This kind of
duces mesenchymatous muscle cells and connective tissue. This kind of
mesoderm occurs in the flatworms, rotifers, nematodes, annelids, and
mesoderm occurs in the flatworms, rotifers, nematodes, annelids, and
molluses. Although the coelenterates are usually considered as two
molluses. Although the coelenterates are usually considered as two
layered, there is often present a third layer, mesogloea, which, though
layered, there is often present a third layer, mesogloea, which, though
Line 4,399: Line 4,084:
dermal layer contains both ectoderm and mesoderm (using the term in
dermal layer contains both ectoderm and mesoderm (using the term in
a doubtful sense) and consists of (a) outer epithelium, (b) canal system
a doubtful sense) and consists of (a) outer epithelium, (b) canal system
except the flagellated chambers which are not included here, (c) connec—
except the flagellated chambers which are not included here, (c) connec—
tive tissue, and (d) sex cells.
tive tissue, and (d) sex cells.


Line 4,406: Line 4,091:


In coelenterates a distinction can hardly be made between ectoderm
In coelenterates a distinction can hardly be made between ectoderm
and mesoderm. Although hydroids have only two layers, still the inter-
and mesoderm. Although hydroids have only two layers, still the interstitial cells which are at the bases of the epithelial cells and which later
stitial cells which are at the bases of the epithelial cells and which later
form the gonads may be considered as forerunners of the mesoderm.
form the gonads may be considered as forerunners of the mesoderm.


In the Actinozoa, the distinction between ectoderm and endoderm is
In the Actinozoa, the distinction between ectoderm and endoderm is
more sharply defined than in hydroids. In the Alcyonaria, there is often
more sharply defined than in hydroids. In the Alcyonaria, there is often
connective tissue with skeletal structure, and this layer is ectodermal.
connective tissue with skeletal structure, and this layer is ectodermal.
The ectoderm becomes many layered, and a jelly substance is secreted
The ectoderm becomes many layered, and a jelly substance is secreted
between the cells of the deeper layers which become separated from
between the cells of the deeper layers which become separated from
each other. Thus two layers are formed, an outer epithelium and an
each other. Thus two layers are formed, an outer epithelium and an
inner gelatinous layer which may be thought of as representing ecto-
inner gelatinous layer which may be thought of as representing ectomesoderm.
mesoderm.


In the ctenophores the mesoderm becomes more highly differentiated
In the ctenophores the mesoderm becomes more highly differentiated
Line 4,423: Line 4,106:
is now known to be ectomesodermal in origin. Kowalevsky and Chun
is now known to be ectomesodermal in origin. Kowalevsky and Chun
found that the mesoderm originates from ectoderm in the region of the
found that the mesoderm originates from ectoderm in the region of the
gut. (See Fig. 14B.) This is of particular interest because in forms with
gut. (See fig. 14B.) This is of particular interest because in forms with
the spiral type of cleavage the larval mesoblast originates in relation
the spiral type of cleavage the larval mesoblast originates in relation
to the blastomeres which produce the stomodacal invagination. In the
to the blastomeres which produce the stomodacal invagination. In the
polyclads, according to Surface, the ectomesoderm produces chiefly
polyclads, according to Surface, the ectomesoderm produces chiefly
musculature of the pharynx.
musculature of the pharynx.


Since the work on cell lineage, the development of annelids and
Since the work on cell lineage, the development of annelids and
molluscs is more definitely understoo(l, and we now know that the part
molluscs is more definitely understoo(l, and we now know that the part
of the mesoderm which is to become the mesenchyme of the trochophore
of the mesoderm which is to become the mesenchyme of the trochophore
arises from the ectoderm. In all forms with spiral type of cleavage, the
arises from the ectoderm. In all forms with spiral type of cleavage, the
first three quartettes form the ectoderm. Wilson has shown for poly-
first three quartettes form the ectoderm. Wilson has shown for polyelads that the mesoderm cells are formed by division of the cells of the
elads that the mesoderm cells are formed by division of the cells of the
second quartette, and that the third quartette probably also shares in
second quartette, and that the third quartette probably also shares in
the formation of mesoblast. The mesoderm formed in this way is the
the formation of mesoblast. The mesoderm formed in this way is the
Line 4,440: Line 4,122:
and annelids and therefore being endodermal in origin.
and annelids and therefore being endodermal in origin.


The relations in other flatworms, nernerteans and nematodes, is not
The relations in other flatworms, nernerteans and nematodes, is not
clear. In rotifers the entire mesoderm appears to be larval mesoblast
clear. In rotifers the entire mesoderm appears to be larval mesoblast
and some of this has been shown to be ectodermal. There are no meso-
and some of this has been shown to be ectodermal. There are no mesoderm bands and the gonads come from primary endoderm and may
derm bands and the gonads come from primary endoderm and may
represent the mesoderm bands of related forms.
represent the mesoderm bands of related forms.


In a number of the annelids the ectomesoderm arises definitely from
In a number of the annelids the ectomesoderm arises definitely from
three cells of the third quartette, 3a, 3c, 3d. The anlage is thus asym-
three cells of the third quartette, 3a, 3c, 3d. The anlage is thus asymmetrical, being paired on the dorsal side, while on the ventral only the
metrical, being paired on the dorsal side, while on the ventral only the
left forms it. In some molluscs the ectomesoderm arises exclusively from
left forms it. In some molluscs the ectomesoderm arises exclusively from
the third quartette. In Trochus (Fig. 33, 34, Table p. 56) it arises from
the third quartette. In Trochus (fig. 33, 34, Table p. 56) it arises from
3c and 3d from the dorsal cells of the quartette. In other forms the second
3c and 3d from the dorsal cells of the quartette. In other forms the second
124 MESODERM FORMATION
124 MESODERM FORMATION
Line 4,459: Line 4,139:


Ectomesoderm produces connective tissue and larval musculature of
Ectomesoderm produces connective tissue and larval musculature of
the trochophore larva. For annelids and molluscs it seems to be a pro-
the trochophore larva. For annelids and molluscs it seems to be a provisional tissue degenerating upon metamorphosis. It is doubtful whether
visional tissue degenerating upon metamorphosis. It is doubtful whether
the ectomesoderm produces excretory organs, but the kidneys of some
the ectomesoderm produces excretory organs, but the kidneys of some
molluscs are known to be of ectodermal origin.
molluscs are known to be of ectodermal origin.
Line 4,467: Line 4,146:
also in many groups which are near the trochophore type; these may be
also in many groups which are near the trochophore type; these may be
collectively called Prostomia. Endomesoderm appears to be lacking in
collectively called Prostomia. Endomesoderm appears to be lacking in
the Molluscoidea. It seems striking that the entire group called Deutero-
the Molluscoidea. It seems striking that the entire group called Deuterostomia (composed of Enteropneusta, Echinodermata, and Chordata)
stomia (composed of Enteropneusta, Echinodermata, and Chordata)
shows scarcely any ectomesoderm. Thus we recognize two great stems
shows scarcely any ectomesoderm. Thus we recognize two great stems
of the animal kingdom, in so far as mesoderm formation is concerned.
of the animal kingdom, in so far as mesoderm formation is concerned.
Line 4,479: Line 4,157:
pouches or through the coming together of mesenchyme cells. We shall
pouches or through the coming together of mesenchyme cells. We shall
consider each of these cases separately under the following heads:
consider each of these cases separately under the following heads:
(a) Teloblastic mesoderm band formation. In these cases paired meso-
(a) Teloblastic mesoderm band formation. In these cases paired mesoderm bands take their origin from two primitive mesoderm cells as in
derm bands take their origin from two primitive mesoderm cells as in
annelids and molluscs. (b) Secondary or derived mesoderm band formation. Those cases belong here in which paired mesoderm bands are laid
annelids and molluscs. (b) Secondary or derived mesoderm band forma-
down without primitive mesoderm cells. They are often modifications
tion. Those cases belong here in which paired mesoderm bands are laid
of the first type, since they occur among forms derived from annelids and
down without primitive mesoderm cells. They are often modifications
of the first type, since they occur among forms derived from annelids and
molluscs. Examples are arthropods and cephalopods. (c) Enterocoele
molluscs. Examples are arthropods and cephalopods. (c) Enterocoele
formation. The formation of coelomic sacs by outfolding from the
formation. The formation of coelomic sacs by outfolding from the
Line 4,517: Line 4,193:
   
   


FIG. 83. Mesoderm of the snail, Physa. (Redrawn from Korschelt and Heider, after
fiG. 83. Mesoderm of the snail, Physa. (Redrawn from Korschelt and Heider, after
Wierzejski.)
Wierzejski.)
The four larger cells M“, M", M“, and M“ and three pairs of micromeres m‘, m1,
The four larger cells M“, M", M“, and M“ and three pairs of micromeres m‘, m1,
Line 4,525: Line 4,201:
cells are more nearly like endoderm than ectoderm in appearance, size,
cells are more nearly like endoderm than ectoderm in appearance, size,
and yolk content. This intimate relation of 4d to primary endoderm is
and yolk content. This intimate relation of 4d to primary endoderm is
shown by the fact that, besides the primitive mesoderm, 4d often pro-
shown by the fact that, besides the primitive mesoderm, 4d often produces other cells which contribute to the formation of the midgut.
duces other cells which contribute to the formation of the midgut.


In most forms the third quartette is given off dexiotropically and 4d
In most forms the third quartette is given off dexiotropically and 4d
Line 4,538: Line 4,213:
126 MESODERM FORMATION
126 MESODERM FORMATION


formed, the two median ones of which, M 1’ and M?’-’, become the primi-
formed, the two median ones of which, M 1’ and M?’-’, become the primitive cells of the mesoderm bands. The two other large cells in some forms
tive cells of the mesoderm bands. The two other large cells in some forms
(pulmonates) have been said to give rise to the primitive kidney of the
(pulmonates) have been said to give rise to the primitive kidney of the
trochophore, A series of divisions of primitive mesoderm cells now
trochophore, A series of divisions of primitive mesoderm cells now
follows and two rows of small cells are formed. These become surrounded
follows and two rows of small cells are formed. These become surrounded
by the ectodermal products of the first quartettes.
by the ectodermal products of the first quartettes.


In many yolk-poor eggs, as in oligochaetes, mesoderm bands are
In many yolk-poor eggs, as in oligochaetes, mesoderm bands are
formed very early before the beginning of gastrulation, and lie in the
formed very early before the beginning of gastrulation, and lie in the
blastocoele at the blastula stage. The mesoderm bands are at first
blastocoele at the blastula stage. The mesoderm bands are at first
dorsal and produce cells ventrally. With changes of body form they go
dorsal and produce cells ventrally. With changes of body form they go
through changes of position. The bands are given off horizontally and
through changes of position. The bands are given off horizontally and
Line 4,554: Line 4,228:
   
   


FIG. 84. Embryo of Crepidula. at the time of the closure of the hlastopore and the
fiG. 84. Embryo of Crepidula. at the time of the closure of the hlastopore and the
formation of the stomodaeum. In addition mesodormal cells (In) and the gut cavity are
formation of the stomodaeum. In addition mesodormal cells (In) and the gut cavity are
to be seen. (After Conklin.)
to be seen. (After Conklin.)
Line 4,583: Line 4,257:


In the arthropods, as in the annelids, we find a pair of mesoderm
In the arthropods, as in the annelids, we find a pair of mesoderm
bands. At first solid and sometimes single layered, these bands later
bands. At first solid and sometimes single layered, these bands later


FIG 85 Diagrams of the development of Trochophorn showing the shift in position
fiG 85 Diagrams of the development of Trochophorn showing the shift in position
of the mesoderm bands (After Korsehelt and Heider)
of the mesoderm bands (After Korsehelt and Heider)


Line 4,598: Line 4,272:


paired mesoderm cells, and from them mesodermal bands develop.
paired mesoderm cells, and from them mesodermal bands develop.
These bands arise through teloblastic growth, by successive cell prolifera-
These bands arise through teloblastic growth, by successive cell proliferation from the sides of the original mesoderm cells. In the arthropods, on
tion from the sides of the original mesoderm cells. In the arthropods, on
the other hand, the anlage of the mesoderm bands is many layered from
the other hand, the anlage of the mesoderm bands is many layered from
the beginning. From the moment that they may be recognized as sepa-
the beginning. From the moment that they may be recognized as separate cell groups no original mesodermal cells are observed and no teleblastic cells increase. Gastrulation in most of the arthropods is in the
rate cell groups no original mesodermal cells are observed and no tele-
blastic cells increase. Gastrulation in most of the arthropods is in the
form of a many-celled solid ingrowth. The ingrowing cells form the
form of a many-celled solid ingrowth. The ingrowing cells form the
primitive entoderm which spreads itself under the ectoderm as a so-called
primitive entoderm which spreads itself under the ectoderm as a so-called
under layer since it pushes up to the opposite side of the central yolk
under layer since it pushes up to the opposite side of the central yolk
mass. Now there is a division into an endodermal cell mass and into
mass. Now there is a division into an endodermal cell mass and into
paired mesoderm bands. These latter spread out and divide into seg-
paired mesoderm bands. These latter spread out and divide into segmented sections.
mented sections.


In some few arthropods there has been observed a special place of
In some few arthropods there has been observed a special place of
Line 4,624: Line 4,294:
Here there is at the hinder end a cross row of eight teloblasts which
Here there is at the hinder end a cross row of eight teloblasts which
through division.produce the mesoderm of the metanauplius germ band.
through division.produce the mesoderm of the metanauplius germ band.
There is here only a distant relation to the annelid type as the condi-
There is here only a distant relation to the annelid type as the conditions are entirely different.
tions are entirely different.


In the cephalopods there is no trace of the spiral type of cleavage and
In the cephalopods there is no trace of the spiral type of cleavage and
Line 4,638: Line 4,307:
A consideration of the mesoderm formation of the Enteropneusta will
A consideration of the mesoderm formation of the Enteropneusta will
lead us naturally to the other chordates. The Enteropneusta form an
lead us naturally to the other chordates. The Enteropneusta form an
ancestral group through which the echinoderms are brought into con-
ancestral group through which the echinoderms are brought into connection with the chordates. In this small group different types of coelome
nection with the chordates. In this small group different types of coelome
formation may be observed, the type of simple enterocoele formation
formation may be observed, the type of simple enterocoele formation
and the type of coelome formation by the coming together of single
and the type of coelome formation by the coming together of single
Line 4,648: Line 4,316:
together. Let us consider first the coelome of Balanoglossus. Here there
together. Let us consider first the coelome of Balanoglossus. Here there
are, corresponding to the three body regions, three coelomic cavities;
are, corresponding to the three body regions, three coelomic cavities;
the head, unpaired but showing by its two pores and incomplete mesen-
the head, unpaired but showing by its two pores and incomplete mesentery a double nature, the collar, and the body coelornes. The latter coelome consists of paired spaces separated by a median mesentery. The
tery a double nature, the collar, and the body coelornes. The latter coe-
lome consists of paired spaces separated by a median mesentery. The
head coelome is known to be formed by the cutting off of a vesicle at
head coelome is known to be formed by the cutting off of a vesicle at
the forward end of the primitive gut, the end opposite the blastopore.
the forward end of the primitive gut, the end opposite the blastopore.
Line 4,658: Line 4,324:
and body coelome. In those forms of
and body coelome. In those forms of
Balanoglossus which have no tornaria, but
Balanoglossus which have no tornaria, but
develop directly, two pairs of gut diverti-
develop directly, two pairs of gut diverticula become_ the collar and body coelomes.
cula become_ the collar and body coelomes.
In another form these two pairs of sacs
In another form these two pairs of sacs
are cut off behind from the first-formed
are cut off behind from the first-formed
coelomic vesicle, the water vesicle. Here
coelomic vesicle, the water vesicle. Here
in a form without tornaria there is a
in a form without tornaria there is a
similarity to the formation of the entere-
similarity to the formation of the enterecoele in most echinoderms which also
coele in most echinoderms which also
form an originally forward vesicle through
form an originally forward vesicle through
the fusion of three pairs of coelomic sacs,
the fusion of three pairs of coelomic sacs,
Line 4,672: Line 4,336:


In the New England tornaria the collar
In the New England tornaria the collar
coelome is formed by paired cell prolifera-
coelome is formed by paired cell proliferations at the side of the stomach, the trunk F“, 86. Diagram of the coelome
tions at the side of the stomach, the trunk F“, 86. Diagram of the coelome
coelome by solid evaginations of the intes- forrxxzmtion of Balanoalossus Kowalevtine. In the tornaria from the Bahamas, §aft'e‘;':n§°’s°h°lt and
coelome by solid evaginations of the intes- forrxxzmtion of Balanoalossus Kowalev-
tine. In the tornaria from the Bahamas, §aft'e‘;':n§°’s°h°lt and
on the other hand, these coelomic spaces
on the other hand, these coelomic spaces
are formed at a considerable distance from the gut by aggregations of
are formed at a considerable distance from the gut by aggregations of
Line 4,685: Line 4,347:
proliferation, (c) through aggregations of mesenchyme cells.
proliferation, (c) through aggregations of mesenchyme cells.


The second type is easily derived from the first, as solid cell prolifera-
The second type is easily derived from the first, as solid cell proliferation is one step beyond a diverticulum. The third type differs, but may
tion is one step beyond a diverticulum. The third type differs, but may
be considered to fall into line if we think of the cells of a solid proliferation as having lost their connection and become scattered mesenchyme
be considered to fall into line if we think of the cells of a solid prolifera-
tion as having lost their connection and become scattered mesenchyme


cells.
cells.
Line 4,705: Line 4,365:
evagination of the ceeloinic sac fiom the
evagination of the ceeloinic sac fiom the
primitive gut. At the same time iiiesenchyine
primitive gut. At the same time iiiesenchyine
cells migrate into the blastocoele. Meson-
cells migrate into the blastocoele. Mesonchyme formation may begin very early, even
chyme formation may begin very early, even
before the beginning of gastrulation, or may
before the beginning of gastrulation, or may
not begin until later. Following this process
not begin until later. Following this process
Line 4,712: Line 4,371:
at the place which will become the top of the
at the place which will become the top of the


Fm 87 Diagram of the me_ primitive gut, a cell migration into the gelati-
Fm 87 Diagram of the me_ primitive gut, a cell migration into the gelati
 
lgiimg forniation Km Cgnlnatulad nous blastocoele. By the time gastrulation is
lgiimg forniation Km Cgnlnatulad nous blastocoele. By the time gastrulation is
ra n rom orse e 1; an - -
ra n rom orse e 1; an - Hefdenvvufter Scehger ) completed, cell migration from the top of the
Hefdenvvufter Scehger ) completed, cell migration from the top of the


gut has already been going on for some time.
gut has already been going on for some time.
There are two types of coelome formation in the echinodeims. Com-
There are two types of coelome formation in the echinodeims. Com
 
atula is an example of one type. In this form the hydiocoele develops
atula is an example of one type. In this form the hydiocoele develops


Line 4,738: Line 4,394:
i
i
A B C
A B C
FIG 88 Metamorphosis of the coelome sacs in the eehinoids (A, B. redrawn from
fiG 88 Metamorphosis of the coelome sacs in the eehinoids (A, B. redrawn from
Korschelt and Heider after Theel, C, redrawn from Korsehelt and I-Ieider after Bury)
Korschelt and Heider after Theel, C, redrawn from Korsehelt and I-Ieider after Bury)


Line 4,761: Line 4,417:
forward enterocoele sac.
forward enterocoele sac.


In chaetognaths and the brachiopods also we find enterocoele forma-
In chaetognaths and the brachiopods also we find enterocoele formation. Amphioxus must also be considered since its mesoderm is formed
tion. Amphioxus must also be considered since its mesoderm is formed
as an enterocoele, paired diverticula originating on the dorsal side of the embryo and
as an enterocoele, paired diverticula originat-
ing on the dorsal side of the embryo and
later surrounding the gut. Hatschek thought
later surrounding the gut. Hatschek thought
that there were primitive mesoderm cells in
that there were primitive mesoderm cells in
Line 4,776: Line 4,430:
At the sides of the notochord are the two Fm. 89. Cross section of an
At the sides of the notochord are the two Fm. 89. Cross section of an
grooves at the anterior end of which paired inS:‘0‘:l“:)i;‘cff
grooves at the anterior end of which paired inS:‘0‘:l“:)i;‘cff
evagmations occur. These evaginations are tion with the enterou. (Re-
evagmations occur. These evaginations are tion with the enterou. (Rethe anlagen of the segments and increase in    “"d
the anlagen of the segments and increase in    “"d
number as new ones are formed behind.
number as new ones are formed behind.


Line 4,789: Line 4,442:
In many cases the coelomic sacs are formed by solid outgrowth from
In many cases the coelomic sacs are formed by solid outgrowth from
the gut. As already mentioned, the collar and body cavities of the New
the gut. As already mentioned, the collar and body cavities of the New
England tornaria originate by outgrowths from the gut. There are sim-
England tornaria originate by outgrowths from the gut. There are similar cases among the eehinoderms, for in Ophiothrix fragz'l2's the two coelome anlagen have at first no lumen, and also among the brachiopods a
ilar cases among the eehinoderms, for in Ophiothrix fragz'l2's the two coe-
lome anlagen have at first no lumen, and also among the brachiopods a
similar condition prevails. In the tunicates likewise mesoderm originates
similar condition prevails. In the tunicates likewise mesoderm originates
as a solid outgrowth from the primitive gut.
as a solid outgrowth from the primitive gut.
Line 4,805: Line 4,456:
and inner splanchnic layers of the mesodermal sacs. The vertebrates do
and inner splanchnic layers of the mesodermal sacs. The vertebrates do
not show the division of the mesodcrm into primitive segments from
not show the division of the mesodcrm into primitive segments from
the first, as does amphioxus, but the segmentation appears later in the
the first, as does amphioxus, but the segmentation appears later in the
form of ring-shaped invaginations. Under the dorsal lip of the blaste-
form of ring-shaped invaginations. Under the dorsal lip of the blastepore the invagination is deep and elsewhere it is hollow. The mesodcrm
pore the invagination is deep and elsewhere it is hollow. The mesodcrm
formed near the dorsal lip is called the gastral mesodcrm, and the mesoderm formed all around the blastopore itself is called the peristemial
formed near the dorsal lip is called the gastral mesodcrm, and the meso-
derm formed all around the blastopore itself is called the peristemial
mesodcrm.
mesodcrm.


   
   


FIG. 90. Gastrula of Rana fusca. (Redrawn from Ziegler, after Schwink.)
fiG. 90. Gastrula of Rana fusca. (Redrawn from Ziegler, after Schwink.)
ch, chorda anluge; ec, ectederm; en, endoderm. n1, mesodcrm, g, gastral cavity.
ch, chorda anluge; ec, ectederm; en, endoderm. n1, mesodcrm, g, gastral cavity.


Line 4,827: Line 4,476:
blood islands form here. In the more posterior region of the embryo
blood islands form here. In the more posterior region of the embryo
the mesodcrm is formed by ingrowth of cells from mesodcrm forming
the mesodcrm is formed by ingrowth of cells from mesodcrm forming
grooves of the endoderm. One of these grooves is adjacent to the note-
grooves of the endoderm. One of these grooves is adjacent to the notechordal region and the other is peripheral. From these grooves groups of
chordal region and the other is peripheral. From these grooves groups of
cells grow into the peripheral blastocoele.
cells grow into the peripheral blastocoele.
THEORIES OF THE ORIGIN OF THE COELOME 133
THEORIES OF THE ORIGIN OF THE COELOME 133
Line 4,839: Line 4,487:
the Bahamas.
the Bahamas.


In general the mesoderm formation of Phoromls-, one of the Mollus-
In general the mesoderm formation of Phoromls-, one of the Molluseoidea, is from scattered mesenehyme. Phoronis has an invaginate gastrula. At this stage single endodermal cells migrate into the blastoeoele
eoidea, is from scattered mesenehyme. Phoronis has an invaginate gas-
trula. At this stage single endodermal cells migrate into the blastoeoele
and become mesenehyme. This migration appears to be especially great
and become mesenehyme. This migration appears to be especially great
in the region of the edge of the blastopore. The mesenchyme cells which
in the region of the edge of the blastopore. The mesenchyme cells which
are at first scattered in the blaste-
are at first scattered in the blastecoele early show an inclination to lie
coele early show an inclination to lie
on the inner surface of the ectoderm,
on the inner surface of the ectoderm,
and later on the gut endoderm. Thus
and later on the gut endoderm. Thus
Line 4,854: Line 4,499:
a method of mesoderm formation is
a method of mesoderm formation is


FIG. 91. Oblique section through gas-
fiG. 91. Oblique section through gas
 
prhnltiva We "light infer that Such trula of Phm-om's sahatieri. (Redrawn from
prhnltiva We "light infer that Such trula of Phm-om's sahatieri. (Redrawn from


is the case since Morgan’s tornaria Iforst-halt and H_eidor. after Selys-Lomz-
is the case since Morgan’s tornaria Iforst-halt and H_eidor. after Selys-Lomzfrom the Bahamas shows this kind cmnms) Sh°w‘(';§es_;'_"°s°n°hyme cells
from the Bahamas shows this kind cmnms) Sh°w‘(';§es_;'_"°s°n°hyme cells
of mesoderm formation and other
of mesoderm formation and other


Line 4,868: Line 4,511:
III. THEORIES OF THE ORIGIN OF THE COELOME
III. THEORIES OF THE ORIGIN OF THE COELOME


A discussion of the origin of the mesoderm involves also a considera-
A discussion of the origin of the mesoderm involves also a consideration of the origin of the coelome. We might define the coelome as a body
tion of the origin of the coelome. We might define the coelome as a body
cavity lined by peritoneum from which arise the gonads. The tissue of
cavity lined by peritoneum from which arise the gonads. The tissue of
the coelome, as of all other mesoderm, must necessarily arise from the
the coelome, as of all other mesoderm, must necessarily arise from the
Line 4,878: Line 4,520:
The theories of the origin of the coelome are of course hypothetical.
The theories of the origin of the coelome are of course hypothetical.
There are three main theories, the enteroeoele theory, the gonoeoele
There are three main theories, the enteroeoele theory, the gonoeoele
theory, and the nephrocoele theory. The enteroeoele theory was first
theory, and the nephrocoele theory. The enteroeoele theory was first
suggested by Leuekart in 1848 in one of his first papers on the coelenter-
suggested by Leuekart in 1848 in one of his first papers on the coelenterates. According to this theory, the coelome of higher forms is represented by the radial canals and gastric pouches of medusae. The gastric
ates. According to this theory, the coelome of higher forms is repre-
sented by the radial canals and gastric pouches of medusae. The gastric
cavity of coelenterates thus corresponds to both the gastric cavity and
cavity of coelenterates thus corresponds to both the gastric cavity and
coelome of worms and higher forms. This original idea was suggested
coelome of worms and higher forms. This original idea was suggested
134 MESODERM FORMATION
134 MESODERM FORMATION


long before Kowalevsky and Metchnikofi found that the coelome of
long before Kowalevsky and Metchnikofi found that the coelome of
forms such as Sagitta, brachiopods, echinoderms, and amphioxus really
forms such as Sagitta, brachiopods, echinoderms, and amphioxus really
develops from gut pouches. The enterocoele or gut-po11ch theory was
develops from gut pouches. The enterocoele or gut-po11ch theory was
Line 4,897: Line 4,537:
to bear the functions of gonoducts or nephridia. Since the ancestry of
to bear the functions of gonoducts or nephridia. Since the ancestry of
the vertebrates is so problematical, this theory as applied to them must
the vertebrates is so problematical, this theory as applied to them must
be largely conjectural. Lang finally gave up this theory for another.
be largely conjectural. Lang finally gave up this theory for another.


This theory may be true as applied to the entcrocoelous or vertebrate
This theory may be true as applied to the entcrocoelous or vertebrate
Line 4,905: Line 4,545:


Hatschek is responsible for the gonocoele theory of coelome formation,
Hatschek is responsible for the gonocoele theory of coelome formation,
suggesting it in 1876. According to this theory, the pole cells of the tele-
suggesting it in 1876. According to this theory, the pole cells of the teleblasts are primordial germ cells, and the germ band, in which the
blasts are primordial germ cells, and the germ band, in which the
coelome develops, is homologous to a gonad. Lang and others took 11p
coelome develops, is homologous to a gonad. Lang and others took 11p
this theory and assumed that the original ancestral type has essentially
this theory and assumed that the original ancestral type has essentially
the same morphology as a rotifer or flatworm. They suggested that the
the same morphology as a rotifer or flatworm. They suggested that the
original gonad cavity was still connected to the outside by the gonoduct.
original gonad cavity was still connected to the outside by the gonoduct.
Along with the extensions of the gonad cavity, a corresponding reduction
Along with the extensions of the gonad cavity, a corresponding reduction
Line 4,917: Line 4,556:
gonad are partly sterile, the eggs or sperm fall into the coelome and
gonad are partly sterile, the eggs or sperm fall into the coelome and
are taken up by the gonoducts. This theory explains also the reduction
are taken up by the gonoducts. This theory explains also the reduction
of the spaces in the flat worm occupied by the circulatory fluid. These
of the spaces in the flat worm occupied by the circulatory fluid. These
spaces are entirely outside the body cavity and from them are formed the
spaces are entirely outside the body cavity and from them are formed the
blood vessels. In some annelids there is a sinus-like blood system in at
blood vessels. In some annelids there is a sinus-like blood system in at
Line 4,923: Line 4,562:
condition.
condition.


The nephrocoele theory is due chiefly to Ziegler, who regards the
The nephrocoele theory is due chiefly to Ziegler, who regards the
coelome as primarily and originally an organ of excretion. This organ
coelome as primarily and originally an organ of excretion. This organ
consisted of a vesicle, the nephrocoele, and its duct. By its expansion a
consisted of a vesicle, the nephrocoele, and its duct. By its expansion a
modification of the coelome is produced.
modification of the coelome is produced.


These three views are not as sharply distinguished from each other
These three views are not as sharply distinguished from each other
Line 4,989: Line 4,628:
PLANULA
PLANULA


SCYPHISTOMA (Hydra-
SCYPHISTOMA (Hydratuba)
tuba)
Scyphula
Scyphula
Ephyra
Ephyra
Line 5,002: Line 4,640:


MI’JrLLEn’s Larva
MI’JrLLEn’s Larva
Sporocyst, Miricid-
Sporocyst, Miricidium, Redia, Cercaria.
ium, Redia, Cer-
caria.
Cysticercus
Cysticercus
PILIDIUM
PILIDIUM
Line 5,014: Line 4,650:
Actinotrocha.
Actinotrocha.
Cyphonautes (Closely
Cyphonautes (Closely
related to trocho-
related to trocho
 
phore)
(Related to trocho-
phore)
phore)
(Related to trochophore)


TYPES OF INVERTEBRATE LARVAE
TYPES OF INVERTEBRATE LARVAE
Line 5,026: Line 4,660:
Sycandra raphnnus
Sycandra raphnnus


Leucosolenia vari-
Leucosolenia vari
 
abilis
abilis
Clathrina blancu
Clathrina blancu
Line 5,036: Line 4,669:


Actinia urticinia
Actinia urticinia
In family Cere:Ln-
In family Cere:Lnthidue
thidue


Zoanthidac
Zoanthidac
Line 5,061: Line 4,693:
Phylum R Larger Group Larva Type Genus
Phylum R Larger Group Larva Type Genus


'l‘ro<:l1clmintl1e.s Rotifora (Supposed to be per-
'l‘ro<:l1clmintl1e.s Rotifora (Supposed to be per
 
sistent trochophore,
sistent trochophore,


but early develop-
but early develop
 
ment is not in ac
ment is not in ac-
 
cord with this view)
cord with this view)
Cllrzetognzltlla (Fairly direct) Sagitta
Cllrzetognzltlla (Fairly direct) Sagitta
Line 5,075: Line 4,704:
A few decapods
A few decapods


Metanauplius, Proto-
Metanauplius, Protozoaea, Zoaea, Calyptopsis, Copepodid,
zoaea, Zoaea, Calyp-
topsis, Copepodid,
Metazoaea, Mysis,
Metazoaea, Mysis,
Phyllosoma, Mega—
Phyllosoma, Mega—
Line 5,086: Line 4,713:
zoaea)
zoaea)
Alima
Alima
Insecta Larva, pupa, cater-
Insecta Larva, pupa, caterpillar (eruoiform)
pillar (eruoiform)
Campodeiform
Campodeiform
Mollusca Gastropoda Ctenophore stage Patella
Mollusca Gastropoda Ctenophore stage Patella
Line 5,113: Line 4,739:
an amazing diversity in the methods by which the adult is reached after
an amazing diversity in the methods by which the adult is reached after
the period of germ-layer formation has been passed through. In some
the period of germ-layer formation has been passed through. In some
groups most complicated life histories involving adaptations to environ-
groups most complicated life histories involving adaptations to environments that are totally different from that in which the cleaving egg
ments that are totally different from that in which the cleaving egg
found itself are present, while in other groups development is simple
found itself are present, while in other groups development is simple
and direct. Of these many types of invertebrate larvae it is possible to
and direct. Of these many types of invertebrate larvae it is possible to
describe only a few in this chapter. No attempt is made here to de-
describe only a few in this chapter. No attempt is made here to describe the cases of direct development as they occ11r in the various
scribe the cases of direct development as they occ11r in the various
phyla, but it is desired to explain how certain important invertebrate
phyla, but it is desired to explain how certain important invertebrate
larval types undergo their metamorphoses and reach the adult condi-
larval types undergo their metamorphoses and reach the adult condition. In the table showing the occurrence of the Various types of invertebrate larvae these forms which are selected for description are indicated by small capitals, while the others mentioned are of less general
tion. In the table showing the occurrence of the Various types of inver-
tebrate larvae these forms which are selected for description are indi-
cated by small capitals, while the others mentioned are of less general


significance and are for reference.
significance and are for reference.


I. THE PORIFERA
I. THE PORIFERA
Line 5,133: Line 4,754:
is known as an amphiblastula. Its development has been investigated
is known as an amphiblastula. Its development has been investigated
in a number of forms, among the best known of which is Sycandra
in a number of forms, among the best known of which is Sycandra
raphanus (see Fig. 64) studied by Schultze in 1875. Other important
raphanus (see fig. 64) studied by Schultze in 1875. Other important
studies are the series of papers of Maas on various sponges, and the
studies are the series of papers of Maas on various sponges, and the
studies of Minehin on Leucosolenia.
studies of Minehin on Leucosolenia.
Line 5,140: Line 4,761:
position which they occupy when ripe and where the early stages of
position which they occupy when ripe and where the early stages of
development are passed. (In Cliona, the boring sponge, the early stages
development are passed. (In Cliona, the boring sponge, the early stages
of development take place externally.) In a cavity near a flagellated
of development take place externally.) In a cavity near a flagellated
chamber which has a definite cellular lining the cleavage stages are
chamber which has a definite cellular lining the cleavage stages are
undergone, forming an embryo of characteristic appearance known as an
undergone, forming an embryo of characteristic appearance known as an
amphiblastula. At length the embryo emerges into the flagellated
amphiblastula. At length the embryo emerges into the flagellated
chamber and thence passes to the outside to become free swimming.
chamber and thence passes to the outside to become free swimming.
After twenty—four to forty-eight hours of swimming about, it gradually
After twenty—four to forty-eight hours of swimming about, it gradually
finds lodgment and attachment to a substratum, a process which is
finds lodgment and attachment to a substratum, a process which is


138
138
THE AMPHIBLASTULA 139
THE AMPHIBLASTULA 139
spoken of as fixation, and which involves a complete and quite sudden
spoken of as fixation, and which involves a complete and quite sudden
metamorphosis. In different genera of sponges the events do not all take
metamorphosis. In different genera of sponges the events do not all take
place in exactly the same order nor do the larvae reach the same degree
place in exactly the same order nor do the larvae reach the same degree
of advancement at the time of emergence or of fixation. The essential
of advancement at the time of emergence or of fixation. The essential
principles of development are probably not dissimilar, however.
principles of development are probably not dissimilar, however.


The free-swimming larva is at first an ovoid blastula in which there
The free-swimming larva is at first an ovoid blastula in which there
are cells of two obviously different sorts. The large anterior portion
are cells of two obviously different sorts. The large anterior portion
of the embryo is composed of flagellated cells and the posterior portion
of the embryo is composed of flagellated cells and the posterior portion
of larger, non-flagellated, granular cells. Originally open at both ends,
of larger, non-flagellated, granular cells. Originally open at both ends,
the blastula soon grows so that the pointed end is closed and rounded
the blastula soon grows so that the pointed end is closed and rounded
out and the cells become columnar in form and flagellated. The opening
out and the cells become columnar in form and flagellated. The opening
at the other end is surrounded by the granular cells which upon its
at the other end is surrounded by the granular cells which upon its
closure take the form of a flat layer, some of whose cells proliferate and
closure take the form of a flat layer, some of whose cells proliferate and
presently push into the cavity. It is supposed
presently push into the cavity. It is supposed
that the flattening is due to pressure against
that the flattening is due to pressure against
the unyielding Inass of spicules, while the
the unyielding Inass of spicules, while the
columnar cells produce a swelling into the space
columnar cells produce a swelling into the space
of the flagellated chamber adjacent. This is the
of the flagellated chamber adjacent. This is the
condition in which the embryos are extruded
condition in which the embryos are extruded
to form free-swimming larvae.
to form free-swimming larvae.
Line 5,176: Line 4,797:
regions, a refractile portion at the internal end
regions, a refractile portion at the internal end
and a sharply marked-off granular part at the
and a sharply marked-off granular part at the
outer end‘. In living embryos the two.portions FIG 92‘ Amphiblasmln of
outer end‘. In living embryos the two.portions fiG 92‘ Amphiblasmln of
are so distinct as to give superficially the Sycandra. (After Schultze.)
are so distinct as to give superficially the Sycandra. (After Schultze.)
appearance of an inner layer of refractile cells
appearance of an inner layer of refractile cells
covered by an outer granular layer of cells; they are, however,
covered by an outer granular layer of cells; they are, however,
merely parts of the same layer. Between the columnar and the
merely parts of the same layer. Between the columnar and the
posterior granular cells of this form is a zone of intermediate cells
posterior granular cells of this form is a zone of intermediate cells
which are flagellated and entirely granular. The flagellated cells
which are flagellated and entirely granular. The flagellated cells
are much more numerous but much smaller than the granular cells.
are much more numerous but much smaller than the granular cells.
As development proceeds, the number of granular cells increases at the
As development proceeds, the number of granular cells increases at the
expense of the flagellated ones.
expense of the flagellated ones.


The larvae of Leucosolenia are transparent so that a mass of yellowish-
The larvae of Leucosolenia are transparent so that a mass of yellowishbrown pigment at the center may be easily seen. This is shown by
brown pigment at the center may be easily seen. This is shown by
sections to have the form of a tube open in front and behind, enclosing
sections to have the form of a tube open in front and behind, enclosing
a lens-like body of gelatinous character which fills the central, blaste-
a lens-like body of gelatinous character which fills the central, blasteaoelic space. The central cells are so arranged that Minchin regarded
aoelic space. The central cells are so arranged that Minchin regarded
this structure as a premature, light-perceiving organ of larval significance only. i
this structure as a premature, light-perceiving organ of larval signifi-
cance only. i


The free-swimming stage of the amphiblastulae is not of long duration.
The free-swimming stage of the amphiblastulae is not of long duration.
Line 5,200: Line 4,818:
They remain at the surface for perhaps a day, then sink to the bottom
They remain at the surface for perhaps a day, then sink to the bottom
and after another twelve hours of swimming there they are ready for
and after another twelve hours of swimming there they are ready for
fixation. Fixation takes place at the anterior pole, the granular cells
fixation. fixation takes place at the anterior pole, the granular cells
growing about and enclosing the flagellated cells in the process of
growing about and enclosing the flagellated cells in the process of
metamorphosis. This process involves in some genera also the active
metamorphosis. This process involves in some genera also the active
invagination of the flagellated
invagination of the flagellated
cells. At this stage only the two
cells. At this stage only the two
kinds of cells may be distinguished,
kinds of cells may be distinguished,
Line 5,218: Line 4,836:
dermal layer differentiates and
dermal layer differentiates and
two kinds of cells result, one
two kinds of cells result, one
superficial, the other migrating
superficial, the other migrating
beneath the former. They differ
beneath the former. They differ
also in the type of spicules which
also in the type of spicules which
they are to secrete, the superficial
they are to secrete, the superficial
producing the monaxones and the
producing the monaxones and the
other the triradiate spicules. The
other the triradiate spicules. The
Line 5,233: Line 4,851:
F10. 93.
F10. 93.


Fixation of the larx a of Sycandra
fixation of the larx a of Sycandra


Iaphanus. (After Sehultze)
Iaphanus. (After Sehultze)


A, flagellated cells retreating into the in-
A, flagellated cells retreating into the interior; B, cup—shaped larva attached by
terior; B, cup—shaped larva attached by
amocboid processes of the outer granular
amocboid processes of the outer granular
layer, f.c., flagellated cells; g.c., granular
layer, f.c., flagellated cells; g.c., granular
cells.
cells.


presently (in five or six days) dc-
presently (in five or six days) dcvelops an opening to the outside,
velops an opening to the outside,
the osculum, and becomes more
the osculum, and becomes more
complicated. The cells themselves
complicated. The cells themselves
elongate and assume the typical
elongate and assume the typical


collared appearance of choano-
collared appearance of choanocytes. The development of the pores and canals is a matter of slow
cytes. The development of the pores and canals is a matter of slow
growth, involving the formation of pouches and the rearrangement of
growth, involving the formation of pouches and the rearrangement of
cells, the secretion of spicules and gelatinous intercellular substance.
cells, the secretion of spicules and gelatinous intercellular substance.
Other types of larvae have been described for sponges but they may
Other types of larvae have been described for sponges but they may
all be regarded as modifications of the amphiblastula type just described,
all be regarded as modifications of the amphiblastula type just described,
as was shown by Maas (1898). Some sponges also reproduce by forma-
as was shown by Maas (1898). Some sponges also reproduce by formation of gemmules, but this is a process of budding and no free-swimming
tion of gemmules, but this is a process of budding and no free-swimming
larvae are developed.
larvae are developed.
THE PLAN ULA 141
THE PLAN ULA 141
Line 5,279: Line 4,893:
   
   


and the character of the ciliated planula. (After Metschnikofi.)
and the character of the ciliated planula. (After Metschnikofi.)


Actinozoa and Seyphozoa. Because of its simple character and its wide-
Actinozoa and Seyphozoa. Because of its simple character and its widespread occurrence, an evolutionary significance as the ancestral coelenterate is suggested. It is the most important larval stage of this phylum.
spread occurrence, an evolutionary significance as the ancestral coelen-
terate is suggested. It is the most important larval stage of this phylum.


The term planula was formerly applied to a blastula stage, but the
The term planula was formerly applied to a blastula stage, but the
Line 5,292: Line 4,904:
many-celled, unipolar ingressions. There are numerous cases in both
many-celled, unipolar ingressions. There are numerous cases in both
Actinozoa and Scyphozoa in which the endoderm is hollow. The gastral
Actinozoa and Scyphozoa in which the endoderm is hollow. The gastral
cavity does not appear in the hydroids until about the time of attach-
cavity does not appear in the hydroids until about the time of attachment of the swimming larvae. In Pennaria the hydranths are not
ment of the swimming larvae. In Pennaria the hydranths are not
covered by a hydrotheea; each has two circles of tentacles, one about the
covered by a hydrotheea; each has two circles of tentacles, one about the
142 TYPES OF INVERTEBRATE LARVAE
142 TYPES OF INVERTEBRATE LARVAE
Line 5,306: Line 4,917:
they die. In this genus the Inedusa is the less important of the two
they die. In this genus the Inedusa is the less important of the two
generations. The fertilized egg as described by Hargitt goes through a
generations. The fertilized egg as described by Hargitt goes through a
very irregular cleavage, forming an irregular cell mass which differen-
very irregular cleavage, forming an irregular cell mass which differentiates into a solid planula of two layers, the
tiates into a solid planula of two layers, the
outer ciliate(l. After perhaps twelve hours of
outer ciliate(l. After perhaps twelve hours of
swimming about, the planula begins to settle
swimming about, the planula begins to settle
Line 5,316: Line 4,926:


In some forms, notably Tubularia, an
In some forms, notably Tubularia, an
intermediate larval form, the aetinula, in-
intermediate larval form, the aetinula, intervenes between the planula and the attached
tervenes between the planula and the attached
stage. It is neither fixed nor swimming, but
stage. It is neither fixed nor swimming, but
creeping, and is formed by the appearance
creeping, and is formed by the appearance
upon the planula of blunt protuberances, the
upon the planula of blunt protuberances, the


Fm 95_ Enema, features of tentacle buds, which gradually grow longer.
Fm 95_ Enema, features of tentacle buds, which gradually grow longer.
the various stages of develop- First appear the rudiments of the aboral
the various stages of develop- first appear the rudiments of the aboral


ment of the embryo of Tubularm _ - ,
ment of the embryo of Tubularm _ - ,
Line 5,338: Line 4,947:
rapidly and gives rise to the buds which are to form the different zooids
rapidly and gives rise to the buds which are to form the different zooids
of the colony. Thus the aetinula larva is important as the ancestor
of the colony. Thus the aetinula larva is important as the ancestor
hypothecated by Brooks for the origin of the diverse kinds of coelen-
hypothecated by Brooks for the origin of the diverse kinds of coelen
 
terates.
terates.


Line 5,355: Line 4,963:
is commonly done, to form a series with Cumna and Lmope at one end,
is commonly done, to form a series with Cumna and Lmope at one end,


FIG 96 A, gonophores of Tubularuz mdwzsa containing embryos B, creeping Actinula
fiG 96 A, gonophores of Tubularuz mdwzsa containing embryos B, creeping Actinula
larvae, C, attached form of Tubularza, mdwzsa (Redmwn from Allman )
larvae, C, attached form of Tubularza, mdwzsa (Redmwn from Allman )


Line 5,366: Line 4,974:


Obelia, Bougainvillea (medusa and hydranth alternating and of equal importance)
Obelia, Bougainvillea (medusa and hydranth alternating and of equal importance)
Pennaria (medusa fixed during sex cell stage, and of reduced importance)
Pennaria (medusa fixed during sex cell stage, and of reduced importance)
Gonothryca
Gonothryca


Line 5,379: Line 4,987:
evolution of this series cannot have been gone through from Hydra
evolution of this series cannot have been gone through from Hydra
toward Cunina. On the other hand to assume the medusa. to be the more
toward Cunina. On the other hand to assume the medusa. to be the more
primitive form of the two types is hardly in keeping with obvious struc-
primitive form of the two types is hardly in keeping with obvious structural features, and for this reason it is not possible to regard this series
tural features, and for this reason it is not possible to regard this series
as having begun with a form similar to Cunina and to have been evolved
as having begun with a form similar to Cunina and to have been evolved
in the reverse order. Rather some such suggestion as that made long ago
in the reverse order. Rather some such suggestion as that made long ago
Line 5,386: Line 4,993:
suggestion the most primitive type is neither a medusa nor a hydranth,
suggestion the most primitive type is neither a medusa nor a hydranth,
but some small generalized form like the actinula. From this it may be
but some small generalized form like the actinula. From this it may be
supposed that four, perhaps five, series of forms have been derived.
supposed that four, perhaps five, series of forms have been derived.
First there is the hydroid colony like Obelia in which both medusae and
first there is the hydroid colony like Obelia in which both medusae and
hydranths are present in alternating fashion. The remainder of the
hydranths are present in alternating fashion. The remainder of the
series from Obelia through Pennaria to Eudendrium and possibly to
series from Obelia through Pennaria to Eudendrium and possibly to
Line 5,394: Line 5,001:
produced Cunina and Aeginopsis in which no hydranth is present.
produced Cunina and Aeginopsis in which no hydranth is present.
Perhaps a third produced hydra-like forms at the other end with no
Perhaps a third produced hydra-like forms at the other end with no
medusae. The Scyphozoa and the Actinozoa are the fourth and fifth
medusae. The Scyphozoa and the Actinozoa are the fourth and fifth
series respectively which owe their origin to this primitive form of
series respectively which owe their origin to this primitive form of
coelenterate, the actinula—like form.
coelenterate, the actinula—like form.


Of this form the planula is the larval type (Fig. 94). It is the free-
Of this form the planula is the larval type (fig. 94). It is the freeswimming larva common to all coelenterate groups. In some, the
swimming larva common to all coelenterate groups. In some, the
Hydrozoa and many Aetinozoa, it is a solid mass of endoderm with an
Hydrozoa and many Aetinozoa, it is a solid mass of endoderm with an
ectodermal covering. In others, the Scyphozoa and some Actinozoa, the
ectodermal covering. In others, the Scyphozoa and some Actinozoa, the
endoderm is a definite layer with a gastral cavity. The latter is held by
endoderm is a definite layer with a gastral cavity. The latter is held by
some workers to be the more primitive of the two, for it is argued that as
some workers to be the more primitive of the two, for it is argued that as
the organisms were evolved an animal with a solid internal mass of cells
the organisms were evolved an animal with a solid internal mass of cells
would be quite unable to support itself. An embryonic type developing
would be quite unable to support itself. An embryonic type developing
from stored yolk material would find no such difliculty, and so the solid
from stored yolk material would find no such difliculty, and so the solid
form of the planula was thought to be secondary.
form of the planula was thought to be secondary.


The general plan of coelenterate embryology is now clear. The fer-
The general plan of coelenterate embryology is now clear. The fertilized egg develops gradually into a planula which swims about for a
tilized egg develops gradually into a planula which swims about for a
time and, it may be after intervening larval stages have been passed
time and, it may be after intervening larval stages have been passed
SCYPHOZOAN LARVAE ' 145
SCYPHOZOAN LARVAE ' 145
Line 5,416: Line 5,021:
through, settles down, attaches, and elongates into a hydra-like form
through, settles down, attaches, and elongates into a hydra-like form
representing the hydranth generation. This may grow into a hydroid
representing the hydranth generation. This may grow into a hydroid
colony or into the coral polyp or actinian, or go through further develop-
colony or into the coral polyp or actinian, or go through further development processes to produce asexually a. rnedusa which in turn produces
ment processes to produce asexually a. rnedusa which in turn produces
new germ cells.
new germ cells.


Line 5,450: Line 5,054:
Aurelia may serve as a convenient type. F1 G. 97.
Aurelia may serve as a convenient type. F1 G. 97.


_ _ . A, free-swimming pla-
_ _ . A, free-swimming plaThe eggs are shed 1nto the digestive nula of Aurclia aurita; B. section
The eggs are shed 1nto the digestive nula of Aurclia aurita; B. section


through s(-yplustoma having four
through s(-yplustoma having four
Line 5,460: Line 5,063:


the oral arms where they undergo those processes which lead to the planula
the oral arms where they undergo those processes which lead to the planula
stages. Then they emerge and swim about freely. Histological differen-
stages. Then they emerge and swim about freely. Histological differentiation continues, and the larvae are ready for attachment in four or
tiation continues, and the larvae are ready for attachment in four or
five days. After attachment the larva elongates and broadens out, the
five days. After attachment the larva elongates and broadens out, the
mouth opening becomes widened and four tentacle buds appear between
mouth opening becomes widened and four tentacle buds appear between
which the taenolae, endodermal ridges projecting into the gastral
which the taenolae, endodermal ridges projecting into the gastral
146 TYPES OF INVERTEBRATE LARVAE
146 TYPES OF INVERTEBRATE LARVAE


cavity, develop. This larva with its flattened, broadly open, oral disc is
cavity, develop. This larva with its flattened, broadly open, oral disc is
spoken of variously as a scyphistoma, scyphula, or hydra-tuba. Second-
spoken of variously as a scyphistoma, scyphula, or hydra-tuba. Secondary tentacles develop between the original four and then continue to
ary tentacles develop between the original four and then continue to
form until the appropriate number is reached. After further differentiation, the process sets in which distinguishes scyphozoan development
form until the appropriate number is reached. After further differentia-
from other types. It is the cutting off of its oral disc by means of a constriction around the scyphistonia to form an ephyra larva. This process
tion, the process sets in which distinguishes scyphozoan development
from other types. It is the cutting off of its oral disc by means of a con-
striction around the scyphistonia to form an ephyra larva. This process
is known as strobilization and iii a well—fed scyphistoma may take place
is known as strobilization and iii a well—fed scyphistoma may take place
repeatedly until a dozen or fifteen cphyrae are formed from the one larva.
repeatedly until a dozen or fifteen cphyrae are formed from the one larva.


   
   


1‘i(. ‘)5 iSti‘obiliz.it1on of Auiclia amila (Rednivm from Claus)
1‘i(. ‘)5 iSti‘obiliz.it1on of Auiclia amila (Rednivm from Claus)
t, tentacles of strobila t..ie taeniolac, g fiist tiiuisx crsc giome, I, lobes of cphvi 1
t, tentacles of strobila t..ie taeniolac, g fiist tiiuisx crsc giome, I, lobes of cphvi 1


The more usual condition is for each scyphistoma to produce two 01
The more usual condition is for each scyphistoma to produce two 01
Line 5,488: Line 5,087:


The ephyra now continues rapidly its development and differentiation
The ephyra now continues rapidly its development and differentiation
leading to the form of the adult jellyfish. The scyphistoma tentacles aie
leading to the form of the adult jellyfish. The scyphistoma tentacles aie
resorbed and in their place the characteristic lobes of the ephyra appear.
resorbed and in their place the characteristic lobes of the ephyra appear.
The oral cone lengthens into the manubrium and other changes occur
The oral cone lengthens into the manubrium and other changes occur
which result in the metamorphosis of the ephyra into the jellyfish.
which result in the metamorphosis of the ephyra into the jellyfish.


III. THE PLATYHELMINTHES
III. THE PLATYHELMINTHES


Development in the flatworms presents many diverse aspects. Some
Development in the flatworms presents many diverse aspects. Some
eggs undergo no metamorphosis but pass directly into the adult condi-
eggs undergo no metamorphosis but pass directly into the adult condiMULLER’S LARVA 147
MULLER’S LARVA 147


tion. Others reach their final development only after passing through
tion. Others reach their final development only after passing through


‘the most complicated life histories, involving (lifferent hosts, totally
‘the most complicated life histories, involving (lifferent hosts, totally


different environmental conditions, and totally different types of organ-
different environmental conditions, and totally different types of organization. Since it is not the purpose of this chapter to follow through life
ization. Since it is not the purpose of this chapter to follow through life
histories, but merely to show the relations of types of larvae to embryos
histories, but merely to show the relations of types of larvae to embryos
and adults to which they are related, only meager reference can be made
and adults to which they are related, only meager reference can be made
Line 5,533: Line 5,130:
tftu lll)(‘I‘Iil()n (l{e(lrmn from ( lms)
tftu lll)(‘I‘Iil()n (l{e(lrmn from ( lms)


gf Lttslrlt hl um ms mu nmnth rl, \ uious ruli ll lobes of H1111-lll\(‘ an! ‘I n m 11-
gf Lttslrlt hl um ms mu nmnth rl, \ uious ruli ll lobes of H1111-lll\(‘ an! ‘I n m 11gm ll sense org ins
gm ll sense org ins


free-swimming larva of the polyelad Tuibellaiia named after its dis-
free-swimming larva of the polyelad Tuibellaiia named after its discoverer, Johannes Muller.
coverer, Johannes Muller.


1. Mii1ler’s Larva
1. Mii1ler’s Larva


The development of the polyclads is known chiefly from an older
The development of the polyclads is known chiefly from an older
study by Lang or Yungza and a later and more detailed investigation
study by Lang or Yungza and a later and more detailed investigation
by Surface on the embryology of Planocera mquzlma. The cleavage is
by Surface on the embryology of Planocera mquzlma. The cleavage is
Line 5,548: Line 5,143:
formative substances surprisingly like that in the higher forms; the
formative substances surprisingly like that in the higher forms; the
similarity is especially surprising when it is remembered that the
similarity is especially surprising when it is remembered that the
Turbellaria agree closely with the etenophores in many points of struc-
Turbellaria agree closely with the etenophores in many points of structure Gastrulation is by the method characteristic of eggs with spiral
ture Gastrulation is by the method characteristic of eggs with spiral
148 TYPES OF INVERTEBRATE LARVAE
148 TYPES OF INVERTEBRATE LARVAE


Line 5,572: Line 5,166:
one ventral, and the others make up three pairs laterally placed, and all
one ventral, and the others make up three pairs laterally placed, and all
are connected by a continuous ciliated band. Growth in length with the
are connected by a continuous ciliated band. Growth in length with the
gradual reduction of the lobes until the usual form of a flatworm is
gradual reduction of the lobes until the usual form of a flatworm is
reached brings about the external changes. Among the internal changes
reached brings about the external changes. Among the internal changes
involved are the development of eye-spots, the development of the
involved are the development of eye-spots, the development of the
parenchyma (which fills in the interior of the adult, and of which some
parenchyma (which fills in the interior of the adult, and of which some
cells differentiate into muscle cells), and the differentiation of the
cells differentiate into muscle cells), and the differentiation of the
brain and genital organs. The most marked changes, however, are those
brain and genital organs. The most marked changes, however, are those
Line 5,585: Line 5,179:
stomodaeum becomes everted to form the sheath of the pharynx.
stomodaeum becomes everted to form the sheath of the pharynx.
Surface records that the early cleavages as well as the maturation
Surface records that the early cleavages as well as the maturation
divisions require about one hour each. By forty—eight hours small ecto-
divisions require about one hour each. By forty—eight hours small ectodermal cells cover the entire embryo, which become ciliated, and during
dermal cells cover the entire embryo, which become ciliated, and during
the third day rotation is set up in the capsule. Eye-spots appear about
the third day rotation is set up in the capsule. Eye-spots appear about
the fourth day. By the end of the fifth day the ciliated lobes appear, and
the fourth day. By the end of the fifth day the ciliated lobes appear, and


   
   
Line 5,595: Line 5,188:
metamorphosis (After Lang )
metamorphosis (After Lang )


on the sixth the larva breaks from the egg membranes to become free-
on the sixth the larva breaks from the egg membranes to become freeswimming. It swims for some time, eventually settling to the bottom
swimming. It swims for some time, eventually settling to the bottom
and assuming the shape and habits of a typical polyclad.
and assuming the shape and habits of a typical polyclad.


Line 5,613: Line 5,205:
Trematodes are commonly divided into Monogenea and Digenea,
Trematodes are commonly divided into Monogenea and Digenea,
depending upon whether one or more than one host is necessary for their
depending upon whether one or more than one host is necessary for their
development. Since only one host is necessary in the Monogenea, devel-
development. Since only one host is necessary in the Monogenea, development is direct or nearly so, whereas in the Digenea there are often
opment is direct or nearly so, whereas in the Digenea there are often
several intervening stages. In the sheep liver—fluke, which may be chosen
several intervening stages. In the sheep liver—fluke, which may be chosen
as an example, the egg undergoes the early part of its development in a
as an example, the egg undergoes the early part of its development in a
chitinous shell while it is passing through the alimentary canal of the
chitinous shell while it is passing through the alimentary canal of the
Line 5,621: Line 5,212:
   
   


Flo 102 A B, same as above but older
flo 102 A B, same as above but older


sheep. After it has been passed from the body of the host it at length
sheep. After it has been passed from the body of the host it at length
Line 5,628: Line 5,219:
contact with a pond snail or perishes. It is said to be sensitive to the
contact with a pond snail or perishes. It is said to be sensitive to the
presence of the snails and to move toward them actively. At this time
presence of the snails and to move toward them actively. At this time
the larva is in many respects similar to a rhabdocoele turbellarian with-
the larva is in many respects similar to a rhabdocoele turbellarian without gonads. It has nearly the shape of a slender cone with two eye-spots
out gonads. It has nearly the shape of a slender cone with two eye-spots
near the head end (the broader end). There is a brain, a pair of flame
near the head end (the broader end). There is a brain, a pair of flame
cells representing the excretory system, and an imperfect intestine.
cells representing the excretory system, and an imperfect intestine.
The rest of the body is filled with germ cells. After the miracidium has
The rest of the body is filled with germ cells. After the miracidium has
penetrated the body of the snail it loses its ciliated ectoderm, the
penetrated the body of the snail it loses its ciliated ectoderm, the
enteron degenerates, and it elongates into a sporocyst, which is thus
enteron degenerates, and it elongates into a sporocyst, which is thus
Line 5,638: Line 5,228:


merely a transformed miracidium.Within the sporocyst, germ balls*
merely a transformed miracidium.Within the sporocyst, germ balls*
are budded ofl" and each begins a development similar to total cleavage
are budded ofl" and each begins a development similar to total cleavage
to form a blastosphere which in its turn is converted into a gastrula. This
to form a blastosphere which in its turn is converted into a gastrula. This
passes then into the larval type known as the redia. The redia is usually
passes then into the larval type known as the redia. The redia is usually
Line 5,647: Line 5,237:
but in summer they develop into another type of larvae, the cercaria.
but in summer they develop into another type of larvae, the cercaria.
The rediae differ externally from miracidia in the absence of cilia, of
The rediae differ externally from miracidia in the absence of cilia, of
eye-spots, and in the presence of a pharynx and a simple sac-like intes-
eye-spots, and in the presence of a pharynx and a simple sac-like intestine, and their general shape is more cylindrical with a collar or circular
tine, and their general shape is more cylindrical with a collar or circular
ridge near the anterior end and short locomotor processes near the posterior. The cercariae have in an undeveloped condition all the organs
ridge near the anterior end and short locomotor processes near the pos-
terior. The cercariae have in an undeveloped condition all the organs
which are found in the fluke and some other structures including a tail
which are found in the fluke and some other structures including a tail
which are of brief duration and last only during larval life. The cercaria
which are of brief duration and last only during larval life. The cercaria
leaves the snail, encysts upon a blade of grass, and must be eaten by a
leaves the snail, encysts upon a blade of grass, and must be eaten by a
sheep to continue its development. Its final metamorphosis consists in the
sheep to continue its development. Its final metamorphosis consists in the
loss of its tall, the rapid growth of the organs already present, and the
loss of its tall, the rapid growth of the organs already present, and the
development of its reproductive organs.
development of its reproductive organs.
Line 5,668: Line 5,256:
Cestode larvae and life histories are only a little less complicated and
Cestode larvae and life histories are only a little less complicated and
involved than are those of the trematodes. The eggs of cestodes, like
involved than are those of the trematodes. The eggs of cestodes, like
those of the trematodes, are surrounded in the uterus by a thin egg-
those of the trematodes, are surrounded in the uterus by a thin eggshell. In some forms there are also included “yolk cells” which contribute
shell. In some forms there are also included “yolk cells” which contribute
food to the developing embryo. Cleavage is irregular in type, although
food to the developing embryo. Cleavage is irregular in type, although
characteristic features are to be recognized. An outer layer of cells is
characteristic features are to be recognized. An outer layer of cells is
formed from micromeres which separate from the larger cells early in
formed from micromeres which separate from the larger cells early in
cleavage. In most cases this layer of superficial cells gives rise to a
cleavage. In most cases this layer of superficial cells gives rise to a
chitinous coat which is thrown off ultimately. Only the central mass of
chitinous coat which is thrown off ultimately. Only the central mass of
cells which is enclosed by the superficial layer takes part in the forma-
cells which is enclosed by the superficial layer takes part in the formation of the embryo. This mass of cells develops a series of six hooks and
tion of the embryo. This mass of cells develops a series of six hooks and
becomes the hexacanth embryo. The development of the hexacanth
becomes the hexacanth embryo. The development of the hexacanth


Line 5,687: Line 5,273:
coat with its inclusions of yolk material take place within the uterus
coat with its inclusions of yolk material take place within the uterus
of the posterior proglottids, and in this condition the embryo is passed
of the posterior proglottids, and in this condition the embryo is passed
to the outside; it must await its appropriate intermediate host for fur-
to the outside; it must await its appropriate intermediate host for further development. .
ther development. .


If it is ingested by the proper animal (often along with the entire
If it is ingested by the proper animal (often along with the entire
Line 5,696: Line 5,281:
or other organ. Here it encysts but continues its development. If the
or other organ. Here it encysts but continues its development. If the
intermediate host is an invertebrate the next stage is a cysticercoid; if
intermediate host is an invertebrate the next stage is a cysticercoid; if
a vertebrate, a cysticercus. The difference is chiefly in the large bladder
a vertebrate, a cysticercus. The difference is chiefly in the large bladder
or caudal vesicle of the latter. The cysticercoid has typically three parts:
or caudal vesicle of the latter. The cysticercoid has typically three parts:
scolex (the tapeworm head), a body, and a caudal vesicle, the latter
scolex (the tapeworm head), a body, and a caudal vesicle, the latter
forming an enclosure for the other developing parts inside it. In the final
forming an enclosure for the other developing parts inside it. In the final
host the scolex is pushed out, attaches with its hooks to the wall of the
host the scolex is pushed out, attaches with its hooks to the wall of the
alimentary tract and begins to grow.
alimentary tract and begins to grow.


The cysticercus is attained from the hexacanth embryo in the follow-
The cysticercus is attained from the hexacanth embryo in the following manner. The hexacanth embryo, having reached its place of encystment, enlarges markedly and its interior becomes filled with fluid or
ing manner. The hexacanth embryo, having reached its place of encyst-
ment, enlarges markedly and its interior becomes filled with fluid or
with loose spongy tissue. For this reason it is called the bladder worm
with loose spongy tissue. For this reason it is called the bladder worm
stage. A small invagination into one side appears which deepens and
stage. A small invagination into one side appears which deepens and
Line 5,711: Line 5,294:
its bottom becomes the rostellum, and the suckers appear on the inside
its bottom becomes the rostellum, and the suckers appear on the inside
of the lateral walls near their base. Metamorphosis of such a larval
of the lateral walls near their base. Metamorphosis of such a larval
form takes place after transference to the final host by the eversion of
form takes place after transference to the final host by the eversion of
the scolex and very active growth in the region just behind it to form
the scolex and very active growth in the region just behind it to form
proglottids.
proglottids.
Line 5,719: Line 5,302:
coenurus, which produces as invaginations from its wall many scolices
coenurus, which produces as invaginations from its wall many scolices
that are later to be everted. In Taenia echinococcus this polyembryonic
that are later to be everted. In Taenia echinococcus this polyembryonic
development may go even farther, the ingrowths from the wall becom-
development may go even farther, the ingrowths from the wall becoming separated off to drop into the cavity as secondary bladders. Each of
ing separated off to drop into the cavity as secondary bladders. Each of
these goes on actively producing new crops of scolices.
these goes on actively producing new crops of scolices.


Line 5,726: Line 5,308:


Of the four groups of the nemertean worms only one so far is known
Of the four groups of the nemertean worms only one so far is known
which develops by metamorphosis. In this (Heteronemertini, Schizo-
which develops by metamorphosis. In this (Heteronemertini, Schizonemertini) there are two families and the characteristic and important
nemertini) there are two families and the characteristic and important
larval form is the pilidium. In one of the families, however, there occurs
larval form is the pilidium. In one of the families, however, there occurs
a creeping form which is really a pilidium modified for creeping in keep-
a creeping form which is really a pilidium modified for creeping in keepTHE PILIDIUM 153
THE PILIDIUM 153


ing with the similar habit of the adults. This is known as the larva of
ing with the similar habit of the adults. This is known as the larva of
Desor and is that of the genus Lineus. The nemerteans, while showing a
Desor and is that of the genus Lineus. The nemerteans, while showing a
distinct advance over forms already considered in acquiring a second
distinct advance over forms already considered in acquiring a second
opening to the alimentary tract, the anus, exhibit many primitive fea-
opening to the alimentary tract, the anus, exhibit many primitive features which relate them to the flatworms and also to the ctenophorcs.
tures which relate them to the flatworms and also to the ctenophorcs.
The pilidium itself also is prophetic in certain of its features of the
The pilidium itself also is prophetic in certain of its features of the


Line 5,744: Line 5,323:
The Pilidium
The Pilidium


The eggs of Cerebratulus cleave spirally and form blastulae and gas-
The eggs of Cerebratulus cleave spirally and form blastulae and gastrulae in the manner typical for such eggs. The free-swimming pilidium
trulae in the manner typical for such eggs. The free-swimming pilidium
is a helmet-shaped larva with a spike of long cilia arising from the apical
is a helmet-shaped larva with a spike of long cilia arising from the apical
plate of cells. The cilia elsewhere are uniform in size and distribution
plate of cells. The cilia elsewhere are uniform in size and distribution
except at the margins where a ciliary wreath may be seen. This is the
except at the margins where a ciliary wreath may be seen. This is the
locomotor organ of the embryo, the prototroch. The sides of the um-
locomotor organ of the embryo, the prototroch. The sides of the umbrella-like portion are prolonged downward into hanging lobes or lappets.
brella-like portion are prolonged downward into hanging lobes or lappets.
The pilidium is produced from the symmetrical gastrula by the unequal
The pilidium is produced from the symmetrical gastrula by the unequal
development of certain parts so that the blastopore opening becomes
development of certain parts so that the blastopore opening becomes
Line 5,759: Line 5,336:


From two large cells which pass into the blastocoele the mesenehyme
From two large cells which pass into the blastocoele the mesenehyme
is produced. It consists of a mass of stellate cells whose amoeboid move-
is produced. It consists of a mass of stellate cells whose amoeboid movements may be seen through the transparent outer covering. The pseudopodia which are put out enable the cells to attach and some are converted into muscle fibres. The pilidium is completed in this condition
ments may be seen through the transparent outer covering. The pseudo-
podia which are put out enable the cells to attach and some are con-
verted into muscle fibres. The pilidium is completed in this condition
and swims about for a considerable period, perhaps two weeks, feeding
and swims about for a considerable period, perhaps two weeks, feeding
at the surface of the sea upon microscopic organisms.
at the surface of the sea upon microscopic organisms.
Line 5,782: Line 5,356:


The formation of the worin's body from the larval pilidium begins
The formation of the worin's body from the larval pilidium begins
with four eetodermal invaginations which appear on the flattened lower
with four eetodermal invaginations which appear on the flattened lower
surface. These amniotic invaginations form, in their deeper portions, the
surface. These amniotic invaginations form, in their deeper portions, the
imaginal discs which contribute largely to the definitive body of the
imaginal discs which contribute largely to the definitive body of the
worm. They are distinguished as right and left anterior, in front of the
worm. They are distinguished as right and left anterior, in front of the


Fir: 103 A. pilidium larva of Cerebralulus lactus (Redrawn from M:icBri(le, after
fir: 103 A. pilidium larva of Cerebralulus lactus (Redrawn from M:icBri(le, after
C‘ B Wilson) lap , lappet, oes , oesophagus, st , stom ieh, II|("a0ll , iiie-seneliyme cells
C‘ B Wilson) lap , lappet, oes , oesophagus, st , stom ieh, II|("a0ll , iiie-seneliyme cells
a p . apical plate B, a. pilidium Just before metamorphosis (Redr l.Wll from Mac Bride, ziftei
a p . apical plate B, a. pilidium Just before metamorphosis (Redr l.Wll from Mac Bride, ziftei
Metchnikofi ) 9, p , apical plate, a im , anterior imagimil disc oes , oesophagiis, pr , anlage
Metchnikofi ) 9, p , apical plate, a im , anterior imagimil disc oes , oesophagiis, pr , anlage
of proboscis; pt. im., posterior imaginal disc
of proboscis; pt. im., posterior imaginal disc


mouth, and right and left posterior behind it. They continue to deepen
mouth, and right and left posterior behind it. They continue to deepen
and broaden, growing up over the already formed alimentary canal until
and broaden, growing up over the already formed alimentary canal until
they finally meet and coalesce. Their outer walls form a temporary
they finally meet and coalesce. Their outer walls form a temporary
larval covering known as the amnion, a delicate envelope separating the
larval covering known as the amnion, a delicate envelope separating the
body of the worm from the covering of the larva, and the inner fused
body of the worm from the covering of the larva, and the inner fused
Line 5,801: Line 5,375:
THE PILIDIUM 155
THE PILIDIUM 155


thus included in the body of the new worm and becomes the endo-
thus included in the body of the new worm and becomes the endodermal portion of the latter.
dermal portion of the latter.


Rudiments of the other organs of the worm are developing meanwhile.
Rudiments of the other organs of the worm are developing meanwhile.
Line 5,808: Line 5,381:
a mesodermal mass which is to become the proboscis sheath. The brain
a mesodermal mass which is to become the proboscis sheath. The brain


FIG 104 l‘ullv dt-xcloped pllulinm uitli young Il(_‘l11(‘ll\ Ill sutlun its amniotic mu‘
fiG 104 l‘ullv dt-xcloped pllulinm uitli young Il(_‘l11(‘ll\ Ill sutlun its amniotic mu‘
(ltcdumn flolu lunschnlt and Hculu, after liutsrhli )
(ltcdumn flolu lunschnlt and Hculu, after liutsrhli )


Line 5,834: Line 5,407:
Echiuroidea, also have trochophore larvae, and still other larval forms
Echiuroidea, also have trochophore larvae, and still other larval forms
show relationships to the trochophore which are more or less close. In
show relationships to the trochophore which are more or less close. In
some larvae simple modifications are present and in others the relation-
some larvae simple modifications are present and in others the relationships are harder to trace. It is unquestionably the most important invertebrate type of larva, viewe(l from a phylogenetic standpoint.
ships are harder to trace. It is unquestionably the most important inver-
tebrate type of larva, viewe(l from a phylogenetic standpoint.


The trochophore larva in its simple condition is ovoid and possesses
The trochophore larva in its simple condition is ovoid and possesses
certain characteristic features, most conspicuous of which is the proto-
certain characteristic features, most conspicuous of which is the prototroch, a ciliated band about the equator. The prototroch is the chief
troch, a ciliated band about the equator. The prototroch is the chief
organ of locomotion and participates in getting food. A group of cells
organ of locomotion and participates in getting food. A group of cells
known from its position as the apical organ functions as a sense organ,
known from its position as the apical organ functions as a sense organ,
and from these sensory cells apical cilia grow out as a tuft. In some cases
and from these sensory cells apical cilia grow out as a tuft. In some cases
a metatroch, a secondary belt of cilia, is present posterior to the proto-
a metatroch, a secondary belt of cilia, is present posterior to the prototroch and a second tuft of cilia known as a tclotroch is present at the
troch and a second tuft of cilia known as a tclotroch is present at the
pole opposite to the apical tuft. Departures from the typical arrangement of cilia occur in various species. Larvae with the primary ciliated
pole opposite to the apical tuft. Departures from the typical arrange-
ment of cilia occur in various species. Larvae with the primary ciliated
band only are spoken of as monotrochal. In some, called atrochal, the
band only are spoken of as monotrochal. In some, called atrochal, the
prototroch is not developed, but cilia are present all over; in others,
prototroch is not developed, but cilia are present all over; in others,
Line 5,859: Line 5,427:
as the blastopore after a very temporary closure. The intestine meets
as the blastopore after a very temporary closure. The intestine meets
an ectodermal invagination, the proctodaeum, with which it fuses. and
an ectodermal invagination, the proctodaeum, with which it fuses. and
an opening breaks through completing the alimentary tract. An archi-
an opening breaks through completing the alimentary tract. An archinephridium is present, running from the ocsophageal region diagonally
nephridium is present, running from the ocsophageal region diagonally
to the end of the intestine. Each contains a flame cell, or solenocyte,
to the end of the intestine. Each contains a flame cell, or solenocyte,
with a cavity and a tuft of cilia, and an excretory tube leads from it. In
with a cavity and a tuft of cilia, and an excretory tube leads from it. In
some trochophores there is an eye-spot containing red pigment cells; it
some trochophores there is an eye-spot containing red pigment cells; it
Line 5,876: Line 5,443:
descendants of the 3d cell. This inequality of growth tends to push the
descendants of the 3d cell. This inequality of growth tends to push the
opening sideways. In some forms the blastopore also becomes oval in
opening sideways. In some forms the blastopore also becomes oval in
shape, then constricts in the middle, and the portion in the a-b quad-
shape, then constricts in the middle, and the portion in the a-b quadrants is pushed anteriorly by the growing cells of the d quadrant. Of
rants is pushed anteriorly by the growing cells of the d quadrant. Of
these two openings the anterior one becomes the mouth and the posterior one after temporary closure reopens to become the anus. This
these two openings the anterior one becomes the mouth and the pos-
terior one after temporary closure reopens to become the anus. This
procedure is made much of by some authorities who reason that in this
procedure is made much of by some authorities who reason that in this
manner must have come the separation of the original ingestive opening
manner must have come the separation of the original ingestive opening
into two, one of which is ingestivc and the other egcstivc.
into two, one of which is ingestivc and the other egcstivc.


In the fully grown trochophore larvae of all the groups in which it oc-
In the fully grown trochophore larvae of all the groups in which it occurs are found the points of structure as described. Indeed, the homologies
curs are found the points of structure as described. Indeed, the homologies
between the various groups are complete even to the details of trochophore development. When one considers the remarkable array of organisms which in spite of total absence of agreement in adult features have
between the various groups are complete even to the details of trocho-
this type of larval structure, he must find the fact of their common
phore development. When one considers the remarkable array of organ-
method of origin very surprising and significant. Nemerteans, rotifers,
isms which in spite of total absence of agreement in adult features have
this type of larval structure, he must find the fact of their common
method of origin very surprising and significant. Nemerteans, rotifers,
annclids, molluscs (except cephalopods), and bryozoa, form a series
annclids, molluscs (except cephalopods), and bryozoa, form a series
which certainly presents a complete gamut of adult variation, yet all
which certainly presents a complete gamut of adult variation, yet all
come from larval forms with features that are in general the same. It
come from larval forms with features that are in general the same. It
would, however, be even more surprising if there were not minor differ-
would, however, be even more surprising if there were not minor differences to be found in the trochophores. There are variations in the relation
ences to be found in the trochophores. There are variations in the relation
of the mesoderm mother cells to the gut wall, of the persistence of the
of the mesoderm mother cells to the gut wall, of the persistence of the
protonephridia, the presence of the anal vesicle, of a prototroch, of the
protonephridia, the presence of the anal vesicle, of a prototroch, of the
gastropod shell gland, and in other special organs which are the peculi-
gastropod shell gland, and in other special organs which are the peculiarities of particular groups. It is notthese differences, however, which
arities of particular groups. It is notthese differences, however, which
deserve emphasis, but the common features of development which
deserve emphasis, but the common features of development which
find expression in the widespread trochophore type.
find expression in the widespread trochophore type.


2. The Annelid Trochophore
2. The Annelid Trochophore


The metamorphosis of the trochophore into an adult annelid may
The metamorphosis of the trochophore into an adult annelid may
next be considered. It consists chiefly in the growth in length of the
next be considered. It consists chiefly in the growth in length of the
post—troehal region and in the differentiation of certain elements found
post—troehal region and in the differentiation of certain elements found
there. The essential features of the metamorphosis are (a) the elongation
there. The essential features of the metamorphosis are (a) the elongation
Line 5,915: Line 5,475:


and their resulting changes to form the head of the worm; and (c) the
and their resulting changes to form the head of the worm; and (c) the
disappearance of the ciliated bands. The processes are of course accom-
disappearance of the ciliated bands. The processes are of course accomplished gradually, there being no moment at which the trochophore ends
plished gradually, there being no moment at which the trochophore ends
and the adult begins. The post-trochal region is one of active growth,
and the adult begins. The post-trochal region is one of active growth,
differentiation, and cell multiplication. As an example of the metamor-
differentiation, and cell multiplication. As an example of the metamorphosis of the annelid trochophore, Polygordzus has been often studied,
phosis of the annelid trochophore, Polygordzus has been often studied,


FIG. 105 Troehophorc of P(ll_Ij(]0rdLu8. (After Woltereck) An , .irch1ncphr1d1um
fiG. 105 Troehophorc of P(ll_Ij(]0rdLu8. (After Woltereck) An , .irch1ncphr1d1um


11 p . apical plate, mt. intestine, mtt, mctatroeh, 0 , mouth. pr t. prototroch st
11 p . apical plate, mt. intestine, mtt, mctatroeh, 0 , mouth. pr t. prototroch st
stomach, ti 1: . telotroch.
stomach, ti 1: . telotroch.


and no other is probably better known. It has been figured by Hatschek,
and no other is probably better known. It has been figured by Hatschek,
Agassiz, and others, but is best known from the work of Woltereck.
Agassiz, and others, but is best known from the work of Woltereck.
The elongation of the post-troehal region in Polygordzus involves
The elongation of the post-troehal region in Polygordzus involves
Line 5,940: Line 5,498:
marked off from each other by constrictions which are traced on the
marked off from each other by constrictions which are traced on the
surface by transverse grooves in the ectodermal covering. Their cavities
surface by transverse grooves in the ectodermal covering. Their cavities
grow progressively, and as they expand they fill up the surrounding
grow progressively, and as they expand they fill up the surrounding
space which was the remnant of the blastocoele. Ultimately they meet
space which was the remnant of the blastocoele. Ultimately they meet
above and below the intestine, their walls fuse and break through,
above and below the intestine, their walls fuse and break through,
making a continuous pouch in each segmfint instead of a pair. Evidently
making a continuous pouch in each segmfint instead of a pair. Evidently
in the growing worm, segments are not a
in the growing worm, segments are not a
in the same degree of advancement.
in the same degree of advancement.
Line 5,952: Line 5,510:
other cells from the third quartette and
other cells from the third quartette and
by increase in number of its own cells
by increase in number of its own cells
becomes a protonephridium, a rather com-
becomes a protonephridium, a rather complicated structure whose basis is flame
plicated structure whose basis is flame
cells. The origin of the permanent nephridia
cells. The origin of the permanent nephridia
has been the cause of controversy among
has been the cause of controversy among
embryologists, particularly as to their de-
embryologists, particularly as to their derivation from ectoderm or mesoderm.
rivation from ectoderm or mesoderm.
These posterior or permanent ncphridia
These posterior or permanent ncphridia
or metanephridia grow from strings of
or metanephridia grow from strings of
Line 5,965: Line 5,521:
becomes the tubular nephridrum. In
becomes the tubular nephridrum. In
N crezs, Wilson described these as of
N crezs, Wilson described these as of
eetodermal origin except for the funnel-
eetodermal origin except for the funnelshaped opening which he hsaid lils meso- P115;-orfilfiy agljlgrdliisziiigwlirégvftgi
shaped opening which he hsaid lils meso- P115;-orfilfiy agljlgrdliisziiigwlirégvftgi
dermal. Others consider t at t e entire ‘fiolmeck
dermal. Others consider t at t e entire ‘fiolmeck
end is mesodermal and secondarily at- a_ anus? 1,. posterlor b(,,d(., 0;
end is mesodermal and secondarily at- a_ anus? 1,. posterlor b(,,d(., 0;
tached to the eetoderm. Still others think  h:*:‘:o““1i:E:SDI1 v I>F0t0neDh“d1«*
tached to the eetoderm. Still others think  h:*:‘:o““1i:E:SDI1 v I>F0t0neDh“d1«*
Line 5,997: Line 5,552:
   
   


FIG. 107. Young trochophore of Patclla cocrula. (After Wilson.)
fiG. 107. Young trochophore of Patclla cocrula. (After Wilson.)


a.p., apical plate; 111., mesodermnl cell; m.b., beginning of mesodermal band; 1no.,
a.p., apical plate; 111., mesodermnl cell; m.b., beginning of mesodermal band; 1no.,
mouth; s.g., shell gland; st., stomach.
mouth; s.g., shell gland; st., stomach.


and the foot. The velum is derived from the prototroch of the trocho-
and the foot. The velum is derived from the prototroch of the trochophore and is in the form of a bilobed, much enlarged projection abundantly provided with cilia. It serves as the locomotor organ of the voliger and disappears with metamorphosis. The shell gland is at first a
phore and is in the form of a bilobed, much enlarged projection abun-
dantly provided with cilia. It serves as the locomotor organ of the vol-
iger and disappears with metamorphosis. The shell gland is at first a
simple invagination opposite the month which may open out to form a
simple invagination opposite the month which may open out to form a
flattened disc or actually evert. Its cells secrete a thin, horny cuticle
flattened disc or actually evert. Its cells secrete a thin, horny cuticle
which is the shell of the trochophore. In the case of the bivalve molluscs
which is the shell of the trochophore. In the case of the bivalve molluscs
the rapid extension of this area forms the mantle and calcareous as well
the rapid extension of this area forms the mantle and calcareous as well
Line 6,018: Line 5,570:
The foot in the earliest stages is a thickening of the ectoderm cells just
The foot in the earliest stages is a thickening of the ectoderm cells just
ventral to the mouth. In the cavity of the slight hollow forming behind
ventral to the mouth. In the cavity of the slight hollow forming behind
this bulging foot are mesenehyme cells which contribute to the differ-
this bulging foot are mesenehyme cells which contribute to the differentiation of the organ. Other organs make their appearance in the developing veliger, including a larval kidney which disappears as the foot
entiation of the organ. Other organs make their appearance in the devel-
oping veliger, including a larval kidney which disappears as the foot
grows out, the muscles, the ganglia, gills, coelome, liver, and secondary
grows out, the muscles, the ganglia, gills, coelome, liver, and secondary
structures as crystalline sac and otocyst. The details of their develop-
structures as crystalline sac and otocyst. The details of their development are beyond the scope of the present account.
ment are beyond the scope of the present account.


The metamorphosis of the veliger into an adult-like form is not a
The metamorphosis of the veliger into an adult-like form is not a
Line 6,039: Line 5,588:
the velum; this process and some others coincident with it allow the
the velum; this process and some others coincident with it allow the
organism to assume the external shape of a small adult. The larval
organism to assume the external shape of a small adult. The larval
muscles disintegrate, the anterior region with the mouth shrinks, draw-
muscles disintegrate, the anterior region with the mouth shrinks, drawing closer together the mouth and anterior adductor and advancing the
ing closer together the mouth and anterior adductor and advancing the
front end of the foot. As a result the position of the developing gills is
front end of the foot. As a result the position of the developing gills is
changed and the intestine is shifted and straightened. Although now the
changed and the intestine is shifted and straightened. Although now the
organism has the recognizable form of an adult, it is of course very im-
organism has the recognizable form of an adult, it is of course very immature and numerous internal changes have yet to be undergone. Labial
mature and numerous internal changes have yet to be undergone. Labial
palps and gill filaments in the bivalves, adult kidneys, pericardium, the
palps and gill filaments in the bivalves, adult kidneys, pericardium, the
final relations of the mantle cavity, development of the gonads and
final relations of the mantle cavity, development of the gonads and
their ducts, all these and other minor processes of differentiation are
their ducts, all these and other minor processes of differentiation are
still to be undergone before the final condition is reached.
still to be undergone before the final condition is reached.
162 TYPES or INVERTEBRATE LARVAE
162 TYPES or INVERTEBRATE LARVAE


Line 6,063: Line 5,610:
   
   


Fm. 100. A, ventral View of gastrula stage of .l.staru.s flzwialflis. (Redrzmn {min Mac-
Fm. 100. A, ventral View of gastrula stage of .l.staru.s flzwialflis. (Redrzmn {min MacBride, after Reichenbach.) e. l., cephalic lobe; th. ab., thoracic abdominal thickening.
Bride, after Reichenbach.) e. l., cephalic lobe; th. ab., thoracic abdominal thickening.


B. nauplius stage of the same. an., anus; at‘, rudiment of first antenna; at‘~’, rudiment
B. nauplius stage of the same. an., anus; at‘, rudiment of first antenna; at‘~’, rudiment
of second antenna; car.. ridge making the first trace of the carapace; e.l., cephalic lobe;
of second antenna; car.. ridge making the first trace of the carapace; e.l., cephalic lobe;
lah.. lahrium; m.. mouth; mn., rudiment of mandible; pr. c., protocerebrum; th. ah.,
lah.. lahrium; m.. mouth; mn., rudiment of mandible; pr. c., protocerebrum; th. ah.,
Line 6,073: Line 5,619:
Crustacean eggs show a great range of developmental types, and the
Crustacean eggs show a great range of developmental types, and the
various stages show no uniformity throughout the different groups.
various stages show no uniformity throughout the different groups.
Cleavage may be superficial or it may be total and nearly equal. A cleav-
Cleavage may be superficial or it may be total and nearly equal. A cleavage cavity is usually lacking because of the large amount of yolk, but
age cavity is usually lacking because of the large amount of yolk, but
some species have it in more or less restricted condition. Gastrulation is
some species have it in more or less restricted condition. Gastrulation is
usually by epiboly and ingression, but here again conditions vary. Cross
usually by epiboly and ingression, but here again conditions vary. Cross
fertilization is usual, but there are cases of self—fertilization, and par-
fertilization is usual, but there are cases of self—fertilization, and parthenogenetic development may alternate with normal fertilization. There
thenogenetic development may alternate with normal fertilization. There
are some cases in which only parthenogenesis has so far been discovered.
are some cases in which only parthenogenesis has so far been discovered.
But in all cases a nauplius stage is at length reached.
But in all cases a nauplius stage is at length reached.


The form named nauplius by Muller actually had four pairs of appen-
The form named nauplius by Muller actually had four pairs of appendages, whereas the stage now known as the nauplius has only three
dages, whereas the stage now known as the nauplius has only three
NAUPLIUS LARVA
NAUPLIUS LARVA


Line 6,107: Line 5,650:
segmen tmg
segmen tmg


larva, therefore, has three pairs of appendages, first and second antennal,
larva, therefore, has three pairs of appendages, first and second antennal,


and mandlbular. But the degree of
and mandlbular. But the degree of
development toward independent ex-
development toward independent existence in the nauplius stage is by no
istence in the nauplius stage is by no
means uniform in the difieient Crustacea. There is in fact a series of larval
means uniform in the difieient Crus-
stages in the C1 ustacea, the most important of which are nauplius, metanauplius, protozoaca, zoaea, mysis, all
tacea. There is in fact a series of larval
stages in the C1 ustacea, the most im-
portant of which are nauplius, meta-
nauplius, protozoaca, zoaea, mysis, all
leading to the adult. There are, also,
leading to the adult. There are, also,
others less generally important, but
others less generally important, but
Line 6,124: Line 5,663:
only, in some forms of which all are
only, in some forms of which all are
represented. For every stage listed
represented. For every stage listed
there is some group of higher crusta-
there is some group of higher crustaceans in which the larva hatches from
ceans in which the larva hatches from
the egg at the corresponding time.
the egg at the corresponding time.
That is, hatching, or the breaking
That is, hatching, or the breaking
Line 6,132: Line 5,670:
   
   


FIG 111
fiG 111


Nnuphus of Cyclops (After
Nnuphus of Cyclops (After
Claus)
Claus)


an‘, first antenna; an’, second an-
an‘, first antenna; an’, second antenna. man , mandibular appendage.
tenna. man , mandibular appendage.
lab , labrmm, ex , exopodlte. en , endopodxte
lab , labrmm, ex , exopodlte. en , en-
dopodxte


egg membrane, is a variable process and some certain species may be
egg membrane, is a variable process and some certain species may be
Line 6,150: Line 5,686:
which the nauplius is a free-swimming larva, as in the barnacles. In the
which the nauplius is a free-swimming larva, as in the barnacles. In the


FIG. 112. Zones. of Penaeus, ventral view. (After Claus.)
fiG. 112. Zones. of Penaeus, ventral view. (After Claus.)


uni, first antenna; an“, second antenna; e., eye stalk; mn., mandible; mx‘, mx’. first and
uni, first antenna; an“, second antenna; e., eye stalk; mn., mandible; mx‘, mx’. first and
second maxilla; mxp*, mxp’, mxp3. first, second. and third muxillipeds; pl., beginning
second maxilla; mxp*, mxp’, mxp3. first, second. and third muxillipeds; pl., beginning
of pleopods; ur, uropod; e.f.. caudal fin.
of pleopods; ur, uropod; e.f.. caudal fin.


crayfish, for example, the nauplius condition is shown by three pairs of
crayfish, for example, the nauplius condition is shown by three pairs of
mere thickenings or buds instead of developed appendages and there are
mere thickenings or buds instead of developed appendages and there are
in the embryo in addition only two cephalic lobes, two thoracico-abdominal
in the embryo in addition only two cephalic lobes, two thoracico-abdominal
Line 6,166: Line 5,702:


segmentation, but with an enlarged labrum, openings of the alimentary
segmentation, but with an enlarged labrum, openings of the alimentary
tract, a single median eye, and the three pairs of appendages. The first
tract, a single median eye, and the three pairs of appendages. The first
antennal appendage shows no sign of a biramous character, but both the
antennal appendage shows no sign of a biramous character, but both the
second antennal and the mandibular have at least partially developed
second antennal and the mandibular have at least partially developed
Line 6,173: Line 5,709:
is preceded by one in which three primary segments are recognizable.
is preceded by one in which three primary segments are recognizable.
These become subdivided into eight lobes, which are the labrum, right
These become subdivided into eight lobes, which are the labrum, right
and left first antennal from the first primary segment, the right and left
and left first antennal from the first primary segment, the right and left
second antennal from the second segment, and the right and left man-
second antennal from the second segment, and the right and left mandibular and the telson from the third. Future growth takes place between the mandibular lobes and the telson. From this stage the next
dibular and the telson from the third. Future growth takes place be-
tween the mandibular lobes and the telson. From this stage the next
changes lead to the metanauplius.
changes lead to the metanauplius.


Line 6,184: Line 5,718:
Exopoditcs of the walking legs are to be noted (ex.).
Exopoditcs of the walking legs are to be noted (ex.).


The metanauplius condition is reached at the end of the first molt
The metanauplius condition is reached at the end of the first molt
in those forms which hatch as nauplii, but occurs before hatching in
in those forms which hatch as nauplii, but occurs before hatching in
such forms as Branchipus and Lucifer. Two additional pairs of appen-
such forms as Branchipus and Lucifer. Two additional pairs of appendages are present, the first and second maxillae, and segmentation is
dages are present, the first and second maxillae, and segmentation is
beginning.
beginning.


In the protozoaea, illustrated by a newly hatched Squzlla, the first
In the protozoaea, illustrated by a newly hatched Squzlla, the first
and second maxillipeds are present as well as the appendages of the
and second maxillipeds are present as well as the appendages of the
earlier types, the abdomen is partially segmented, but not the thorax,
earlier types, the abdomen is partially segmented, but not the thorax,
and the compound eyes are making their appearance.
and the compound eyes are making their appearance.


The zoaea, the stage in which the crab hatches, possesses third maxil-
The zoaea, the stage in which the crab hatches, possesses third maxillipeds, some of the thoracic appendages, the number varying with different forms, compound eyes, an abdomen completely segmented, but
lipeds, some of the thoracic appendages, the number varying with dif-
ferent forms, compound eyes, an abdomen completely segmented, but
the thorax showing as yet incomplete indications.
the thorax showing as yet incomplete indications.


Line 6,207: Line 5,738:
complete. The lobster also hatches in an advanced mysis stage.
complete. The lobster also hatches in an advanced mysis stage.


Finally in the fresh-water shrimp, Crangon, the condition of the adult
finally in the fresh-water shrimp, Crangon, the condition of the adult
is reached so far as external features are concerned at the time of
is reached so far as external features are concerned at the time of
hatching.
hatching.
Line 6,219: Line 5,750:
complex larvae and more or less complete metamorphosis, or may be
complex larvae and more or less complete metamorphosis, or may be
direct. The structure and cleavage of typical insect eggs have already
direct. The structure and cleavage of typical insect eggs have already
been described in the section on superficial cleavage. The cleavage of
been described in the section on superficial cleavage. The cleavage of
the centrolecithal egg results in the formation of a blastoderm which
the centrolecithal egg results in the formation of a blastoderm which
may be of uniform thickness in development or may have early shown
may be of uniform thickness in development or may have early shown
Line 6,233: Line 5,764:
example. From the material of this invaginating groove comes the inner
example. From the material of this invaginating groove comes the inner
layer from which is derived the mesoderm and endoderm. (2) In certain
layer from which is derived the mesoderm and endoderm. (2) In certain
other insects the formation of the mesoderm may be accomplished with-
other insects the formation of the mesoderm may be accomplished without the formation of a tube but rather from a middle plate which remains nearly flat and is overgrown at the edges by the lateral folds. It
out the formation of a tube but rather from a middle plate which re-
mains nearly flat and is overgrown at the edges by the lateral folds. It
occurs in certain Lepidoptera and other forms.
occurs in certain Lepidoptera and other forms.


(3) Still another type of mesoderm formation takes on the character
(3) Still another type of mesoderm formation takes on the character
of a proliferation and invagination of cells from a median ventral blasto-
of a proliferation and invagination of cells from a median ventral blastoderm region. This is characteristic of the Orthoptera. At the edges of
derm region. This is characteristic of the Orthoptera. At the edges of
the germ band the blastoderm begins a folding process and at length the
the germ band the blastoderm begins a folding process and at length the
two folds meet over the band in the middle region. Their union produces
two folds meet over the band in the middle region. Their union produces
Line 6,253: Line 5,781:


eyes, and antennae and mouth parts appear as rudiments in proper
eyes, and antennae and mouth parts appear as rudiments in proper
serial fashion. The appendages likewise are outpocketings of the ecto-
serial fashion. The appendages likewise are outpocketings of the ectodermal germ bands. It is evident of course that the variety of structures
dermal germ bands. It is evident of course that the variety of structures
found among the insects means great variability in details by which
found among the insects means great variability in details by which
these steps are accomplished. The general body form of the insect is
these steps are accomplished. The general body form of the insect is


I-fNfl\ (W v-'m~r>-'*a“">n n "We «now» -,0...
I-fNfl\ (W v-'m~r>-'*a“">n n "We «now» -,0...
d 5 £ ?
d 5 £ ?
,;a“’o°, «°" =6 ?~sm,§§§'**‘e *9 V7‘ 3"“
,;a“’o°, «°" =6 ?~sm,§§§'**‘e *9 V7‘ 3"“
Line 6,295: Line 5,822:
A, tmrisverse section, showing completed blastoderm Dorsal side of egg toward top
A, tmrisverse section, showing completed blastoderm Dorsal side of egg toward top
of page B, section of egg 9. little older than in A through anterior region Cells of veiitml
of page B, section of egg 9. little older than in A through anterior region Cells of veiitml
blastoderm are crowded, but dorsal blastoderm is thin and flattened eh . chorion, v pl
blastoderm are crowded, but dorsal blastoderm is thin and flattened eh . chorion, v pl
ventral plate.
ventral plate.


completed by the growth of the margins of the germ band dorsally
completed by the growth of the margins of the germ band dorsally
until they finally close over and form a dorsal wall. While this has been
until they finally close over and form a dorsal wall. While this has been
going on the progress and development of the internal structures has
going on the progress and development of the internal structures has
likewise been considerable and the embryo continues its development
likewise been considerable and the embryo continues its development
until finally ready to hatch into a larva.
until finally ready to hatch into a larva.


During the larval stage the insect feeds, sometimes voraciously, stor-
During the larval stage the insect feeds, sometimes voraciously, storing up nutritive material for its subsequent development. In the more
ing up nutritive material for its subsequent development. In the more
168 TYPES OF INVERTEBRATE LARVAE
168 TYPES OF INVERTEBRATE LARVAE


specialized insects this development is very complicated involving a com-
specialized insects this development is very complicated involving a complete metamorphosis with entire changes of form and often of function
plete metamorphosis with entire changes of form and often of function
as well. The groups of insects which undergo this indirect type of
as well. The groups of insects which undergo this indirect type of
development” or complete metamorphosis are spoken of as the Holo-
development” or complete metamorphosis are spoken of as the Holometabola and include the Coleoptera, Strepsiptera, Neuroptera, Mecoptera, Trichoptera, Lepidoptera, Diptera, Siphonaptera, and Hymenoptera. The less specialized groups comprise the Heterometabola in which
metabola and include the Coleoptera, Strepsiptera, Neuroptera, Mecop-
tera, Trichoptera, Lepidoptera, Diptera, Siphonaptera, and Hymenop-
tera. The less specialized groups comprise the Heterometabola in which


FIG. 115. (‘ontinuation of 114.
fiG. 115. (‘ontinuation of 114.


A, Transverse section of egg after closure of gastral invagination. mes., mesoderm; am.
A, Transverse section of egg after closure of gastral invagination. mes., mesoderm; am.
Line 6,344: Line 5,866:
   
   


F10. 116. Successive stages through the embryonic area. of Hydrophzlus. (From Kor-
F10. 116. Successive stages through the embryonic area. of Hydrophzlus. (From Korschelt and Hc-ider, after Helder)
schelt and Hc-ider, after Helder)


A, Formation of invaginnted groove wluch 15 to produce the under layer B, Origin ol
A, Formation of invaginnted groove wluch 15 to produce the under layer B, Origin ol
Line 6,359: Line 5,880:
Ametabola.
Ametabola.


Upon hatching, the larvae emerge with certain characteristics depend-
Upon hatching, the larvae emerge with certain characteristics depending upon the group to which they belong; one is usually able to classify
ing upon the group to which they belong; one is usually able to classify
the insect into its order by mere reference to the type of larva. Common
the insect into its order by mere reference to the type of larva. Common


Line 6,379: Line 5,899:
fundamentally of two groups, the campodeiform and the eruciform. The
fundamentally of two groups, the campodeiform and the eruciform. The
campodeiform are also spoken of as the thysanuriform in reference to
campodeiform are also spoken of as the thysanuriform in reference to
their generalized structure. They are flattened, have a long body, often
their generalized structure. They are flattened, have a long body, often
THE INSECTA 171
THE INSECTA 171


with long legs and antennae, hard body plates, caudal cerci with well-
with long legs and antennae, hard body plates, caudal cerci with welldeveloped mandibles and active habits. These are characteristics of the
developed mandibles and active habits. These are characteristics of the
adult thysanurans, especially of the genus Campodea, but in the insects
adult thysanurans, especially of the genus Campodea, but in the insects
which undergo metamorphosis they are of transitory importance only.
which undergo metamorphosis they are of transitory importance only.
Line 6,403: Line 5,922:
the larva which hatches from the egg is distinctly campodeiform and
the larva which hatches from the egg is distinctly campodeiform and
active but it enters the egg sac of a spider and becomes sedentary, loses
active but it enters the egg sac of a spider and becomes sedentary, loses
use of its legs and completely changes its form, that is, becomes an cruci-
use of its legs and completely changes its form, that is, becomes an cruciform larva. For the changes which occur during the growth of the larvae,
form larva. For the changes which occur during the growth of the larvae,
the frequency of the melts, and the great variety of adaptive structures
the frequency of the melts, and the great variety of adaptive structures
that are assumed in the various larvae of the insects, the reader must
that are assumed in the various larvae of the insects, the reader must
Line 6,412: Line 5,930:


The internal changes which accompany the metamorphosis of insects
The internal changes which accompany the metamorphosis of insects
are only incompletely understood. In those forms in which metamor-
are only incompletely understood. In those forms in which metamorphosis is incomplete certain organs are of larval significance only and
phosis is incomplete certain organs are of larval significance only and
their tissues must give way and provide the materials for other struc—
their tissues must give way and provide the materials for other struc—
tures characteristic of the imago. This destruction of larval tissue, or
tures characteristic of the imago. This destruction of larval tissue, or
Line 6,419: Line 5,936:
int.
int.


FIG. 119. Successive stages in the development of u. hrpmnaria of the asteroids. (After
fiG. 119. Successive stages in the development of u. hrpmnaria of the asteroids. (After
Leuckart.)
Leuckart.)


ad. c., adoral ciliated band, int., intestine. mo., mouth. oes . oesophagus; pr. 0. c., pre-
ad. c., adoral ciliated band, int., intestine. mo., mouth. oes . oesophagus; pr. 0. c., pre
 
oral ciliated band; pt. o.c., post-oral ciliated band.
oral ciliated band; pt. o.c., post-oral ciliated band.
histolysis, takes place commonly during the pupal period through the
histolysis, takes place commonly during the pupal period through the
activity of phagocytes and is followed by a period of the construction
activity of phagocytes and is followed by a period of the construction
of imaginal tissues or histogenesis. At the end of this constructive period
of imaginal tissues or histogenesis. At the end of this constructive period
the animal is ready for the final metamorphosis which converts it into
the animal is ready for the final metamorphosis which converts it into
an active adult or image.
an active adult or image.


Line 6,437: Line 5,953:
THE ECHINOIJERMATA 173
THE ECHINOIJERMATA 173


in this group metamorphosis has a peculiar and unusual significance.
in this group metamorphosis has a peculiar and unusual significance.
The larval stages are preparatory for the changes which are to adapt
The larval stages are preparatory for the changes which are to adapt
the adult forms to a great variety of living conditions, and they bridge
the adult forms to a great variety of living conditions, and they bridge
the gap from a rather simple ancestral form to the diverse conditions
the gap from a rather simple ancestral form to the diverse conditions
found among the five classes of living echinoderms. One has only to
found among the five classes of living echinoderms. One has only to
consider the different types of adults found among the asteroids, echi-
consider the different types of adults found among the asteroids, echinoids, ophiuroids, the holothurians and the crinoids to appreciate the
noids, ophiuroids, the holothurians and the crinoids to appreciate the
problem which confronts the simple type of ancestral larval form. Such
problem which confronts the simple type of ancestral larval form. Such
extensive metamorphoses as are found here have for their special func-
extensive metamorphoses as are found here have for their special function the adapting of the organism to the very changed conditions in
tion the adapting of the organism to the very changed conditions in
which it finds itself. Since the larval condition is retained to the last
which it finds itself. Since the larval condition is retained to the last
possible moment in development, although internal changes of the most
possible moment in development, although internal changes of the most


Line 6,456: Line 5,970:
Letters as in 118 and 119.
Letters as in 118 and 119.


profound character are taking place, metamorphosis is of a typo some-
profound character are taking place, metamorphosis is of a typo sometimes spoken of as cataelysmal.
times spoken of as cataelysmal.


The gastrula of all the echinoderms develops into a form similar to
The gastrula of all the echinoderms develops into a form similar to
what was probably the hypotheticalancestor of all the classes of the
what was probably the hypotheticalancestor of all the classes of the
group; it is known as a. dipleurula. From this dipleurula it is conceived
group; it is known as a. dipleurula. From this dipleurula it is conceived
that the echinopluteus of the sea-urchin, the ophiopluteus of the brittle-
that the echinopluteus of the sea-urchin, the ophiopluteus of the brittlestar, the bipinnaria of the starfish, and the auricularia of the holothurian
star, the bipinnaria of the starfish, and the auricularia of the holothurian
are derived. Of these four larval forms the first two are more closely
are derived. Of these four larval forms the first two are more closely
related to each other than to the other group, in which also affinities
related to each other than to the other group, in which also affinities
are discoverable to the larvae of the crinoids. It is not feasible to under-
are discoverable to the larvae of the crinoids. It is not feasible to undertake here a description of the development of the larvae and their
take here a description of the development of the larvae and their
metamorphoses in all these cases. For particular reasons and also because
metamorphoses in all these cases. For particular reasons and also because
it is the form most commonly studied, we choose to follow through the
it is the form most commonly studied, we choose to follow through the
development of the starfish larva, the bipinnaria, from its origin from
development of the starfish larva, the bipinnaria, from its origin from
the gastrula to its metamorphosis.
the gastrula to its metamorphosis.
174 TYPES OF INVERTEBRATE LARVAE
174 TYPES OF INVERTEBRATE LARVAE
Line 6,476: Line 5,987:
1. The Bipinnaria
1. The Bipinnaria


It is characteristic of echinoderm larvae that there should be a bilat-
It is characteristic of echinoderm larvae that there should be a bilateral symmetry. Two important trends are noticeable as the transition
eral symmetry. Two important trends are noticeable as the transition
from larva to’ adult takes place, namely the great development of the
from larva to’ adult takes place, namely the great development of the
left side of the larva with the corresponding decrease of the right side,
left side of the larva with the corresponding decrease of the right side,
and the complete change of symmetry to a radial type whose axis is at
and the complete change of symmetry to a radial type whose axis is at
right angles to the former larval axis. The egg of the starfish goes through
right angles to the former larval axis. The egg of the starfish goes through
a rapid and regular process of radial cleavage resulting in a blastula of
a rapid and regular process of radial cleavage resulting in a blastula of
about equal—sized cells. The cells become ciliated uniformly, the embryo
about equal—sized cells. The cells become ciliated uniformly, the embryo
Line 6,488: Line 5,998:
of mesenchyme is not completed until after the
of mesenchyme is not completed until after the
f ree—swimming stage is reached. The larva elongates,
f ree—swimming stage is reached. The larva elongates,
becomes somewhat flattened on the ventral side,
becomes somewhat flattened on the ventral side,
the blastopore is metamorphosed into the anus, and
the blastopore is metamorphosed into the anus, and
the larval mouth breaks through anteriorly. The
the larval mouth breaks through anteriorly. The
cilia disappear except for certain specialized ciliated
cilia disappear except for certain specialized ciliated
_ bands which take on a shape characteristic of par-
_ bands which take on a shape characteristic of particular species. Gradually there appear as outgrowths certain special processes which as they
ticular species. Gradually there appear as out-
growths certain special processes which as they
grow carry out the ciliated bands to their borders
grow carry out the ciliated bands to their borders


Line 6,503: Line 6,011:
“3“““-) The earlier investigators were inclined to the
“3“““-) The earlier investigators were inclined to the
al , alimentary - - _ ‘
al , alimentary - - _ ‘
mm mm” mouth; opinion that the starfish arose as a bud on the 1: ft
mm mm” mouth; opinion that the starfish arose as a bud on the 1: ft


pr o 0., pre—oral
pr o 0., pre—oral
Line 6,510: Line 6,018:
band.
band.


side of the larva. It is now realized that this appear-
side of the larva. It is now realized that this appearance is superficial only and that the larger part of
ance is superficial only and that the larger part of
the larval body is involved in the production of
the larval body is involved in the production of


the adult. The earliest trace of the adult body
the adult. The earliest trace of the adult body
appears as a five-lobed structure in the left posterior portion of the
appears as a five-lobed structure in the left posterior portion of the
larva. By the growth and dilferentiation of this structure and the loss
larva. By the growth and dilferentiation of this structure and the loss
of the larval mouth and oesophagus and the formation of the new
of the larval mouth and oesophagus and the formation of the new
opening, the metamorphosis into the little starfish is accomplished.
opening, the metamorphosis into the little starfish is accomplished.
In the case of the starfish a temporary fixed stage which is not found
In the case of the starfish a temporary fixed stage which is not found
in all types of echinoderm is passed through. During this stage
in all types of echinoderm is passed through. During this stage
certain other larval arms and processes are developed and the larva is
certain other larval arms and processes are developed and the larva is
spoken of as a brachiolaria.
spoken of as a brachiolaria.
It is now desirable to follow in more detail the changes which have
It is now desirable to follow in more detail the changes which have
been thus briefly sketched.
been thus briefly sketched.
THE DIPLEURULA 175
THE DIPLEURULA 175


Line 6,535: Line 6,042:
They possess a V—shaped adoral ciliated band; the alimentary canal
They possess a V—shaped adoral ciliated band; the alimentary canal


FIG 122 A, Bipinnai-1.1 of Astcmas (Frontal view) B, Side view of an older bipinnaria.
fiG 122 A, Bipinnai-1.1 of Astcmas (Frontal view) B, Side view of an older bipinnaria.
Median brarhioliirian process beginning to grow out at b (After Agassiz )
Median brarhioliirian process beginning to grow out at b (After Agassiz )


a , anus, a d a . anterior dorsal arm, ad e , adoral eiliated band, int , intestine. L eoel .
a , anus, a d a . anterior dorsal arm, ad e , adoral eiliated band, int , intestine. L eoel .
left coelome,m d a, median dorsal arm,mo , mouth, oes. oesophagus. pt d a . postero-
left coelome,m d a, median dorsal arm,mo , mouth, oes. oesophagus. pt d a . posterodorsiil arm, pt 1 a . postero-lateral arm, pt 0 a , post~oral arm, pt 0 e . post-oral band of
dorsiil arm, pt 1 a . postero-lateral arm, pt 0 a , post~oral arm, pt 0 e . post-oral band of
fllld, pr .1, pre—oral arm, pr 0 c. pre-oral band of cilia, r eoel , right coelomic sac, st,
fllld, pr .1, pre—oral arm, pr 0 c. pre-oral band of cilia, r eoel , right coelomic sac, st,
stomach
stomach


Line 6,555: Line 6,061:


the echinoderm existing today have been derived. This hypothetical
the echinoderm existing today have been derived. This hypothetical
ancestor is known as a dipleurula. To this larva the characteristic fea-
ancestor is known as a dipleurula. To this larva the characteristic features of the ophiuroids most faithfully conform, and of all echinoderm
tures of the ophiuroids most faithfully conform, and of all echinoderm
types it is the most nearly bilaterally symmetrical, for which reason,
types it is the most nearly bilaterally symmetrical, for which reason,
along with ‘others, it is probably to be regarded as the most primitive.
along with ‘others, it is probably to be regarded as the most primitive.
Line 6,565: Line 6,070:
coelome is divided into only two parts (unless the stone canal and its
coelome is divided into only two parts (unless the stone canal and its
connections are to be regarded as the homologues of the anterior coelome
connections are to be regarded as the homologues of the anterior coelome
of the dipleurula and the anterior coelome of the starfish is homologous
of the dipleurula and the anterior coelome of the starfish is homologous
to the middle portion of the dipleurulan structure). The middle part of
to the middle portion of the dipleurulan structure). The middle part of


Line 6,574: Line 6,079:
l.pt.coel.
l.pt.coel.


FIG. 123. Diagrammatie reconstruction of ancestral dipleurula.
fiG. 123. Diagrammatie reconstruction of ancestral dipleurula.


u.. anus; an. coel., anterior coelome; l. hyd.. left hydrocoelc; l.pt. coel., left posterior
u.. anus; an. coel., anterior coelome; l. hyd.. left hydrocoelc; l.pt. coel., left posterior
Line 6,604: Line 6,109:
3. Metamorphosis of Asterias
3. Metamorphosis of Asterias


By the end of the first day after hatching the free-swimining blastula
By the end of the first day after hatching the free-swimining blastula
has been converted into a gastrula which is distinguished from the usual
has been converted into a gastrula which is distinguished from the usual
type of invaginate gastrula in that the archenteron occupies only a small
type of invaginate gastrula in that the archenteron occupies only a small
portion of the inner space, leaving a large blastocoele still present. Into
portion of the inner space, leaving a large blastocoele still present. Into
this space are early budded mesenchymc cells which send out processes
this space are early budded mesenchymc cells which send out processes
and make a network in a gelatinous fluid
and make a network in a gelatinous fluid
filling the blastocoele. The gradual leiigthen-
filling the blastocoele. The gradual leiigthening of the gastrula to take on the form of a
ing of the gastrula to take on the form of a
cylinder with round ends, the differentiation
cylinder with round ends, the differentiation
of the ciliated apical plate and especially of
of the ciliated apical plate and especially of
Line 6,620: Line 6,124:
of the cilia elsewhere on the larval body, are
of the cilia elsewhere on the larval body, are
the next characteristic changes through which
the next characteristic changes through which
the young larva passes (Fig. 122). In the
the young larva passes (fig. 122). In the
meantime the coelomic sacs are budded off pm 124 Larva of Asmm
meantime the coelomic sacs are budded off pm 124 Larva of Asmm
from the apex of the arclienteron as in the *1‘ days Old. from dorsal surface
from the apex of the arclienteron as in the *1‘ days Old. from dorsal surface
case of dipleurula. The gut grows forward, (Alflgjeflgiwftu) I m.
case of dipleurula. The gut grows forward, (Alflgjeflgiwftu) I m.
becomes constricted into the intestine, (left), persicscoiiixiniidigpiiiiéiiiirg,
becomes constricted into the intestine, (left), persicscoiiixiniidigpiiiiéiiiirg,
stomach,and oesophagus, and the oesophagus ;f"‘v’~:‘1‘,l‘:l"t‘;1(;”’§:::,“‘ ' ii: 2 2 v
stomach,and oesophagus, and the oesophagus ;f"‘v’~:‘1‘,l‘:l"t‘;1(;”’§:::,“‘ ' ii: 2 2 v
Line 6,637: Line 6,141:
are borne by the preoral band two larval arms called the preoral and
are borne by the preoral band two larval arms called the preoral and
a median dorsal one, while in A. glaczalzs, A. rubens, and A. berylmus
a median dorsal one, while in A. glaczalzs, A. rubens, and A. berylmus
(Fig. 122), European species, there are also on this preoral band a
(fig. 122), European species, there are also on this preoral band a
median ventral arm and a. median dorsal one which are directed forward;
median ventral arm and a. median dorsal one which are directed forward;
there are also in both cases a pair of antero—dorsals, and a pair of
there are also in both cases a pair of antero—dorsals, and a pair of
Line 6,646: Line 6,150:
178 TYPES OF INVERTEBRATE LARVAE
178 TYPES OF INVERTEBRATE LARVAE


dorsals, and the larva is termed a brachiolaria. Into these arms ex-
dorsals, and the larva is termed a brachiolaria. Into these arms extensions of the coelome push out and in this particular they differ from
tensions of the coelome push out and in this particular they differ from
the arms of the bipinnaria. These arms as listed include all the lobe-like
the arms of the bipinnaria. These arms as listed include all the lobe-like
outgrowths which are found in other starfish larvae.
outgrowths which are found in other starfish larvae.
Line 6,654: Line 6,157:
coelome form the most important contribution to the starfish body.
coelome form the most important contribution to the starfish body.
After a period of slow enlargement near the oesophagus where they
After a period of slow enlargement near the oesophagus where they
originated, the coelomic sacs begin a remarkable series of transforma-
originated, the coelomic sacs begin a remarkable series of transformations. The right sac in some of the
tions. The right sac in some of the
larvae grows to form a canal leading
larvae grows to form a canal leading
to the outside through the right
to the outside through the right
Line 6,664: Line 6,166:
short vertical growth to the dorsal
short vertical growth to the dorsal
surface, forming the pore canal and
surface, forming the pore canal and
uniting with an eetodermal depres-
uniting with an eetodermal depression to form the primary madroporic
sion to form the primary madroporic
pore. Through the beating of its cilia
pore. Through the beating of its cilia
water is passed into the coelome.
water is passed into the coelome.
These structures of the left side are
These structures of the left side are
significant for the future of the
significant for the future of the
FM 135_ 1.~m,,m1V;Cw(,;u1;mchio1,.,;,. larvae, for it is the left side which
FM 135_ 1.~m,,m1V;Cw(,;u1;mchio1,.,;,. larvae, for it is the left side which


(3°m°“’h“t 3"“ AB*‘5Si”)- will develop to the greater part of
(3°m°“’h“t 3"“ AB*‘5Si”)- will develop to the greater part of
a., anus; a.d.a., anterior dorsal arm; the adult Starfish, While the right
a., anus; a.d.a., anterior dorsal arm; the adult Starfish, While the right


br.a., anterior median brachiolar arm; _ _ _
br.a., anterior median brachiolar arm; _ _ _
int., intestine;l.p.c.,left posterior coelome; contributes only a minimum. Never-
int., intestine;l.p.c.,left posterior coelome; contributes only a minimum. Never
 
pt.l.a., posterior lateral arm; pt.o.a., post- ‘
pt.l.a., posterior lateral arm; pt.o.a., post- ‘
oral arm; pr.o.a.. pre-oral arm; pt.d.a., thelebs’ anccstrally the larva‘ was
oral arm; pr.o.a.. pre-oral arm; pt.d.a., thelebs’ anccstrally the larva‘ was
Line 6,688: Line 6,188:
left sac just behind the madroporic pore divides it into the left anterior
left sac just behind the madroporic pore divides it into the left anterior
and posterior coelomes. The hinder part of the left anterior coelome
and posterior coelomes. The hinder part of the left anterior coelome
swells out to form a rather circular five-lobed outgrowth. This is the
swells out to form a rather circular five-lobed outgrowth. This is the
beginning of the water vascular system and is known as the hydrocoele.
beginning of the water vascular system and is known as the hydrocoele.
In some forms (Asterina) a right hydrocoele and the right anterior and
In some forms (Asterina) a right hydrocoele and the right anterior and
Line 6,695: Line 6,195:
anterior coelome. Its origin and position have been variously described,
anterior coelome. Its origin and position have been variously described,
but the best opinion now seems to derive it from the right coelome.
but the best opinion now seems to derive it from the right coelome.
These developments complete the structure of the free-swimming bi-
These developments complete the structure of the free-swimming biMETAMORPHOSIS OF ASTERI AS 179
METAMORPHOSIS OF ASTERI AS 179


pinnaria. It is now ready to settle down, become attached, grow into
pinnaria. It is now ready to settle down, become attached, grow into
the brachiolaria and begin the metamorphosis which will produce the
the brachiolaria and begin the metamorphosis which will produce the
adult starfish. Between the bases of the brachiolar arms a region of
adult starfish. Between the bases of the brachiolar arms a region of
fixation appears by means of which the larva becomes attached (Fig.
fixation appears by means of which the larva becomes attached (fig.
126B). It is a thickening of the ectoderm, which becomes glandular,
126B). It is a thickening of the ectoderm, which becomes glandular,
enabling it to fix the little animal to the substratum. The attachment
enabling it to fix the little animal to the substratum. The attachment
takes place near the anterior end of the larva and gives to that portion
takes place near the anterior end of the larva and gives to that portion


Line 6,721: Line 6,220:
    
    


Fm. 126. Lateral \ iews of bruoliiolnria ol'As(cr2as1uIgan~r in process of fixation. (Modified
Fm. 126. Lateral \ iews of bruoliiolnria ol'As(cr2as1uIgan~r in process of fixation. (Modified
from Goto.)
from Goto.)


A, Left side of earliest stage. temporary fixation bv the bruchioluriun arms; B, part
A, Left side of earliest stage. temporary fixation bv the bruchioluriun arms; B, part
of older brachiolaria corresponding to the base of A and showing the permanent fixation
of older brachiolaria corresponding to the base of A and showing the permanent fixation
by means of the fixing disc, the pre—oral lob'e liming shrunk. 1-5, lobes of hydrocoelc
by means of the fixing disc, the pre—oral lob'e liming shrunk. 1-5, lobes of hydrocoelc
growing out to corresponding enlargements of the body wall, I——V, the unlugen of the arms.
growing out to corresponding enlargements of the body wall, I——V, the unlugen of the arms.
Line 6,740: Line 6,239:


While the larva is becoming attached and constrictions which divide
While the larva is becoming attached and constrictions which divide
both right and left coelomes into anterior and posterior parts are becom-
both right and left coelomes into anterior and posterior parts are becom180 TYPES OF INVERTEBRATE LARVAE
180 TYPES OF INVERTEBRATE LARVAE


ing more evident, the left posterior sends a process over to the right side
ing more evident, the left posterior sends a process over to the right side
Line 6,749: Line 6,247:
anterior coelome. The right posterior coelome, however, is entirely c11t
anterior coelome. The right posterior coelome, however, is entirely c11t
off from the right anterior and forms the epigastric coelome of the adult.
off from the right anterior and forms the epigastric coelome of the adult.
During the time that the left anterior and posterior coelomes were di-
During the time that the left anterior and posterior coelomes were divided from each other by a septum formed by their opposed portions,
vided from each other by a septum formed by their opposed portions,
there appears a groove on the anterior side which is to form the stone
there appears a groove on the anterior side which is to form the stone
canal, while one on the posterior side is the first sign of the perioral
canal, while one on the posterior side is the first sign of the perioral
coelome. The stone canal becomes connected with the madroporic pore
coelome. The stone canal becomes connected with the madroporic pore
canal and runs down to the hydrocoele. The perioral coelome becomes a
canal and runs down to the hydrocoele. The perioral coelome becomes a
crescentic tube about a bud of the stomach which represents the adult
crescentic tube about a bud of the stomach which represents the adult
stomach. The further development of the alimentary tract is as follows:
stomach. The further development of the alimentary tract is as follows:
The stomodaeum gradually disappears, having first become discon-
The stomodaeum gradually disappears, having first become disconnected from the midgut. The oesophagus itself gradually shortens and
nected from the midgut. The oesophagus itself gradually shortens and
atrophies as does the intestine, the larval anus having closed. It is stated,
atrophies as does the intestine, the larval anus having closed. It is stated,
however, that a remnant of the intestine persists and from it the rectum
however, that a remnant of the intestine persists and from it the rectum
of the adult arises. From the left side of the larval stomach the bud
of the adult arises. From the left side of the larval stomach the bud
referred to above grows to form the cardiac stomach of the adult which
referred to above grows to form the cardiac stomach of the adult which
may be cverted for the purposes of food getting. As it grows it is sur-
may be cverted for the purposes of food getting. As it grows it is surrounded by the perioral coelome. At a point on the left side of the larva,
rounded by the perioral coelome. At a point on the left side of the larva,
which consequently is to be known as the oral side of the adult, the growing bud makes connections with the ectoderm and an opening appears
which consequently is to be known as the oral side of the adult, the grow-
ing bud makes connections with the ectoderm and an opening appears
forming the mouth. The rectum and adult anus do not appear until the
forming the mouth. The rectum and adult anus do not appear until the
body form of the young starfish is practically complete.
body form of the young starfish is practically complete.


Final Metamorphos1's. Since the left side of the larva becomes the oral
final Metamorphos1's. Since the left side of the larva becomes the oral
side the right side is the future aboral and the first signs of the body
side the right side is the future aboral and the first signs of the body
form are seen as five thickened lobe-like elevations of the ectoderm which
form are seen as five thickened lobe-like elevations of the ectoderm which
Line 6,776: Line 6,270:
disc. With the growth of the disc portion, the coelomes become displaced
disc. With the growth of the disc portion, the coelomes become displaced
backward in the larva to occupy what will be their position in the new
backward in the larva to occupy what will be their position in the new
body region. The hydrocoele becomes entirely separated from the ante-
body region. The hydrocoele becomes entirely separated from the anterior coelome. It sends out lobes which are the ru(Iiments of the radial
rior coelome. It sends out lobes which are the ru(Iiments of the radial
canals of the water vascular system and from which tube feet and outer
canals of the water vascular system and from which tube feet and outer
parts of the system are later formed. The stalk portion, becoming less
parts of the system are later formed. The stalk portion, becoming less
Line 6,783: Line 6,276:
of its cells and to phagocytic action on some of the others, is reduced
of its cells and to phagocytic action on some of the others, is reduced
until it is included in the disc area and is covered by the oral disc. Only
until it is included in the disc area and is covered by the oral disc. Only
a small projection from the oral disc holds the larva fast to the sub-
a small projection from the oral disc holds the larva fast to the substratum and at length it is broken as the little starfish completes its
stratum and at length it is broken as the little starfish completes its
body form and wrenches itself free. The further changes which the
body form and wrenches itself free. The further changes which the
ENTEROPNEUSTA l 81
ENTEROPNEUSTA l 81
Line 6,794: Line 6,286:
and its ielated genera present a great deal of variation. In the genus
and its ielated genera present a great deal of variation. In the genus


FIG 127 New England tornarm. from left side (After l\Iorgan )
fiG 127 New England tornarm. from left side (After l\Iorgan )


a . anus, a d l , axitenor dorsal loop of the longitudinal r-iliated bind up . apical plate;
a . anus, a d l , axitenor dorsal loop of the longitudinal r-iliated bind up . apical plate;
up m , apical muscle band, 011 long longitudinal minted band (-001 H first, second,
up m , apical muscle band, 011 long longitudinal minted band (-001 H first, second,
third. pairs of (oelomie ca\ mes g p, gill pouches mt , intestine o mouth oes , oeso-
third. pairs of (oelomie ca\ mes g p, gill pouches mt , intestine o mouth oes , oesophagus per , penoardml sac, pl 1 , posterior lateral ll‘!!! of the lomzitudm 11 mliatod band.
phagus per , penoardml sac, pl 1 , posterior lateral ll‘!!! of the lomzitudm 11 mliatod band.
prol, pre—oral loop of the longitudinal cihated bind, st, atom l(‘h ttr telotroch,
prol, pre—oral loop of the longitudinal cihated bind, st, atom l(‘h ttr telotroch,
wp , water—pore.
wp , water—pore.


Dolzchoglossus there is a large yolky egg which by a mueh—abridged
Dolzchoglossus there is a large yolky egg which by a mueh—abridged
series of stages reaches the adult without the intervention of any inde-
series of stages reaches the adult without the intervention of any independent larval form. In several of the species of Balanoglossus a type of
pendent larval form. In several of the species of Balanoglossus a type of
development which is probably more primitive is found, involving the
development which is probably more primitive is found, involving the
presence of a special larva known as the tornaria. Originally when this
presence of a special larva known as the tornaria. Originally when this
Line 6,813: Line 6,303:
C
C


FIG. 128. Metamorphosis of tornaria from Bahamas. (After Morgan.)
fiG. 128. Metamorphosis of tornaria from Bahamas. (After Morgan.)


A, just before metamorphosis; B, during metamorphosis; C, young balanoglossid worm
A, just before metamorphosis; B, during metamorphosis; C, young balanoglossid worm
Line 6,825: Line 6,315:


not all of the types of tornaria which have been described agree in all
not all of the types of tornaria which have been described agree in all
points, and several different methods for example of inesoderm forma-
points, and several different methods for example of inesoderm formation and development of the coelomic cavities have been recorded for
tion and development of the coelomic cavities have been recorded for
this larva. The work of Heider, although the most recent, is the only
this larva. The work of Heider, although the most recent, is the only
one which deals with the early stages. He was able to follow through
one which deals with the early stages. He was able to follow through
Line 6,832: Line 6,321:
could keep his specimens alive only eight days. Morgan’s account from
could keep his specimens alive only eight days. Morgan’s account from
species taken at Woods Hole begins about where Heider’s specimens
species taken at Woods Hole begins about where Heider’s specimens
died so a fairly complete history is available. The structure of the tor-
died so a fairly complete history is available. The structure of the tornaria larva superficially resembles that of the young bipinnaria and it
naria larva superficially resembles that of the young bipinnaria and it
is possible to apply the designations used on
is possible to apply the designations used on
the bipinnaria to the longitudinal ciliated
the bipinnaria to the longitudinal ciliated
Line 6,865: Line 6,353:
the coelome. In the latter the wall of the body cavity is formed by the
the coelome. In the latter the wall of the body cavity is formed by the
aggregation of scattered mesenchyme cells, a procedure which is rarely
aggregation of scattered mesenchyme cells, a procedure which is rarely
witnessed in the animal kingdom. At the time of the constriction divid-
witnessed in the animal kingdom. At the time of the constriction dividing the proboscis region from that posterior to it a dorsal strip of ectoderm
ing the proboscis region from that posterior to it a dorsal strip of ectoderm
remains unconstricted and becomes depressed beneath the surface in the
remains unconstricted and becomes depressed beneath the surface in the
form of a groove. This is the neural groove which is folded off and forms
form of a groove. This is the neural groove which is folded off and forms
Line 6,876: Line 6,363:
out to form the notochord. Gill pouches develop as several pairs of pockets
out to form the notochord. Gill pouches develop as several pairs of pockets
from the sides of the oesophagus. The further development of the larva
from the sides of the oesophagus. The further development of the larva
consists largely in the formation of the modifications of the coelome, the
consists largely in the formation of the modifications of the coelome, the
formation of the collar pores and of the genital organs. The metamor-
formation of the collar pores and of the genital organs. The metamorphosis is brought about by the development of a fold in the region
phosis is brought about by the development of a fold in the region
between the collar and trunk coelomes and the general growth "in length
between the collar and trunk coelomes and the general growth "in length
of the trunk portion of the animal. No such complications of develop-
of the trunk portion of the animal. No such complications of development and metamorphosis are found here as characterize the echino—
ment and metamorphosis are found here as characterize the echino—
derms, for the adult itself is of comparatively simple structure. Since
derms, for the adult itself is of comparatively simple structure. Since
the aim of this discussion is merely to show how the embryo is trans-
the aim of this discussion is merely to show how the embryo is transformed into a young worm similar to the adult, it seems unnecessary
formed into a young worm similar to the adult, it seems unnecessary
to follow through further the details of the development of this very
to follow through further the details of the development of this very
interesting animal.
interesting animal.
Line 6,893: Line 6,377:
are the following: Schultze, Minchin, Maas, Metchnikoff, Géttc, MacBride, Brooks,
are the following: Schultze, Minchin, Maas, Metchnikoff, Géttc, MacBride, Brooks,
Appelliif, Korschelt and Heider, Salensky, Lang, Surface, Woltereck, Balfour, Claus,
Appelliif, Korschelt and Heider, Salensky, Lang, Surface, Woltereck, Balfour, Claus,
Grave, Bury, Field, Batcson, Morgan, Ritter, I-leider on Balanoglossus. These works
Grave, Bury, field, Batcson, Morgan, Ritter, I-leider on Balanoglossus. These works
are cited in full in the bibliography on page 406.
are cited in full in the bibliography on page 406.


Line 6,902: Line 6,386:
applies to the vertebrate groups the most logical procedure at this stage (in which
applies to the vertebrate groups the most logical procedure at this stage (in which
we have considered various invertebrate larval forms) would be the detailed study
we have considered various invertebrate larval forms) would be the detailed study
of various vertebrate embryos. It would be proper to consider in detail the embry-
of various vertebrate embryos. It would be proper to consider in detail the embryology of amphioxus, the shark, a teleost fish, the frog, and the chick, as is so commonly
ology of amphioxus, the shark, a teleost fish, the frog, and the chick, as is so commonly
done in courses dealing with this subject, and of course there are other forms also
done in courses dealing with this subject, and of course there are other forms also
\vhich might be r-hosen.]
\vhich might be r-hosen.]


So much material is available upon these various forms that it has seemed Wiser
So much material is available upon these various forms that it has seemed Wiser
not to devote space to a discussion of the embryology of any of them. Most text-
not to devote space to a discussion of the embryology of any of them. Most textbooks of vertebrate embryology discuss at least some of these, and both brief and
books of vertebrate embryology discuss at least some of these, and both brief and
detailed expositions of the subject are easily available in English. Indeed the choice
detailed expositions of the subject are easily available in English. Indeed the choice
of forms difiers a great deal with instructors so that it would perhaps be necessary
of forms difiers a great deal with instructors so that it would perhaps be necessary
to include all of them to satisfy the selections that would be made in different insti-
to include all of them to satisfy the selections that would be made in different institutions. In our own case it is our practice to ask the student to obtain a copy of
tutions. In our own case it is our practice to ask the student to obtain a copy of
Patton's “Embryology of the (‘hick” and to study the chick intensively in the
Patton's “Embryology of the (‘hick” and to study the chick intensively in the
laboratory. Because of the good accounts which are so generally available and be-
laboratory. Because of the good accounts which are so generally available and because it is felt that nothing could be added in the present volume that is not easily
cause it is felt that nothing could be added in the present volume that is not easily
available in other accounts, it has been decided not to ofier any special discussion
available in other accounts, it has been decided not to ofier any special discussion
of the groups mentioned.
of the groups mentioned.


On the other hand, the mammals present many embryological variations from
On the other hand, the mammals present many embryological variations from
the other vertebrate groups, the understanding of which is by no means so easy to
the other vertebrate groups, the understanding of which is by no means so easy to
obtain as the preceding cases. In the discussions in the chapters on cleavage, gastru-
obtain as the preceding cases. In the discussions in the chapters on cleavage, gastrul.-ition, etc., it has often been said that the conditions throughout the animal kingdom are as stated except for the mammals. For these reasons it has seemed best to
l.-ition, etc., it has often been said that the conditions throughout the animal king-
dom are as stated except for the mammals. For these reasons it has seemed best to
include here an aiccount of the formation of the mammalian embryo and to leave
include here an aiccount of the formation of the mammalian embryo and to leave
other groups and the later history of the mammalian embryo for more detailed works.
other groups and the later history of the mammalian embryo for more detailed works.
Line 6,936: Line 6,414:
found in the reptiles more than they forecast conditions of the higher
found in the reptiles more than they forecast conditions of the higher


mammals. A detailed discussion of the monotreme seems to be un-
mammals. A detailed discussion of the monotreme seems to be unnecessary.
necessary.


I. MONOTREMES
I. MONOTREMES


The monotreme egg is the largest of all mammalian eggs since it con-
The monotreme egg is the largest of all mammalian eggs since it contains yolk varying in diameter from 2.5 to 4.0 mm. The accounts as
tains yolk varying in diameter from 2.5 to 4.0 mm. The accounts as


given for Echidna and Ornithorhynchus do not all agree in the exact size
given for Echidna and Ornithorhynchus do not all agree in the exact size
Line 6,951: Line 6,427:
within a follicle consisting of only one or two layers of cells and when
within a follicle consisting of only one or two layers of cells and when
it is passed to the outside receives a covering of albumen and a shell.
it is passed to the outside receives a covering of albumen and a shell.
In Ornithorhynchus the shell is said to be calcified. _
In Ornithorhynchus the shell is said to be calcified. _


Owing to the presence of a large amount of yolk, segmentation is
Owing to the presence of a large amount of yolk, segmentation is
discoidal, forming a blastoderm upon an unsegmented yolk mass. Semen
discoidal, forming a blastoderm upon an unsegmented yolk mass. Semen
failed to find yolk nuclei here as is the usual case in eggs with discoidal
failed to find yolk nuclei here as is the usual case in eggs with discoidal
cleavage. The first two furrows are meridional while the third is parallel
cleavage. The first two furrows are meridional while the third is parallel
to the first and at right angles to the second. A many-layered blaste-
to the first and at right angles to the second. A many-layered blastederm is formed having the shape of a biconvex lens, the deeper-arched
derm is formed having the shape of a biconvex lens, the deeper-arched
side of which is imbedded in the yolk.
side of which is imbedded in the yolk.


The chief departure of the monotreme egg from other discoidal eggs
The chief departure of the monotreme egg from other discoidal eggs
comes in the rapid closure of the blastopore which takes place rela-
comes in the rapid closure of the blastopore which takes place relatively early. The edges meet in a spot where yolk and upper and lower
tively early. The edges meet in a spot where yolk and upper and lower
cell layers are continuous with each other, a condition which has given
cell layers are continuous with each other, a condition which has given
rise to some misconceptions as to the homologues of these structures
rise to some misconceptions as to the homologues of these structures
with those of lower forms. The blastopore itself is the elongated primi-
with those of lower forms. The blastopore itself is the elongated primitive groove.
tive groove.


II. THE MARSUPIALS
II. THE MARSUPIALS


The embryology of marsupials has been the subject of study during
The embryology of marsupials has been the subject of study during
the last fifty years on the part of several investigators. The work of
the last fifty years on the part of several investigators. The work of


Caldwell and Selenka in 1887 represents the first attempt at a study of
Caldwell and Selenka in 1887 represents the first attempt at a study of
Line 6,984: Line 6,457:
but the two mentioned are the chief source of our information.
but the two mentioned are the chief source of our information.


The ovarian egg of Dasyurus, the largest mammalian egg known out-
The ovarian egg of Dasyurus, the largest mammalian egg known outside of the monotremes, measures 0.28 mm. according to Hill, while
side of the monotremes, measures 0.28 mm. according to Hill, while
that of the opossum varies from 0.14 to 0.16 mm. The egg of the former
that of the opossum varies from 0.14 to 0.16 mm. The egg of the former
is scantily supplied with albumen, whereas around the latter albumen islaid
is scantily supplied with albumen, whereas around the latter albumen islaid
Line 6,991: Line 6,463:
supplied with yolk compared to other mammalian eggs but a strange
supplied with yolk compared to other mammalian eggs but a strange
phenomenon occurs by which yolk is extruded from the cells themselves
phenomenon occurs by which yolk is extruded from the cells themselves
into the space surrounding the blastomeres. In Dasyurus (Fig. 130),
into the space surrounding the blastomeres. In Dasyurus (fig. 130),
according to Hill, extrusion takes place before cleavage begins in the
according to Hill, extrusion takes place before cleavage begins in the
form of a yolk body at the vegetative pole, but in Didelphys the yolk
form of a yolk body at the vegetative pole, but in Didelphys the yolk
THE MARSUPIALS 187
THE MARSUPIALS 187


is passed out during the first few cleavages and at no time forms a con-
is passed out during the first few cleavages and at no time forms a concentrated mass. It is thrown out from both ends or from all sides in
centrated mass. It is thrown out from both ends or from all sides in
greater or less amount during the early divisions. The greatest amount
greater or less amount during the early divisions. The greatest amount
seems to be given off between 2- and 4-cell stages and since the yolk is
seems to be given off between 2- and 4-cell stages and since the yolk is
distributed around the periphery of the egg no one point is the center
distributed around the periphery of the egg no one point is the center
of the extrusion. The orientation of the eggs likewise differs in these two
of the extrusion. The orientation of the eggs likewise differs in these two
genera. According to Hill the accumulation of the yolk marks the vege-
genera. According to Hill the accumulation of the yolk marks the vegetative pole. The first three cleavages of Dasyurus are meridional but
tative pole. The first three cleavages of Dasyurus are meridional but
the fourth is horizontal and divides the eight blastomeres into an upper
the fourth is horizontal and divides the eight blastomeres into an upper
ring of eight small lighter-staining cells and a lower ring of larger more
ring of eight small lighter-staining cells and a lower ring of larger more
Line 7,011: Line 6,481:
rise to the outer layers of the
rise to the outer layers of the
embryos which are spoken of as
embryos which are spoken of as
trophoblastic. The embryonic por-
trophoblastic. The embryonic portion is derived from the small cells
tion is derived from the small cells
of the 16—cell stage and therefore
of the 16—cell stage and therefore
from the vegetative half of the egg
from the vegetative half of the egg
Line 7,020: Line 6,489:
produce the trophoblastic portion.
produce the trophoblastic portion.
In Dzdelphys no such orientation
In Dzdelphys no such orientation
can be found. Here the first cleavage wF)‘?mg2 ( flfgvage Smges Bugle :0‘
can be found. Here the first cleavage wF)‘?mg2 ( flfgvage Smges Bugle :0‘
divides the egg into two blastomeres mrgtlnianus EAR;  D 1,8
divides the egg into two blastomeres mrgtlnianus EAR;  D 1,8
without any indication of polarity A. sectlon through 2-0811 stage. B.
without any indication of polarity A. sectlon through 2-0811 stage. B.
Line 7,036: Line 6,505:


From the 4-cell stage on, the cleavage of the opossum egg is irregular,
From the 4-cell stage on, the cleavage of the opossum egg is irregular,
it being possible to find stages of 6, 8, 10, 12, 15, cells and others. The
it being possible to find stages of 6, 8, 10, 12, 15, cells and others. The
space between the blastomeres represents a blastocyst cavity and even
space between the blastomeres represents a blastocyst cavity and even
in the early stages the blastomeres tend to migrate to the wall of the
in the early stages the blastomeres tend to migrate to the wall of the
“ovum” and arrange themselves in contact with it. Here they flatten
“ovum” and arrange themselves in contact with it. Here they flatten
and their outer surfaces take on the curvatures of the surrounding
and their outer surfaces take on the curvatures of the surrounding
albumen layer. Thus the yolk is left within the cavity formed by the
albumen layer. Thus the yolk is left within the cavity formed by the
Line 7,054: Line 6,523:
   
   


FIG. 131.
fiG. 131.


   
   
Line 7,061: Line 6,530:


A. 2-cell condition; B. 6-cell stage showing polarity and the fate of the two l’)lu.StUI1ll:I‘(“$
A. 2-cell condition; B. 6-cell stage showing polarity and the fate of the two l’)lu.StUI1ll:I‘(“$
of the preceding stage; C, 16-cell stage; D, a blastocyst of 40 to 50 cells in which no e\ i-
of the preceding stage; C, 16-cell stage; D, a blastocyst of 40 to 50 cells in which no e\ idence of polarity is seen. although it will shortly be reestablished with reappearance of
dence of polarity is seen. although it will shortly be reestablished with reappearance of


the endoderm.
the endoderm.


The blastocyst of Dasyurus is formed in a different manner. Here the
The blastocyst of Dasyurus is formed in a different manner. Here the
cells of each ring multiply rapidly but continue to occupy their hori-
cells of each ring multiply rapidly but continue to occupy their hori
 
   
   


Line 7,078: Line 6,545:
(After
(After


FIG. 132.
fiG. 132.
blastocyst of the opossum.
blastocyst of the opossum.
Hartman.)
Hartman.)
Line 7,087: Line 6,554:
showing six of the ten endoderm
showing six of the ten endoderm
mother cells; C. little later blastocyst
mother cells; C. little later blastocyst
showing differentiation of the embry-
showing differentiation of the embryonic area and trophoblastic ectoderm.
onic area and trophoblastic ectoderm.


zontal positions. Upon reaching the
zontal positions. Upon reaching the
periphery they too become applied to
periphery they too become applied to
the inner surface of the shell, the forma-
the inner surface of the shell, the formative cells at one pole and the non-formative at the other. This constitutes a
tive cells at one pole and the non-forma-
blastocyst of one layer of cells, a unilaminar blastocyst. Here too the yolk
tive at the other. This constitutes a
blastocyst of one layer of cells, a uni-
laminar blastocyst. Here too the yolk
remains within the cavity. Presently
remains within the cavity. Presently
the cells of the formative ectoderiii
the cells of the formative ectoderiii
Line 7,105: Line 6,568:
the surface and there unite to form a
the surface and there unite to form a
second layer, the endoderm. This layer
second layer, the endoderm. This layer
continues to proliferate and finally
continues to proliferate and finally
closes up to form a complete lining for
closes up to form a complete lining for
the entire blastocyst, the primitive
the entire blastocyst, the primitive
Line 7,114: Line 6,577:
among the mammals.
among the mammals.


Hartman also describes endoderm mother cells which detach them-
Hartman also describes endoderm mother cells which detach themselves from their place in the blastocyst wall and behave in the manner
selves from their place in the blastocyst wall and behave in the manner
THE MARSUPIALS 189
THE MARSUPIALS 189


closely resembling that described for Dasyurus. The important difference
closely resembling that described for Dasyurus. The important difference
here lies in the impossibility of distinguishing formative and non-
here lies in the impossibility of distinguishing formative and nonformative cells among the early blastomeres a11d of relating such cells
formative cells among the early blastomeres a11d of relating such cells
to the trophoblast and to the ectodcrm of the unilaminar blastocyst.
to the trophoblast and to the ectodcrm of the unilaminar blastocyst.


B
B


FIG. 133. Continuation of Fig. 125. A. B, showing progressive differentiation of the
fiG. 133. Continuation of fig. 125. A. B, showing progressive differentiation of the
endoderm and trophoblast.
endoderm and trophoblast.


Clearly there is no way by which the endoderm mother cells can be
Clearly there is no way by which the endoderm mother cells can be
traced back in the opossum to the early cleavage stages and, as Hart-
traced back in the opossum to the early cleavage stages and, as Hartman remarked, cleavage is entirely indeterminativc.
man remarked, cleavage is entirely indeterminativc.


While the cleaving ovum of Dasyurus shows a greater degree of deter-
While the cleaving ovum of Dasyurus shows a greater degree of determination and much more marked polarity than is the case in Didelphys,
mination and much more marked polarity than is the case in Didelphys,
190 FORMATION OF THE MAMMALIAN EMBRYO
190 FORMATION OF THE MAMMALIAN EMBRYO


Line 7,142: Line 6,601:
by the cells of the more rapidly dividing group and the trophoblast
by the cells of the more rapidly dividing group and the trophoblast
from those of the other. In discussing the formation of the embryo of
from those of the other. In discussing the formation of the embryo of
Eutheria it will appear that the “inner cell mass” of the latter is homol-
Eutheria it will appear that the “inner cell mass” of the latter is homologous with the embryonic area of the marsupials and the trophoblast of
ogous with the embryonic area of the marsupials and the trophoblast of
both groups show a complete homology, a view in which both Hartman
both groups show a complete homology, a view in which both Hartman
and Hill join. In the Eutheria, however, it is held that the trophoblast
and Hill join. In the Eutheria, however, it is held that the trophoblast
comes from one of the two blastomeres of the 2-cell stage and the inner
comes from one of the two blastomeres of the 2-cell stage and the inner
cell mass from the other. Clearly the fate of the two blastomeres is dif-
cell mass from the other. Clearly the fate of the two blastomeres is different in these two groups for in the marsupials one half of each blastomere goes into the production of the embryonic area and the other half
ferent in these two groups for in the marsupials one half of each blasto-
mere goes into the production of the embryonic area and the other half
into the trophoblast.
into the trophoblast.


Line 7,155: Line 6,611:


The embryonic area having become localized, a number of small cells
The embryonic area having become localized, a number of small cells
undergo modification and become the endodermal mother cells pre-
undergo modification and become the endodermal mother cells previously referred to. This process begins to take place in blastocysts
viously referred to. This process begins to take place in blastocysts
containing 50 to 60 cells. The cells increase in size, project into the
containing 50 to 60 cells. The cells increase in size, project into the
blastocyst cavity, and undergo other recognizable changes. Presently
blastocyst cavity, and undergo other recognizable changes. Presently
they free themselves from the wall of the blastocyst and by putting out
they free themselves from the wall of the blastocyst and by putting out
extended tips come in contact with each other so that a layer of endo-
extended tips come in contact with each other so that a layer of endoderm is formed. Sometimes several divisions take place on the part of
derm is formed. Sometimes several divisions take place on the part of
these cells before they have detached from the wall. The process of true
these cells before they have detached from the wall. The process of true
endoderm formation in the opossum and in Dasyurus as well is thus one
endoderm formation in the opossum and in Dasyurus as well is thus one
Line 7,174: Line 6,628:
size, in absence of polar differentiation in the unsegmented egg, in the
size, in absence of polar differentiation in the unsegmented egg, in the
crossed arrangement of blastomeres in the 4-cell stage, in indeterminate
crossed arrangement of blastomeres in the 4-cell stage, in indeterminate
cleavage, and in early proliferation of endoderm it approaches the con-
cleavage, and in early proliferation of endoderm it approaches the conditions of the Eutheria. But in the lack of a morula stage, of an inner
ditions of the Eutheria. But in the lack of a morula stage, of an inner
cell mass as such (although the embryonic area is homologous with it),
cell mass as such (although the embryonic area is homologous with it),
and in the method of endoderm formation it resembles Dasyurus. The
and in the method of endoderm formation it resembles Dasyurus. The
large size of the latter as compared to other mammals, and the locali-
large size of the latter as compared to other mammals, and the localization of the yolk mass in one portion of the egg (not far removed from
zation of the yolk mass in one portion of the egg (not far removed from
ENDODERM FORMATION 191
ENDODERM FORMATION 191


Line 7,187: Line 6,639:
The blastocyst of the opossum during its later stages undergoes some
The blastocyst of the opossum during its later stages undergoes some
important changes, most of which are concerned with its growth and
important changes, most of which are concerned with its growth and
enlargement. Its growth takes place by means of spreading and attenu-
enlargement. Its growth takes place by means of spreading and attenuation as well as by the more rapid multiplication of the trophoblastic
ation as well as by the more rapid multiplication of the trophoblastic


   
   
Line 7,196: Line 6,647:
Fm. 134. Later blastoeysts of the opossum. (After Hartman.)
Fm. 134. Later blastoeysts of the opossum. (After Hartman.)


A. just completed bilaminar blastoeyst. B, a later blastocyst nearly ready for the up-
A. just completed bilaminar blastoeyst. B, a later blastocyst nearly ready for the uppeurance of the mesoderm; C, D, sections showing details of the trophohlast and of the
peurance of the mesoderm; C, D, sections showing details of the trophohlast and of the
embryonic eetoderm respectively.
embryonic eetoderm respectively.


emb. ec-t., embryonic ectoderm; tr. ect., trophoblastic ectoderm; s.m., shell membrane; alb.,
emb. ec-t., embryonic ectoderm; tr. ect., trophoblastic ectoderm; s.m., shell membrane; alb.,
albumen.
albumen.
cells. Finally a maximum size of 1.0 to 1.5 min. is reached and the
cells. finally a maximum size of 1.0 to 1.5 min. is reached and the
trophoblastic region has come to occupy from four—fifths to five-sixths
trophoblastic region has come to occupy from four—fifths to five-sixths
of the entire surface of the blastocyst. That is, the increase in size con-
of the entire surface of the blastocyst. That is, the increase in size concerns the trophoblastic region mainly, the embryonic area growing very
cerns the trophoblastic region mainly, the embryonic area growing very


slowly if at all.
slowly if at all.
The cells of the embryonic area become much crowded and the endo-
The cells of the embryonic area become much crowded and the endo
 
derm attains a depth of three or four cells without taking on an epithelial character. The’ cells of necessity are irregular in size and shape.
derm attains a depth of three or four cells without taking on an epi-
thelial character. The’ cells of necessity are irregular in size and shape.
Then largely because of the migration of the endoderm cells they begin
Then largely because of the migration of the endoderm cells they begin
192 FORMATION OF THE MAMMALIAN EMBRYO
192 FORMATION OF THE MAMMALIAN EMBRYO
Line 7,217: Line 6,664:
to spread. While this migration is active on the part of the cells, no
to spread. While this migration is active on the part of the cells, no
amoeboid movement has been detected by Hartman. With this process
amoeboid movement has been detected by Hartman. With this process
the blastocyst becomes biconvex in form, the flattening occurring in the
the blastocyst becomes biconvex in form, the flattening occurring in the
direction of the egg axis with the formative area pressed against the
direction of the egg axis with the formative area pressed against the
shell membrane. The continuous growth of the trophoblastie area finally
shell membrane. The continuous growth of the trophoblastie area finally
brings it also in contact with the shell membrane, thus effecting for the
brings it also in contact with the shell membrane, thus effecting for the
blastocyst a. return to the spherical shape and completing the formation
blastocyst a. return to the spherical shape and completing the formation
Line 7,228: Line 6,675:
the point opposite its own place of origin, and thus a closed endodermal
the point opposite its own place of origin, and thus a closed endodermal
sac is formed within the ectoderm. During all this time the ectoderm
sac is formed within the ectoderm. During all this time the ectoderm
has remained as a single layer of quite flat cells. N ow, however, these
has remained as a single layer of quite flat cells. N ow, however, these
gradually thicken and become cuboidal. With this condition reached,
gradually thicken and become cuboidal. With this condition reached,
the formation of the blastocyst of the opossum is completed. From the
the formation of the blastocyst of the opossum is completed. From the
formative area, the embryo proper is developed in a manner quite com-
formative area, the embryo proper is developed in a manner quite comparable to that of the placental mammals; this phase of its embryology
parable to that of the placental mammals; this phase of its embryology
is not taken up here as a separate subject for discussion, since the formation of the embryo in the placental mammals is the subject matter of
is not taken up here as a separate subject for discussion, since the forma-
tion of the embryo in the placental mammals is the subject matter of
the next division of this chapter.
the next division of this chapter.


Line 7,245: Line 6,690:
of characteristics, the first of which is the size, for all are microscopic.
of characteristics, the first of which is the size, for all are microscopic.
They range from 0.07 mm. in the mouse to 0.145 mm. in the dog and
They range from 0.07 mm. in the mouse to 0.145 mm. in the dog and
0.13 to 0.14 mm. in man. (These figures are from Hartman’s calcula-
0.13 to 0.14 mm. in man. (These figures are from Hartman’s calculations.) Even at this small size, however, the eggs are large in comparison
tions.) Even at this small size, however, the eggs are large in comparison
to other cells of the body, for here as in other animals there is an accumulation of yolk within the egg. In the older works it was commonly said
to other cells of the body, for here as in other animals there is an accumu-
lation of yolk within the egg. In the older works it was commonly said
that the eggs of mammals are alecithal or yolkless. As already pointed
that the eggs of mammals are alecithal or yolkless. As already pointed
out in an earlier chapter this is untrue, for although it is small in amount
out in an earlier chapter this is untrue, for although it is small in amount
Line 7,263: Line 6,706:


The lack of yolk in the eggs of placental mammals is one of the two
The lack of yolk in the eggs of placental mammals is one of the two
major factors which are responsible for a very extensive modification
major factors which are responsible for a very extensive modification
found in the early embryology of these forms. Derived as they are from
found in the early embryology of these forms. Derived as they are from
forms that are highly laden with yolk with an extremely discoidal type
forms that are highly laden with yolk with an extremely discoidal type
of development, it is not to be expected that the reduction in yolk
of development, it is not to be expected that the reduction in yolk
would mean for the Placentalia a return to the simple methods of devel-
would mean for the Placentalia a return to the simple methods of development which are found in the holoblastic regularly cleaving forms, as
opment which are found in the holoblastic regularly cleaving forms, as
for example the echinoderms and amphioxus. The presence in all forms
for example the echinoderms and amphioxus. The presence in all forms
of Plaeentalia of a yolk sac, which is derived through the discoidal
of Plaeentalia of a yolk sac, which is derived through the discoidal
Line 7,276: Line 6,718:
eliminated during the first cleavages. Not even the elimination takes
eliminated during the first cleavages. Not even the elimination takes
place among the higher mammals for so little is present that it is easily
place among the higher mammals for so little is present that it is easily
used up during the early divisions. The lack of a yolk—filled hemisphere
used up during the early divisions. The lack of a yolk—filled hemisphere
in the uneleaved mammalian egg very obviously means a most striking
in the uneleaved mammalian egg very obviously means a most striking
modification of the type of development, for in the discoidal monotreme
modification of the type of development, for in the discoidal monotreme
only the animal half of the egg participates in the formation of the
only the animal half of the egg participates in the formation of the
embryo. The fate of the yolkless vegetative half in the formation of the
embryo. The fate of the yolkless vegetative half in the formation of the
trophoblastic portion of the egg has already been foretold in the forma-
trophoblastic portion of the egg has already been foretold in the formation of the blastodise of the marsupials.
tion of the blastodise of the marsupials.


The second major factor in bringing about the modifications which
The second major factor in bringing about the modifications which
are characteristic of higher mammals is also correlated with the yolkless
are characteristic of higher mammals is also correlated with the yolkless
condition. It is the (levelopment of an entirely different mechanism for
condition. It is the (levelopment of an entirely different mechanism for
supplying nourishment to the embryo and foetus before birth and takes
supplying nourishment to the embryo and foetus before birth and takes
the form of a placenta. The segmenting ovum becomes related to the
the form of a placenta. The segmenting ovum becomes related to the
uterine wall in a most intimate manner. This process is called placen-
uterine wall in a most intimate manner. This process is called placentation.
tation.


As a result of the factors mentioned the mammalian egg develops
As a result of the factors mentioned the mammalian egg develops
Line 7,320: Line 6,760:
J’
J’


FIG 135. Section thioiigli ow an of ('4 dog (l min Kellicott, iiftcr \\ aldeyer)
fiG 135. Section thioiigli ow an of ('4 dog (l min Kellicott, iiftcr \\ aldeyer)


0., ‘ Germinzil epithelium ', l) egg tubes c, suiiill ox anon follicles, d. older Uvflrldll fol-
0., ‘ Germinzil epithelium ', l) egg tubes c, suiiill ox anon follicles, d. older Uvflrldll follicles, c, ovum surrounded by discus proluzerus, f, semnd ovum in follicle with (- (Onlv
licles, c, ovum surrounded by discus proluzerus, f, semnd ovum in follicle with (- (Onlv
rarely are two ov.i thus found in in single follicle) 3:, outer capsule of the follicle, h, inner
rarely are two ov.i thus found in in single follicle) 3:, outer capsule of the follicle, h, inner
capsule of the follicle. i, nieinbmmi granulosa, k, collapsed, degenerating follicle, 1, blood
capsule of the follicle. i, nieinbmmi granulosa, k, collapsed, degenerating follicle, 1, blood
Line 7,330: Line 6,769:


cation period is past at the tiuie of birth. Many of these cells are utilized
cation period is past at the tiuie of birth. Many of these cells are utilized
only in the production of the follicle cells which surround each develop-
only in the production of the follicle cells which surround each developing ovum. They multiply, become columnar, and form a follicular epitheliuin. On one side only of the follicle a definite accumulation of cells
ing ovum. They multiply, become columnar, and form a follicular epi-
theliuin. On one side only of the follicle a definite accumulation of cells


* In 8. recent paper, Hargitt (Jour Morphology and Physiology, Vol 50, 1930)
* In 8. recent paper, Hargitt (Jour Morphology and Physiology, Vol 50, 1930)
l’m1l((‘\ the claim that in the ovanes of some mammals the production of germ cells
l’m1l((‘\ the claim that in the ovanes of some mammals the production of germ cells
ifi continuous
ifi continuous
DEVELOPMENT UP TO THE BLASTOCYST 195
DEVELOPMENT UP TO THE BLASTOCYST 195


Line 7,342: Line 6,779:
side a cavity is left by the separation of the cells of the follicle from
side a cavity is left by the separation of the cells of the follicle from
each other as the structure enlarges. This cavity becomes gradually
each other as the structure enlarges. This cavity becomes gradually
larger, and is filled with a liquid, the liquor folliculi.
larger, and is filled with a liquid, the liquor folliculi.


The fully grown follicle is known as a Graaflan follicle. The egg itself
The fully grown follicle is known as a Graaflan follicle. The egg itself
passes through its growth period in this follicle and becomes surrounded
passes through its growth period in this follicle and becomes surrounded
by definitely recognizable layers. The presence of the vitelline mem-
by definitely recognizable layers. The presence of the vitelline membrane, derived from the ovum, is a matter of dispute in various main
brane, derived from the ovum, is a matter of dispute in various main-
 
Fru. 136. Fully grown human ooeyte just removed from the ovary. (From Kellieott.
Fru. 136. Fully grown human ooeyte just removed from the ovary. (From Kellieott.
after Wuldeyer.)
after Wuldeyer.)
Line 7,362: Line 6,797:


The beginning of maturation occurs at the end of the growth period
The beginning of maturation occurs at the end of the growth period
when the egg is ready to escape from the ovary. The first polar body is
when the egg is ready to escape from the ovary. The first polar body is
given off before the ovum has eserred. In the mouse this process is
given off before the ovum has eserred. In the mouse this process is
said to take place one-half hour before ovulation. Then the Graafian
said to take place one-half hour before ovulation. Then the Graafian
196 FORMATION OF THE MAMMALIAN EMBRYO
196 FORMATION OF THE MAMMALIAN EMBRYO


follicle is ruptured, the ovum escapes into the periovarian space, and is
follicle is ruptured, the ovum escapes into the periovarian space, and is
carried into the fimbriated ostium of the oviduct which is in close prox-
carried into the fimbriated ostium of the oviduct which is in close proximity. The second polar spindle has already been formed and the second
imity. The second polar spindle has already been formed and the second
polar body is given off after fertilization in the upper part of the oviduct.
polar body is given off after fertilization in the upper part of the oviduct.
Related to ‘the process of ovulation are changes in the follicle, which is
Related to ‘the process of ovulation are changes in the follicle, which is
converted into a corpus luteum, as well as physiological changes of great
converted into a corpus luteum, as well as physiological changes of great
importance to the organism. However, the history of the embryo, which
importance to the organism. However, the history of the embryo, which
is the subject of this discussion, does not require the further considera-
is the subject of this discussion, does not require the further consideration of these changes connected with the ovary itself, although they are
tion of these changes connected with the ovary itself, although they are
of greatest physiological importance. The cleavage stages occur slowly
of greatest physiological importance. The cleavage stages occur slowly
as the egg passes down the oviduct. Twenty—four to forty-eight hours
as the egg passes down the oviduct. Twenty—four to forty-eight hours
elapse before the completion of the first and second cleavages in the
elapse before the completion of the first and second cleavages in the
mouse. In the rabbit fourteen or fifteen hours are occupied by the first
mouse. In the rabbit fourteen or fifteen hours are occupied by the first
cleavage and a correspondingly longer time elapses before the ovum
cleavage and a correspondingly longer time elapses before the ovum
reaches the uterus. Eighty hours are required in the mouse for this
reaches the uterus. Eighty hours are required in the mouse for this
passage through the oviduct, four days in the rabbit, eight to ten days
passage through the oviduct, four days in the rabbit, eight to ten days
in the dog and in certain ungulates it is said that the ovum remains
in the dog and in certain ungulates it is said that the ovum remains
over the winter in the oviduct. Cleavage is total and at first nearly
over the winter in the oviduct. Cleavage is total and at first nearly
equal, but rapidly becomes very irregular. Figures are available for
equal, but rapidly becomes very irregular. figures are available for
various animals showing cleavage stages consisting of almost any num-
various animals showing cleavage stages consisting of almost any number of cells up to sixteen or twenty. Evidently it is impossible to determine for these eggs the orientation, polarity, and such facts of promoi-—
ber of cells up to sixteen or twenty. Evidently it is impossible to deter-
mine for these eggs the orientation, polarity, and such facts of promoi-—
phology as have been shown to apply to eggs of lower forms. Cleavage
phology as have been shown to apply to eggs of lower forms. Cleavage
results in a mass of cells spoken of commonly as a morula. The cells
results in a mass of cells spoken of commonly as a morula. The cells
Line 7,409: Line 6,840:
the inner cell mass is derived from the other is based on evidence from
the inner cell mass is derived from the other is based on evidence from
some forms only and probably cannot be maintained with certainty for
some forms only and probably cannot be maintained with certainty for
all mammalian types owing to the difficulties in determining the orien-
all mammalian types owing to the difficulties in determining the orientation. The cavity of the blastodermic vesicle or blastocyst becomes filled
tation. The cavity of the blastodermic vesicle or blastocyst becomes filled
fiG. 137. Developing eggs of the rabbit. (After Van Beneden.)
FIG. 137. Developing eggs of the rabbit. (After Van Beneden.)
A, so-called metagastrula gtage preparatory to the formation of the blastocyst; B, beginning of znstrula cavity. the formation of the inner cell mass.
A, so-called metagastrula gtage preparatory to the formation of the blastocyst; B, be-
ginning of znstrula cavity. the formation of the inner cell mass.
198 FORMATION OF THE MAMMALIAN EMBRYO
198 FORMATION OF THE MAMMALIAN EMBRYO


with a fluid which is supposed by some to represent the yolk of lower
with a fluid which is supposed by some to represent the yolk of lower
forms. The subsequent history of the blastocyst varies in different groups.
forms. The subsequent history of the blastocyst varies in different groups.


There are three important stages in connection with the early history
There are three important stages in connection with the early history
of the formation of the embryo. The first is the growth of the blasto-
of the formation of the embryo. The first is the growth of the blastodermic vesicle during which it takes on the form typical of the particular
dermic vesicle during which it takes on the form typical of the particular
animal discussed. The second is the formation of the embryo body proper;
animal discussed. The second is the formation of the embryo body proper;
this stage involves the subsequent history of the surrounding layers of
this stage involves the subsequent history of the surrounding layers of
Line 7,430: Line 6,858:
The growth of the blastocyst takes place in a manner similar to that
The growth of the blastocyst takes place in a manner similar to that
described for the marsupial, the trophoblastic cells becoming extended
described for the marsupial, the trophoblastic cells becoming extended
and flattened and the cells increasing rapidly in number. Cell division
and flattened and the cells increasing rapidly in number. Cell division
at this stage takes place much more rapidly than in the earlier cleavage
at this stage takes place much more rapidly than in the earlier cleavage
stages, for in three days after the embryo has reached the uterus in the
stages, for in three days after the embryo has reached the uterus in the
Line 7,438: Line 6,866:
is spherical in the mouse, ovoid in the rabbit, and in the ungulates is
is spherical in the mouse, ovoid in the rabbit, and in the ungulates is
long and tapering, reaching a length of 20 cm. in the sheep of twelve
long and tapering, reaching a length of 20 cm. in the sheep of twelve
days although the diameter remains nearly constant, a couple of milli-
days although the diameter remains nearly constant, a couple of millimeters. This growth, as in the opossum, is limited to the trophoblast,
meters. This growth, as in the opossum, is limited to the trophoblast,
the inner cell mass remaining very small and restricted.
the inner cell mass remaining very small and restricted.


Up to the conclusion of the growth of the blastocyst no distinction
Up to the conclusion of the growth of the blastocyst no distinction
as to ectoderm and endoderm has been possible among its cells. Forma-
as to ectoderm and endoderm has been possible among its cells. Formation of the endoderm now begins as described for the opossum from the
tion of the endoderm now begins as described for the opossum from the
differentiation of those cells of the inner cell mass which border the
differentiation of those cells of the inner cell mass which border the
cavity of the blastocyst. Here these cells multiply rapidly and at the
cavity of the blastocyst. Here these cells multiply rapidly and at the
same time migrate so that they come to form a layer over the entire
same time migrate so that they come to form a layer over the entire
inner surface of the trophoblast which in this manner becomes two-
inner surface of the trophoblast which in this manner becomes twolayered and may be spoken of as a gastrula. Obviously this method of
layered and may be spoken of as a gastrula. Obviously this method of
endoderm formation is more closely related to that of eggs cleaving discoidally than to that of the holoblastic types. In some mammals, notably
endoderm formation is more closely related to that of eggs cleaving dis-
coidally than to that of the holoblastic types. In some mammals, notably
the primates, the endodermal layer remains much smaller than the
the primates, the endodermal layer remains much smaller than the
blastocyst itself, thus forming a double-layered vesicle whose outer layer
blastocyst itself, thus forming a double-layered vesicle whose outer layer
Line 7,471: Line 6,895:
of the embryonic knob which especially concerns us.
of the embryonic knob which especially concerns us.


FIG. 139. A. B, diagram showing the early formation of the blastocyst and the rela-
fiG. 139. A. B, diagram showing the early formation of the blastocyst and the relation of the ectoderm, endoderm, and trophoblast; C, diagram of the development of the
tion of the ectoderm, endoderm, and trophoblast; C, diagram of the development of the
insectivore Tupaija from Hubrecht's observations showing the development of the cavity
insectivore Tupaija from Hubrecht's observations showing the development of the cavity
of the ectoderm which opens out to form the embryonic shield: I), development of hedge-
of the ectoderm which opens out to form the embryonic shield: I), development of hedgehog type, also after Hubrecht‘s observations. (Modified from Keibel.)
hog type, also after Hubrecht‘s observations. (Modified from Keibel.)


At about the time when the embryonic knob is distinctly recognizable,
At about the time when the embryonic knob is distinctly recognizable,
Line 7,482: Line 6,904:
begins to form. Of implantation there are three types.
begins to form. Of implantation there are three types.


(a) Central, found in Carnivora and Ungulata, in some rodents in-
(a) Central, found in Carnivora and Ungulata, in some rodents including the rabbit in which it was first described and in the lower primates. In this type the blastodermic vesicle attaches directly to the
cluding the rabbit in which it was first described and in the lower pri-
mates. In this type the blastodermic vesicle attaches directly to the
uterine wall, projecting as it grows into the cavity of the uterus.
uterine wall, projecting as it grows into the cavity of the uterus.
THE BLASTOCYST 201
THE BLASTOCYST 201
Line 7,502: Line 6,922:


Fro. 140. Series of diagrams to show development with entypy of the germ. A, the
Fro. 140. Series of diagrams to show development with entypy of the germ. A, the
relations of the embryonic knob, the endoderm, and the trophoblast; B, later stage show-
relations of the embryonic knob, the endoderm, and the trophoblast; B, later stage showing the cells of the embryonic knob arranging themselves to form an embryonic shield
ing the cells of the embryonic knob arranging themselves to form an embryonic shield
with the amniotic cavity and Rauber’s layer above it; C‘, later stage in its development.
with the amniotic cavity and Rauber’s layer above it; C‘, later stage in its development.
I), Still later stage showing inversion of germ layers. (Modified from Hubrecht’s observa-
I), Still later stage showing inversion of germ layers. (Modified from Hubrecht’s observa
 
tions on the hedgehog.)
tions on the hedgehog.)


Line 7,513: Line 6,931:
becoming embedded therein is entirely covered over by the mucosa.
becoming embedded therein is entirely covered over by the mucosa.


The time relations of the development of early stages in the mam-
The time relations of the development of early stages in the mammals seems worthy of note, for a very much greater amount of time in
mals seems worthy of note, for a very much greater amount of time in
202 FORMATION OF THE MAMMALIAN EMBRYO
202 FORMATION OF THE MAMMALIAN EMBRYO


Line 7,520: Line 6,937:
stages in the mammals than is the case in tlie Sauropsida or in other
stages in the mammals than is the case in tlie Sauropsida or in other
lower forms. Even the cleavage stages take place much more slowly.
lower forms. Even the cleavage stages take place much more slowly.
It has been suggested that the delay in the development of the embry-
It has been suggested that the delay in the development of the embryonic shield (sce below) until after implantation has been accomplished
onic shield (sce below) until after implantation has been accomplished


FIG. 141. A, B, diagram showing the rapid enlargement of the extraembryonic coelome
fiG. 141. A, B, diagram showing the rapid enlargement of the extraembryonic coelome
and the cliorionic vesicle. (B, modified from Bailey and Miller.)
and the cliorionic vesicle. (B, modified from Bailey and Miller.)


is due to the very meager nutrition of the embryo during the period in
is due to the very meager nutrition of the embryo during the period in
which it is free in the uterus. This view is perhaps borne out by the
which it is free in the uterus. This view is perhaps borne out by the
sudden rapid development which takes place immediately after implan-
sudden rapid development which takes place immediately after implantation has been accomplished. Yet it is hard to understand why the
tation has been accomplished. Yet it is hard to understand why the
cleavages should be slowed down to such an extent as we find to be the
cleavages should be slowed down to such an extent as we find to be the
case if the factor of nutrition is the only one involved, for during the
case if the factor of nutrition is the only one involved, for during the
cleavage stages at least a small amount of yolk is always available.
cleavage stages at least a small amount of yolk is always available.
Line 7,538: Line 6,953:
and mesoderm has been formed. As the extraembryonic mesoderm grows,
and mesoderm has been formed. As the extraembryonic mesoderm grows,
it pushes in between the trophoblast and the yolk sac endodcrm and
it pushes in between the trophoblast and the yolk sac endodcrm and
the entire extraembryonic wall takes part in the formation of the so-
the entire extraembryonic wall takes part in the formation of the socalled chorion, the serosa. Sometimes the trophoblast is spoken of as
called chorion, the serosa. Sometimes the trophoblast is spoken of as
the chorionic ectoderm. The formation of the mesoderm in the mammal
the chorionic ectoderm. The formation of the mesoderm in the mammal
is a less conspicuous process than in some of the lower forms. It takes
is a less conspicuous process than in some of the lower forms. It takes
Line 7,545: Line 6,959:
from the ectoderm. In some forms it is stated that the mesoderm is
from the ectoderm. In some forms it is stated that the mesoderm is
related to the endoderm but certainly the usual derivation is from the
related to the endoderm but certainly the usual derivation is from the
embryonic ectoderm. It will be noted that this separation of the meso-
embryonic ectoderm. It will be noted that this separation of the mesodermal layer takes place before the formation of a primitive streak or
dermal layer takes place before the formation of a primitive streak or
any other elements of the body proper.
any other elements of the body proper.


Line 7,556: Line 6,969:
but also the amnion and the structures connected with it. It is necessary
but also the amnion and the structures connected with it. It is necessary
to consider the formation of the amnion before taking up the origin of
to consider the formation of the amnion before taking up the origin of
the embryonic shield. Mammals show two separate methods of the for-
the embryonic shield. Mammals show two separate methods of the formation of the amnion depending apparently upon the relations of the
mation of the amnion depending apparently upon the relations of the
trophoblast to the embryonic knob. In some forms the trophoblast comes
trophoblast to the embryonic knob. In some forms the trophoblast comes
to be interrupted over the embryonic knob which thereupon develops
to be interrupted over the embryonic knob which thereupon develops
in a manner that is entirely different from the cases in which the tropho-
in a manner that is entirely different from the cases in which the trophoblast is continuous. In the latter case the trophoblast cells are said to
blast is continuous. In the latter case the trophoblast cells are said to
constitute Rauber’s layer.
constitute Rauber’s layer.


The details of the formation of the amnion under these two conditions
The details of the formation of the amnion under these two conditions
vary in the different orders of the mammals and cannot be gone into
vary in the different orders of the mammals and cannot be gone into
here. The important features only can be pointed out. Taking up first
here. The important features only can be pointed out. Taking up first
the case in which the trophoblast is interrupted above the embryonic
the case in which the trophoblast is interrupted above the embryonic
knob, we find two different methods by which the amnion is established
knob, we find two different methods by which the amnion is established
although its subsequent history is quite alike in both cases. In the one
although its subsequent history is quite alike in both cases. In the one
which is illustrated by the inseetivore Tupaija studied by Hubrecht,
which is illustrated by the inseetivore Tupaija studied by Hubrecht,
Line 7,574: Line 6,985:
edges of this groove make contact with the trophoblast adjoining them
edges of this groove make contact with the trophoblast adjoining them
and later fold over to form the amnion itself. The bottom portion of the
and later fold over to form the amnion itself. The bottom portion of the
groove gradually flattens out and it is this area which becomes the em-
groove gradually flattens out and it is this area which becomes the embryonic shield and from which the body of the animal develops. In the
bryonic shield and from which the body of the animal develops. In the
other case as illustrated by the rabbit, the cells of the knob take on the
other case as illustrated by the rabbit, the cells of the knob take on the
form of a flat plate without the formation of a groove, but their edges
form of a flat plate without the formation of a groove, but their edges
are connected with the trophoblast and fold upward to form the amnion
are connected with the trophoblast and fold upward to form the amnion
204 FORMATION OF THE MAMMALIAN EMBRYO
204 FORMATION OF THE MAMMALIAN EMBRYO
Line 7,585: Line 6,995:
in those forms having typical discoidal cleavage such as the birds and
in those forms having typical discoidal cleavage such as the birds and
reptiles. The subsequent development of the embryonic shield in these
reptiles. The subsequent development of the embryonic shield in these
forms also recalls that of the sauropsidan blastoderm. (Figs. 139 and
forms also recalls that of the sauropsidan blastoderm. (figs. 139 and
140.)
140.)


Flu. l42.—Sections through four stages in the early development of the insectivorc
flu. l42.—Sections through four stages in the early development of the insectivorc
Tupaua javanica. (From Kellicott, after Hubrecht.)
Tupaua javanica. (From Kellicott, after Hubrecht.)


A, blastodermic vesicle completely closed. endoderm still continuous with the embry-
A, blastodermic vesicle completely closed. endoderm still continuous with the embryonic ectodcrm. B, C, embryonic ectoderm split and folding out upon the surface of the
onic ectodcrm. B, C, embryonic ectoderm split and folding out upon the surface of the
vesicle. pushing away the trophohlnst cells: D, embryonic cctoderm forming a flat disc
vesicle. pushing away the trophohlnst cells: D, embryonic cctoderm forming a flat disc
on the surface of the blastodcrmic vesicle.
on the surface of the blastodcrmic vesicle.


Line 7,599: Line 7,008:
trophoblast.
trophoblast.


The second method of formation of the amnion differs in many par-
The second method of formation of the amnion differs in many particulars from the first. The trophoblastic layer entirely covers the embryonic knob, a condition which is known to mammalian embryologists
ticulars from the first. The trophoblastic layer entirely covers the em-
bryonic knob, a condition which is known to mammalian embryologists
as entypy of the germ, and because of it the so-called inversion of the
as entypy of the germ, and because of it the so-called inversion of the
germ layers is brought about. It will be recalled that the embryonic
germ layers is brought about. It will be recalled that the embryonic
Line 7,625: Line 7,032:
   
   


FIG. 143. Sections through the blastodermic vesicle and blastocyst of the albino rat.
fiG. 143. Sections through the blastodermic vesicle and blastocyst of the albino rat.


(After Huber)
(After Huber)
Line 7,640: Line 7,047:
hand becomes the embryonic shield. The inner layer of the shield is
hand becomes the embryonic shield. The inner layer of the shield is
thus ectodermal while the layer which for a time is actually the outer
thus ectodermal while the layer which for a time is actually the outer
is endodermal. (Fig. 143.)
is endodermal. (fig. 143.)


In some cases, of which the guinea pig and the mouse are examples,
In some cases, of which the guinea pig and the mouse are examples,
the embryonic knob moves gradually to a position well down inside
the embryonic knob moves gradually to a position well down inside
the blastocyst. This process carries with it the lengthening of the endo-
the blastocyst. This process carries with it the lengthening of the endodermal layer on the outside. Earlier students of these forms removed
dermal layer on the outside. Earlier students of these forms removed
the outer layers of the blastocyst and came upon the embryonic knob
the outer layers of the blastocyst and came upon the embryonic knob
which they properly regarded as the formative area. Because of the
which they properly regarded as the formative area. Because of the
Line 7,652: Line 7,058:
layer to be of endoderm. Hence they spoke of the inversion of the germ
layer to be of endoderm. Hence they spoke of the inversion of the germ
layers in these forms and the phrase is still retained in the literature of
layers in these forms and the phrase is still retained in the literature of
mammalian embryology, although of course it has no real significance
mammalian embryology, although of course it has no real significance
as will be seen from the future development of the body form.
as will be seen from the future development of the body form.


Line 7,661: Line 7,067:
to accompanies the embryonic knob in its growth into the cavity of the
to accompanies the embryonic knob in its growth into the cavity of the
vesicle. Within this trophoblastic knob a second cavity may occur called
vesicle. Within this trophoblastic knob a second cavity may occur called
the false amniotic cavity. It has no relation to the true amnion, a com-
the false amniotic cavity. It has no relation to the true amnion, a completely closed vesicle, and presently disappears without further significance. In certain cases other spaces also develop as in the case of the
pletely closed vesicle, and presently disappears without further signifi-
cance. In certain cases other spaces also develop as in the case of the
interamniotic cavity between the cavities of the true and false amnions
interamniotic cavity between the cavities of the true and false amnions
in the guinea pig. The false cavity may reach a relatively large size in
in the guinea pig. The false cavity may reach a relatively large size in
Line 7,684: Line 7,088:
in its developmental processes to the blastoderm of the chick or other
in its developmental processes to the blastoderm of the chick or other
discoidal type. Its development has been studied in a great variety of
discoidal type. Its development has been studied in a great variety of
mammals including the bat, dog, mouse, rabbit, guinea pig, mole, hedge-
mammals including the bat, dog, mouse, rabbit, guinea pig, mole, hedgehog, pig, and of course man.
hog, pig, and of course man.


As one looks down upon the shield after the trophoblast has been
As one looks down upon the shield after the trophoblast has been
removed from above, the similarity to the chick is so striking that a
removed from above, the similarity to the chick is so striking that a
very brief description will be sufficient to make clear the main point in
very brief description will be sufficient to make clear the main point in
development. It consists of a layer of embryonic ectoderm three or four
development. It consists of a layer of embryonic ectoderm three or four


   
   


FIG. 144. Surface view of the embryonic shield of a dog. 13 to 15 days. (After Kellicott.)
fiG. 144. Surface view of the embryonic shield of a dog. 13 to 15 days. (After Kellicott.)
sh., embryonal shield; k.n., Henson's node; p.s., primitive streak.
sh., embryonal shield; k.n., Henson's node; p.s., primitive streak.


cells thick under which is a single-celled layer of endoderm. This stage
cells thick under which is a single-celled layer of endoderm. This stage
is reached during the seventh day in the rabbit and about the fourteenth
is reached during the seventh day in the rabbit and about the fourteenth
in the dog. Then there occurs in the middle region of the disc a thicken-
in the dog. Then there occurs in the middle region of the disc a thickening and condensation of the cell layers to form Hens0n’s node or the
ing and condensation of the cell layers to form Hens0n’s node or the
primitive knot, and extending backward from this is a rather broad
primitive knot, and extending backward from this is a rather broad
line which disappears in the thicker cells of the posterior margin of the
line which disappears in the thicker cells of the posterior margin of the
shield. Henson’s node and this broad line are of course recognizable as
shield. Henson’s node and this broad line are of course recognizable as
the primitive streak, and shortly extending along its middle the primi-
the primitive streak, and shortly extending along its middle the primitive groove is to be discerned. In front of the node the mesoderm can
tive groove is to be discerned. In front of the node the mesoderm can
be easily made out in sections appearing as a sheet between the ectoderm and the endoderm. This sheet early separates and, as has already
be easily made out in sections appearing as a sheet between the ecto-
derm and the endoderm. This sheet early separates and, as has already
been stated, its extension into the extraembryonic area participates
been stated, its extension into the extraembryonic area participates
in the formation of the serosa. It is supposed that the mesoderm takes
in the formation of the serosa. It is supposed that the mesoderm takes
Line 7,717: Line 7,117:
for the Sauropsida. This is to be expected from the relations of the yolk
for the Sauropsida. This is to be expected from the relations of the yolk
sac, as already remarked, and shows that the conditions found in the
sac, as already remarked, and shows that the conditions found in the
mammals represent a modification of the type of development where a
mammals represent a modification of the type of development where a
large mass of yolk is present. The development of the body cavity,
large mass of yolk is present. The development of the body cavity,
embryonic and cxtraembryonic, of the splanchnic and somatic layers of
embryonic and cxtraembryonic, of the splanchnic and somatic layers of
the mesoderm, appearance of the head fold, and the other characteristic
the mesoderm, appearance of the head fold, and the other characteristic
features of the sauropsidan type of development have their counter-
features of the sauropsidan type of development have their counterparts here, and as it is not the purpose of this chapter to discuss mammalian embryology after the body form has been established, it seems
parts here, and as it is not the purpose of this chapter to discuss mam-
malian embryology after the body form has been established, it seems
unnecessary to go into these matters. For a discussion of them the
unnecessary to go into these matters. For a discussion of them the


Line 7,752: Line 7,150:
as insect eggs, have more and thicker egg membranes.
as insect eggs, have more and thicker egg membranes.


Egg membranes are classified with reference to their origin. Primary
Egg membranes are classified with reference to their origin. Primary
egg membranes are formed by the egg itself, secondary by the follicle
egg membranes are formed by the egg itself, secondary by the follicle
cells around the egg, and tertiary by the uterus or oviduct. All three
cells around the egg, and tertiary by the uterus or oviduct. All three
Line 7,775: Line 7,173:
which underlies it but which is physically different from it. The presence
which underlies it but which is physically different from it. The presence
of the layer has been demonstrated by micro-dissection experiments
of the layer has been demonstrated by micro-dissection experiments
(Chambers and others) which show that the surface of the egg is firm
(Chambers and others) which show that the surface of the egg is firm
and somewhat elastic, offering resistance to mechanical injury. Plas-
and somewhat elastic, offering resistance to mechanical injury. Plas
 
molysis experiments have shown that this layer is a semi-permeable membrane and that it plays an important role in regulating the exchange
molysis experiments have shown that this layer is a semi-permeable membrane and that it plays an important role in regulating the exchange
which takes place between the cell and its surroundings.
which takes place between the cell and its surroundings.


In the animal kingdom as a whole there is an astonishing variability
In the animal kingdom as a whole there is an astonishing variability
in the manner in which egg coverings appear. In sponges, the develop-
in the manner in which egg coverings appear. In sponges, the development of the egg within the adult body makes membranes unnecessary.
ment of the egg within the adult body makes membranes unnecessary.
They are lacking also in Hydrozoa, Siphonophora, and Anthozoa, although some coelenterates do have them. In some of the lamellibranchs,
They are lacking also in Hydrozoa, Siphonophora, and Anthozoa, al-
though some coelenterates do have them. In some of the lamellibranchs,
as Drezssensza, no membranes are present, and the eggs of some others,
as Drezssensza, no membranes are present, and the eggs of some others,
as M ytilus, have them in the beginning of their development and later
as M ytilus, have them in the beginning of their development and later
Line 7,791: Line 7,186:
   
   


FIG 145 Cross section of egg of Hydra arzsea (Redmwn from Korsehelt and Heidor,
fiG 145 Cross section of egg of Hydra arzsea (Redmwn from Korsehelt and Heidor,
after Ehrenberg and Brauer )
after Ehrenberg and Brauer )


Line 7,805: Line 7,200:
Vitellme Membrane. In many and perhaps in all eggs, there is a
Vitellme Membrane. In many and perhaps in all eggs, there is a
vitelline or fertilization membrane. This membrane is the most constant
vitelline or fertilization membrane. This membrane is the most constant
of the primary membranes, though it is often difficult to see before
of the primary membranes, though it is often difficult to see before
fertilization. Early workers had thought that the fertilization membrane
fertilization. Early workers had thought that the fertilization membrane
was formed at the moment of fertilization, for, in many eggs, as for
was formed at the moment of fertilization, for, in many eggs, as for
Line 7,827: Line 7,222:
between the egg and its fertilization
between the egg and its fertilization
membrane is the perivitelline space.
membrane is the perivitelline space.
(See Fig. 7 ) Its size varies considerably
(See fig. 7 ) Its size varies considerably
in different species.
in different species.


In some eggs the vitelline membrane
In some eggs the vitelline membrane
is apparently lacking and the egg is
is apparently lacking and the egg is
covered directly by a chorion or secon-
covered directly by a chorion or secondary membrane as in the cephalopods.
dary membrane as in the cephalopods.
In many eggs it is present before the
In many eggs it is present before the
sperm touches the egg, though the
sperm touches the egg, though the
Line 7,855: Line 7,249:
the egg is shed into the water, another
the egg is shed into the water, another
membrane, the perivitelline, is formed
membrane, the perivitelline, is formed
inside the first, a space intervening Fie 146 Successive stages in the
inside the first, a space intervening fie 146 Successive stages in the


between the two. ‘But immediately c,l,,e.:/ne,l?f:,l,'::":,,°fC31:‘:la:““(:'}:r"'§‘$$.‘f
between the two. ‘But immediately c,l,,e.:/ne,l?f:,l,'::":,,°fC31:‘:la:““(:'}:r"'§‘$$.‘f
Line 7,862: Line 7,256:
212 EGG AND EMBRYONIC MEMBRANES
212 EGG AND EMBRYONIC MEMBRANES


inner membrane hardens and the two fuse. Thus is formed the fertiliza-
inner membrane hardens and the two fuse. Thus is formed the fertilization membrane which is separated from the egg by the perivitelline space.
tion membrane which is separated from the egg by the perivitelline space.


The vitelline membrane is usually structureless, transparent, and
The vitelline membrane is usually structureless, transparent, and
Line 7,878: Line 7,271:


The true vitelline membrane is a part of the egg itself, but it proves
The true vitelline membrane is a part of the egg itself, but it proves
difficult in some eggs to determine whether the membrane which has
difficult in some eggs to determine whether the membrane which has
been designated the vitelline is really primary or secondary. Confusion
been designated the vitelline is really primary or secondary. Confusion
also seems to exist regarding the origin of the zona radiata, the mem-
also seems to exist regarding the origin of the zona radiata, the membrane which lies next to the vitelline membrane. In some eggs, as in
brane which lies next to the vitelline membrane. In some eggs, as in
selachians and in Petromyzon, the zona radiata lies inside it, and in
selachians and in Petromyzon, the zona radiata lies inside it, and in
others, as in the teleosts, the zona radiata lies outside it. This membrane
others, as in the teleosts, the zona radiata lies outside it. This membrane
derives its name from the radiations which are seen in cross section and
derives its name from the radiations which are seen in cross section and
which in the vertebrates at least are due to fine canals.
which in the vertebrates at least are due to fine canals.


To classify properly the vitelline membrane and zona radiata of a
To classify properly the vitelline membrane and zona radiata of a
Line 7,913: Line 7,305:
layer through the vitelline membrane.” The zona radiata of Nereis
layer through the vitelline membrane.” The zona radiata of Nereis
thus secretes the jelly which surrounds the egg. The structures which
thus secretes the jelly which surrounds the egg. The structures which
seem to be radiations are the collapsed walls of the alveoli. The so-
seem to be radiations are the collapsed walls of the alveoli. The socalled zona radiata of Nereis is thus not homologous to the membrane
called zona radiata of Nereis is thus not homologous to the membrane
of that name in other forms.
of that name in other forms.


The zona radiata has a wide distribution among vertebrate eggs
The zona radiata has a wide distribution among vertebrate eggs
and is found in all classes. It is in many cases doubtful whether this
and is found in all classes. It is in many cases doubtful whether this
layer is formed from the outer part of the egg or from the follicle epi-
layer is formed from the outer part of the egg or from the follicle epithelium. In cases where there are two or more egg coverings it probably
thelium. In cases where there are two or more egg coverings it probably
arises from the egg itself. When the zona radiata
arises from the egg itself. When the zona radiata
arises later than the egg membrane outside it, it
arises later than the egg membrane outside it, it
Line 7,926: Line 7,316:
shown for Fundulus.
shown for Fundulus.


The purpose of the zona radiata in many verte-
The purpose of the zona radiata in many vertebrates is clear. Through the delicate canals of this
brates is clear. Through the delicate canals of this
layer, protoplasmic processes of the follicle cells _
layer, protoplasmic processes of the follicle cells _
penetrate. Nutrient substances from these cells are 5-f-
penetrate. Nutrient substances from these cells are 5-f
 
        
        


Line 7,947: Line 7,335:
is here a true primary membrane, being formed
is here a true primary membrane, being formed
before the follicle cells themselves. The zona in this
before the follicle cells themselves. The zona in this
form is a provisional egg covering for the develop-
form is a provisional egg covering for the development of the egg in the ovary. When the egg development is complete, it becomes a thin membrane.
ment of the egg in the ovary. When the egg de-
velopment is complete, it becomes a thin membrane.


Contrasted with the provisional zona radiata of
Contrasted with the provisional zona radiata of
Line 7,957: Line 7,343:
surface layer of the egg
surface layer of the egg
of Scyllmm cam'cula.
of Scyllmm cam'cula.
(Redrawn from Kor-
(Redrawn from Korschelt and Hcider, after
schelt and Hcider, after
Balfour.)
Balfour.)


f.e., follicular epi-
f.e., follicular epithelium; s.f., secondary
thelium; s.f., secondary
follicular epithelium;
follicular epithelium;
v.m., vitelline mem-
v.m., vitelline membrane; y., yolk; z.r., zona
brane; y., yolk; z.r., zona
radiata.
radiata.


of cyclostomes, teleosts, and ganoids. In these fishes the zona radiata
of cyclostomes, teleosts, and ganoids. In these fishes the zona radiata
is often divided into two layers or at least there are two radially
is often divided into two layers or at least there are two radially
striped layers which have the same origin. In some of the fishes as
striped layers which have the same origin. In some of the fishes as
Perca there is a. gelatinous layer outside of it through which run cell
Perca there is a. gelatinous layer outside of it through which run cell
processes that connect it with the follicle cells. This and other similar
processes that connect it with the follicle cells. This and other similar
Line 7,977: Line 7,360:
in Fundulus they are derived from the egg itself.
in Fundulus they are derived from the egg itself.


Although the origin of the zona radiata from the egg has been de-
Although the origin of the zona radiata from the egg has been determined for the selachians and for Fundulus, more work must be done
termined for the selachians and for Fundulus, more work must be done
214 EGG AND EMBRYONIC MEMBRANES
214 EGG AND EMBRYONIC MEMBRANES


to ascertain what part the follicle cells may have in the formation of
to ascertain what part the follicle cells may have in the formation of
this layer in other fishes.
this layer in other fishes.


In the bony fishes, since the egg membrane, which is often sticky, is
In the bony fishes, since the egg membrane, which is often sticky, is
present before fertilization, the micropyle must be formed in a different
present before fertilization, the micropyle must be formed in a different
manner from‘ that mentioned above for many of the invertebrates.
manner from‘ that mentioned above for many of the invertebrates.
Line 8,003: Line 7,385:
   
   


FIG 148 Section through the fol- _ _ _
fiG 148 Section through the fol- _ _ _
hole and outer layers of the egg of vzmdzs. In this form the early follicle 1S
hole and outer layers of the egg of vzmdzs. In this form the early follicle 1S


fi:'l§:rfi)“”“”l” (‘Um K°“’°h°” and one—layered. In it cells of two sizes may
fi:'l§:rfi)“”“”l” (‘Um K°“’°h°” and one—layered. In it cells of two sizes may


fc’ follicular eI,,the1,um, L gala. be distinguished, large cells, the centers
fc’ follicular eI,,the1,um, L gala. be distinguished, large cells, the centers
tmous layer. ov. ovarml epithelium: of which are filled with round nuclei,
tmous layer. ov. ovarml epithelium: of which are filled with round nuclei,
§f,‘,,‘,;,,‘§{°°“‘°“‘°“"" ' ’°"" ' ' ' ‘°““ and smaller cells with oval nuclei. The
§f,‘,,‘,;,,‘§{°°“‘°“‘°“"" ' ’°"" ' ' ' ‘°““ and smaller cells with oval nuclei. The
egg itself has a delicate surface layer,
egg itself has a delicate surface layer,
Line 8,017: Line 7,399:
shaped and send processes to the egg. Some of the cells remain round
shaped and send processes to the egg. Some of the cells remain round
and lodge between the stalks of the pear-shaped cells. The small cells
and lodge between the stalks of the pear-shaped cells. The small cells
take up a more distal position, and mean-
take up a more distal position, and meanwhile the processes of the larger ones become branched to penetrate the plasma
while the processes of the larger ones be-
come branched to penetrate the plasma
of the egg. The follicle now thickens and
of the egg. The follicle now thickens and
the zona takes on its characteristic radiate
the zona takes on its characteristic radiate
structure. Finally the follicle cells dimin-
structure. finally the follicle cells diminish in size and the follicle itself is thinner. , fiG 149 Mwropyle formation
ish in size and the follicle itself is thinner. , FIG 149 Mwropyle formation
The nuclei of the large cells lose much of  mus “mamas
The nuclei of the large cells lose much of  mus “mamas
their chromatin as the cells are stretched fc , follicular epithelium, t r ,
their chromatin as the cells are stretched fc , follicular epithelium, t r ,
Line 8,034: Line 7,413:
radiata. It is seldom that the ormation of the membrane is as clear as
radiata. It is seldom that the ormation of the membrane is as clear as


in this form. (Fig. 150.)
in this form. (fig. 150.)
!'-?«"?3"-:'o'-
!'-?«"?3"-:'o'
 
fiG. 150. The origin of the egg membranes of Lacerta viridis. (Redmwn from Buchner.
FIG. 150. The origin of the egg membranes of Lacerta viridis. (Redmwn from Buchner.
pfter Retzius.) For description, see text.
pfter Retzius.) For description, see text.
216 EGG AND EMBRYONIC MEMBRANES
216 EGG AND EMBRYONIC MEMBRANES
Line 8,045: Line 7,423:
the granulosa. The zona radiata is later
the granulosa. The zona radiata is later
formed between the ovum and the follicle
formed between the ovum and the follicle
cells and there has been considerable dis-
cells and there has been considerable discussion as to its origin. Bartelmez thinks
cussion as to its origin. Bartelmez thinks
that it is formed from the follicle cells; at
that it is formed from the follicle cells; at
any rate it has a function similar to that
any rate it has a function similar to that
Line 8,068: Line 7,445:
over the egg as in other animals is a structureless membrane usually
over the egg as in other animals is a structureless membrane usually
considered as from the egg itself, though some workers have thought
considered as from the egg itself, though some workers have thought
it to be a product of the follicle cells. It is very diflicult to differentiate
it to be a product of the follicle cells. It is very diflicult to differentiate
the vitelline membrane from the zona radiata and the former may be
the vitelline membrane from the zona radiata and the former may be
in part the anlage of the latter, as in the case of Lacerta which we have
in part the anlage of the latter, as in the case of Lacerta which we have
Line 8,094: Line 7,471:
In unlrun mam rune
In unlrun mam rune


FIG 153 An ovarian follicle approaching maturity (From Patten )
fiG 153 An ovarian follicle approaching maturity (From Patten )


this layer is secreted by the follicle cells, as some workers believe, it is
this layer is secreted by the follicle cells, as some workers believe, it is
Line 8,108: Line 7,485:


Secondary membranes are formed by the follicle cells which surround
Secondary membranes are formed by the follicle cells which surround
the ovum and are therefore the product of maternal tissue. These mem-
the ovum and are therefore the product of maternal tissue. These membranes, which are truly chorionic in nature, may take on a variety of
branes, which are truly chorionic in nature, may take on a variety of
218 EGG AND EMBRYONIC MEMBRANES
218 EGG AND EMBRYONIC MEMBRANES


Line 8,119: Line 7,495:
as in the insect egg. On the other
as in the insect egg. On the other
hand, it may be formed by direct
hand, it may be formed by direct
transformation of the follicle cells them-
transformation of the follicle cells themselves. Its substance is, according to
selves. Its substance is, according to
Tichomirow, chemically like keratin
Tichomirow, chemically like keratin


Line 8,130: Line 7,505:
ms bwolor (Redrawn from Korschelt chitin,
ms bwolor (Redrawn from Korschelt chitin,


and Heme’) Both primary and secondary mem-
and Heme’) Both primary and secondary mem
 
branes are often present before fertilization takes place, and since they
branes are often present before fertilization takes place, and since they
are usually impenetrable to the sperm they are perforated by one or
are usually impenetrable to the sperm they are perforated by one or
Line 8,137: Line 7,511:
nemerteans and in most molluscs the micropyle is near the lower pole,
nemerteans and in most molluscs the micropyle is near the lower pole,
but in cephalopods and also in echinoderms, insects,
but in cephalopods and also in echinoderms, insects,
and fishes, it is near the upper pole. In the Orthoptera
and fishes, it is near the upper pole. In the Orthoptera
it may be either at the lower pole or at the side of the
it may be either at the lower pole or at the side of the
egg, and in Oedzpoda there is a circle of 30 to 40 micro-
egg, and in Oedzpoda there is a circle of 30 to 40 micropyles at the lower pole.
pyles at the lower pole.


The chorion of insect eggs is very different in different
The chorion of insect eggs is very different in different
Line 8,152: Line 7,525:


Porous canals through which the egg obtains air often .. _
Porous canals through which the egg obtains air often .. _
penetrate the chorion. In Ranatra and N epa, water FIG 155 An
penetrate the chorion. In Ranatra and N epa, water fiG 155 An
scorpions, in which the eggs are sunken into plant iii  
scorpions, in which the eggs are sunken into plant iii  
stalks, the chorion is drawn out at the end of the seven processes
stalks, the chorion is drawn out at the end of the seven processes
Line 8,166: Line 7,539:
process remains during the secretion of the chorion and then is drawn
process remains during the secretion of the chorion and then is drawn
back into the follicle. The chorionic pores referred to are formed in
back into the follicle. The chorionic pores referred to are formed in
the same way. Also the micropyle of the bony fishes is formed in a
the same way. Also the micropyle of the bony fishes is formed in a
SECONDARY MEMBRANES 219
SECONDARY MEMBRANES 219


similar manner, but as has been earlier mentioned, the membrane per-
similar manner, but as has been earlier mentioned, the membrane perforated in this case is a zona radiata and not a chorion. (See fig. 191.)
forated in this case is a zona radiata and not a chorion. (See Fig. 191.)


In Octopus the chorion is drawn out into a stalk which becomes
In Octopus the chorion is drawn out into a stalk which becomes
Line 8,185: Line 7,557:


The myxinoids have a characteristic shell. At each pole of the egg are
The myxinoids have a characteristic shell. At each pole of the egg are
attached stiff anchoring filaments which end in lobed umbrella-like
attached stiff anchoring filaments which end in lobed umbrella-like
expansions. At the germinal pole of the egg the shell is marked by a
expansions. At the germinal pole of the egg the shell is marked by a
furrow-like ring so that a lid is formed which the animal pushes off at
furrow-like ring so that a lid is formed which the animal pushes off at
Line 8,192: Line 7,564:
   
   


FIG. 157. The upper part of the egg of Bdellostama stouti. (Rcdrawn from Ziegler, after
fiG. 157. The upper part of the egg of Bdellostama stouti. (Rcdrawn from Ziegler, after
Doflein.)
Doflein.)


A, section showing nucleus and above it the micropyle between the bases of the proc-
A, section showing nucleus and above it the micropyle between the bases of the processes. B. Opereulum and processes.
esses. B. Opereulum and processes.


origin of this shell. Cunningham says that it is the product of the egg
origin of this shell. Cunningham says that it is the product of the egg
itself, and Doflein derives it from the follicle cells. The membrane is
itself, and Doflein derives it from the follicle cells. The membrane is
usually considered as a true chorion.
usually considered as a true chorion.


Line 8,211: Line 7,582:
the vitelline membrane.
the vitelline membrane.


The follicle cells of the ascidians show a special type of modification.
The follicle cells of the ascidians show a special type of modification.
Five envelopes are formed by these cells and thus we have a unique
five envelopes are formed by these cells and thus we have a unique
example of an egg covered by five secondary membranes. When the
example of an egg covered by five secondary membranes. When the
ascidian egg is still young it is surrounded by a primary follicular epi-
ascidian egg is still young it is surrounded by a primary follicular epithelium derived from undifferentiated ovarian cells. Beneath this epithelium is a band of structureless membrane. These flat epithelial cells
thelium derived from undifferentiated ovarian cells. Beneath this epi-
thelium is a band of structureless membrane. These flat epithelial cells
multiply and become cubical. Some of them find their way inside the
multiply and become cubical. Some of them find their way inside the
epithelium and form an inner layer called the test—cell layer while cer-
epithelium and form an inner layer called the test—cell layer while certain of them wander into the egg. The cells of this layer do not give
tain of them wander into the egg. The cells of this layer do not give
rise to the test of the adult ascidian as was formerly supposed to be the
rise to the test of the adult ascidian as was formerly supposed to be the
case. As the egg matures, these test cells degenerate and later are found
case. As the egg matures, these test cells degenerate and later are found
Line 8,227: Line 7,595:
character. These cells, instead of remaining cubical, increase in size and
character. These cells, instead of remaining cubical, increase in size and
become highly vacuolated, resembling a foam structure. They also
become highly vacuolated, resembling a foam structure. They also
develop processes which support the egg and enable it to float.
develop processes which support the egg and enable it to float.


In addition to the follicular membrane and the test-cell layer, two
In addition to the follicular membrane and the test-cell layer, two
Line 8,233: Line 7,601:
two layers already described, the follicle cells secrete a structureless
two layers already described, the follicle cells secrete a structureless
membrane called the chorion. Still another membrane is formed between
membrane called the chorion. Still another membrane is formed between
the basement membrane and the follicle cells. This is the external pave-
the basement membrane and the follicle cells. This is the external pavement epithelium and it may be regarded as another layer of follicle cells.
ment epithelium and it may be regarded as another layer of follicle cells.
There are thus five membranes over the ripe ascidian egg. Next the egg
There are thus five membranes over the ripe ascidian egg. Next the egg
is the gelatinous layer of test cells, and over this are the following
is the gelatinous layer of test cells, and over this are the following
layers, the chorion, the foam-like follicle epithelium, the external pave-
layers, the chorion, the foam-like follicle epithelium, the external pavement epithelium, and the basal, follicle membrane. Since all these membranes are derived from the follicle cells they are secondary membranes.
ment epithelium, and the basal, follicle membrane. Since all these mem-
branes are derived from the follicle cells they are secondary membranes.


In the Dipnoi the primary membranes are covered by the gelatinous
In the Dipnoi the primary membranes are covered by the gelatinous
Line 8,261: Line 7,626:
cells. As described in an earlier chapter, the mammalian ovum is highly
cells. As described in an earlier chapter, the mammalian ovum is highly
specialized because of the intra-uterine development of the embryo.
specialized because of the intra-uterine development of the embryo.
There is only a very small amount of yolk present in the egg as con-
There is only a very small amount of yolk present in the egg as contrasted with the large amount in the eggs of birds and reptiles. Secondary
trasted with the large amount in the eggs of birds and reptiles. Secondary
and tertiary membranes are entirely lacking, but the Graafian follicle
and tertiary membranes are entirely lacking, but the Graafian follicle


Fm 158 The developing ovum and follicle cells of the cat (Redrawn from Buchner)
Fm 158 The developing ovum and follicle cells of the cat (Redrawn from Buchner)
See text for description.
See text for description.


which surrounds the egg is a product of the follicle cells. (Fig. 153.) In
which surrounds the egg is a product of the follicle cells. (fig. 153.) In
earlier times mammals had eggs similar to those of reptiles and birds, for
earlier times mammals had eggs similar to those of reptiles and birds, for
the monotremes, the simplest mammals, possess an egg with shell and
the monotremes, the simplest mammals, possess an egg with shell and
egg albumen. In the entire animal kingdom the Graafian follicle is prob-
egg albumen. In the entire animal kingdom the Graafian follicle is probably the most specialized structure produced as a modification of the follicle cells. In the middle of the follicle is a cavity filled with liquid, known
ably the most specialized structure produced as a modification of the fol-
licle cells. In the middle of the follicle is a cavity filled with liquid, known
as the liquor folliculi. The ovum itself, surrounded by the zona pellucida
as the liquor folliculi. The ovum itself, surrounded by the zona pellucida
and the zona radiata, is attached to the Wall of the Graafian follicle by
and the zona radiata, is attached to the Wall of the Graafian follicle by
a group of cells known as the discus proligerus. The cells of the discus
a group of cells known as the discus proligerus. The cells of the discus
222 EGG AND EMBRYONIC MEMBRANES
222 EGG AND EMBRYONIC MEMBRANES
Line 8,281: Line 7,643:
are continued into the cells of the follicle wall known as the membrana
are continued into the cells of the follicle wall known as the membrana
granulosa, which consists of many layers. Outside the membrana
granulosa, which consists of many layers. Outside the membrana
granulosa the ovarian connective tissue is differentiated into two in-
granulosa the ovarian connective tissue is differentiated into two investing layers, the theca folliculi. The outer of these is densely fibrous,
vesting layers, the theca folliculi. The outer of these is densely fibrous,
and the inner cellular, penetrated by small blood vessels. Buehner
and the inner cellular, penetrated by small blood vessels. Buehner
describes the growth of the Graafian follicle in the cat (Fig. 158), where
describes the growth of the Graafian follicle in the cat (fig. 158), where
it begins as a simple follicle in which the ovum is surrounded by a
it begins as a simple follicle in which the ovum is surrounded by a
cellular layer, the granulosa. The cells about the ovum multiply rapidly,
cellular layer, the granulosa. The cells about the ovum multiply rapidly,
Line 8,293: Line 7,654:
while a cavity known as the antrum
while a cavity known as the antrum
appears between them. This cavity
appears between them. This cavity
becomes filled with a liquid which
becomes filled with a liquid which
is secreted into it and quickly en-
is secreted into it and quickly enlarges. The outer ring of follicle
larges. The outer ring of follicle
cells is crowded to the periphery
cells is crowded to the periphery
and forms the stratum granulosum.
and forms the stratum granulosum.
The ovum itself at first bulges
The ovum itself at first bulges
slightly into the cavity of the
slightly into the cavity of the
follicle, and later as its surround-
follicle, and later as its surrounding cells are undercut protrudes
ing cells are undercut protrudes
farther into it, its attachment to
farther into it, its attachment to
the follicle being new a delicate
the follicle being new a delicate
Line 8,318: Line 7,677:
yolk and the preparation for the attachment of the ovum to the uterus
yolk and the preparation for the attachment of the ovum to the uterus
are all adjustments to the intra-uterine development of the embryo.
are all adjustments to the intra-uterine development of the embryo.
The role of the follicle cells as a nourishing membrane has been definitely
The role of the follicle cells as a nourishing membrane has been definitely
determined in the dog by experiment. The follicle cells are filled with
determined in the dog by experiment. The follicle cells are filled with
mitochondria. When lecithin is injected into a dog these mitochondria
mitochondria. When lecithin is injected into a dog these mitochondria
increase in number. However, if the dog is allowed to become hungry,
increase in number. However, if the dog is allowed to become hungry,
Line 8,325: Line 7,684:
TERTIARY MEMBRANES 223
TERTIARY MEMBRANES 223


developing egg. The identification of lecithin or of a similar substance
developing egg. The identification of lecithin or of a similar substance
has been observed by Russo in the protoplasmic bridges which penetrate
has been observed by Russo in the protoplasmic bridges which penetrate
the zona radiata.
the zona radiata.
Line 8,335: Line 7,694:
or by special glands connected with them. Tertiary membranes are of
or by special glands connected with them. Tertiary membranes are of
various kinds, gelatinous, horny and chitinous, or cocoon-like. The
various kinds, gelatinous, horny and chitinous, or cocoon-like. The
type of membrane shows adaptive correlation to the needs of the de-
type of membrane shows adaptive correlation to the needs of the developing embryo. The gelatinous type of covering is frequently seen in
veloping embryo. The gelatinous type of covering is frequently seen in
fishes and in amphibians and also in many invertebrates, as Geryonia,
fishes and in amphibians and also in many invertebrates, as Geryonia,
and Sagitta. Chitinous shells cover the eggs of the phylopods, Apus
and Sagitta. Chitinous shells cover the eggs of the phylopods, Apus
and Branchipus, and a horny capsule covers the shark’s egg. Under the
and Branchipus, and a horny capsule covers the shark’s egg. Under the
Line 8,343: Line 7,701:
or both for in some eggs all three types are present.
or both for in some eggs all three types are present.


In the cephalopods the tertiary membranes show different modifica-
In the cephalopods the tertiary membranes show different modifications. The egg of Sepia and its surrounding albumen is covered by a
tions. The egg of Sepia and its surrounding albumen is covered by a
black leathery capsule, but in Loligo the eggs, each in a firm envelope,
black leathery capsule, but in Loligo the eggs, each in a firm envelope,
are arranged in a gelatinous mass known as “dead men’s fingers.” The
are arranged in a gelatinous mass known as “dead men’s fingers.” The
flatworms have cocoons which are formed in the ovary. There are
flatworms have cocoons which are formed in the ovary. There are
various kinds. Branchiobdella has a stalked capsule containing one egg.
various kinds. Branchiobdella has a stalked capsule containing one egg.
The rhabdocoele turbellarian cocoon contains several eggs. In this
The rhabdocoele turbellarian cocoon contains several eggs. In this
Line 8,368: Line 7,725:
of which are utilized to contribute to the growth of the embryo formed
of which are utilized to contribute to the growth of the embryo formed
from that one. (This is the phenomenon called by some “cannibalism.”)
from that one. (This is the phenomenon called by some “cannibalism.”)
Some insects also have cocoons which are tertiary membranes as con-
Some insects also have cocoons which are tertiary membranes as contrasted with the larval cocoon formed for the pupa of the butterfly.
trasted with the larval cocoon formed for the pupa of the butterfly.
Periplaneta has a cocoon which is carried by the female attached to the
Periplaneta has a cocoon which is carried by the female attached to the
224 EGG AND EMBRYONIC MEMBRANES
224 EGG AND EMBRYONIC MEMBRANES


posterior end of the abdomen. In this cocoon the eggs are laid each en-
posterior end of the abdomen. In this cocoon the eggs are laid each enclosed in the vitelline membrane and the chorion. H ydrophilus, the water
closed in the vitelline membrane and the chorion. H ydrophilus, the water
beetle, has a round cocoon in the form of a web. The female places
beetle, has a round cocoon in the form of a web. The female places
the cocoon on the under side of a leaf to which it is attached by a stalk.
the cocoon on the under side of a leaf to which it is attached by a stalk.
There are fofty-five to fifty eggs in palisade-like arrangement within the
There are fofty-five to fifty eggs in palisade-like arrangement within the
cocoon nourished from the substance of the web.
cocoon nourished from the substance of the web.


Line 8,383: Line 7,738:
The albumen and the horny capsule are deposited about the egg while
The albumen and the horny capsule are deposited about the egg while
it is in the oviduct. The capsule differs in different species. In the sharks
it is in the oviduct. The capsule differs in different species. In the sharks
its four corners are drawn out into fibers which permit the egg to cling
its four corners are drawn out into fibers which permit the egg to cling
to water plants. Occasionally several eggs are found in one capsule.
to water plants. Occasionally several eggs are found in one capsule.


Line 8,394: Line 7,749:


A gelatinous covering over the egg is typical of the amphibia. In
A gelatinous covering over the egg is typical of the amphibia. In
many of the amphibia there are special modifications of these tertiary
many of the amphibia there are special modifications of these tertiary
envelopes. An interesting example of this kind is that of a tropical
envelopes. An interesting example of this kind is that of a tropical
anuran. At the time of egg laying the oviducal secretion which surrounds
anuran. At the time of egg laying the oviducal secretion which surrounds
the eggs is beaten up by the hind legs of the parents into a fine foam
the eggs is beaten up by the hind legs of the parents into a fine foam
containing many air bubbles. This foam is sometimes placed on the
containing many air bubbles. This foam is sometimes placed on the
surface of the pond and floats about or it may also be placed in a wet
surface of the pond and floats about or it may also be placed in a wet
hollow on the ground. Some of the frogs deposit the eggs in a mass of
hollow on the ground. Some of the frogs deposit the eggs in a mass of
jelly on one or more leaves. Sometimes the single leaf is bent by the
jelly on one or more leaves. Sometimes the single leaf is bent by the
Line 8,447: Line 7,802:
egg itself the animal kingdom possesses numerous cases of accessory
egg itself the animal kingdom possesses numerous cases of accessory
membranes which are developed by the embryo. These are in the
membranes which are developed by the embryo. These are in the
nature of cellular sheets which by various invaginations, foldings, out-
nature of cellular sheets which by various invaginations, foldings, outpushings, etc., cover the embryo or parts of it. They are especially well
pushings, etc., cover the embryo or parts of it. They are especially well
developed in the vertebrates and to that group most of the attention
developed in the vertebrates and to that group most of the attention
is paid by embryologists. Nevertheless, among the invertebrates there
is paid by embryologists. Nevertheless, among the invertebrates there
Line 8,463: Line 7,817:
Of the invertebrates proper certain molluscs show the development
Of the invertebrates proper certain molluscs show the development
of the yolk sac. The amnion occurs more or less developed in the pilidium
of the yolk sac. The amnion occurs more or less developed in the pilidium
larva of the nemerteans, in the developing Polygordius, in the echino-
larva of the nemerteans, in the developing Polygordius, in the echinopluteus when it is undergoing a metamorphosis, in the larva of insects
pluteus when it is undergoing a metamorphosis, in the larva of insects
and of the scorpions. Some of these groups also show the possession of 8.
and of the scorpions. Some of these groups also show the possession of 8.
serosa in connection with the amnion.
serosa in connection with the amnion.
Line 8,471: Line 7,824:
The Yolk Sac
The Yolk Sac


The true yolk sac can occur only in forms having an extreme telo-
The true yolk sac can occur only in forms having an extreme telolecithal type of egg structure. Among the invertebrates the cephalopods
lecithal type of egg structure. Among the invertebrates the cephalopods


FIG. 160. Various stages in the development of 0. squid, showing the relations of the
fiG. 160. Various stages in the development of 0. squid, showing the relations of the
yolk sac. (Modified from Harmon and Gardiner.)
yolk sac. (Modified from Harmon and Gardiner.)


B and C. dorsal views; D, sagittal section. a., arm rudiment; {., funnel; m., mouth; o.c.,
B and C. dorsal views; D, sagittal section. a., arm rudiment; {., funnel; m., mouth; o.c.,
Line 8,497: Line 7,849:
and constitutes the internal yolk sac in contrast with the external one
and constitutes the internal yolk sac in contrast with the external one
which has just been mentioned. The yolk masses of the two are joined
which has just been mentioned. The yolk masses of the two are joined
at all times, however. The further growth of the embryo results in pro-
at all times, however. The further growth of the embryo results in proportionate decrease in the size of the external yolk sac which is gradually
portionate decrease in the size of the external yolk sac which is gradually
included within the body of the young animal. Morphologically this
included within the body of the young animal. Morphologically this
structure represents a precocious median development of the mass of
structure represents a precocious median development of the mass of
tissue which produces the arms of the squid and is comparable to the
tissue which produces the arms of the squid and is comparable to the
developing foot of other molluscs. Strictly speaking it is not merely an
developing foot of other molluscs. Strictly speaking it is not merely an
embryonic appendage, for all of it is finally withdrawn into the body
embryonic appendage, for all of it is finally withdrawn into the body
of the growing animal. A somewhat similar ventral protrusion from the
of the growing animal. A somewhat similar ventral protrusion from the
foot of the snail, Helzlr, was described by Lankester and while not a
foot of the snail, Helzlr, was described by Lankester and while not a
Line 8,513: Line 7,864:
The first structure in the animal kingdom which may be designated
The first structure in the animal kingdom which may be designated
as an amnion is seen in the metamorphosis of the pilidium larva of the
as an amnion is seen in the metamorphosis of the pilidium larva of the
nemerteans which is described on page 153 (Figs. 103 and 104). On the
nemerteans which is described on page 153 (figs. 103 and 104). On the
flattened under surface of the helmet-like pilidium, four amniotic in-
flattened under surface of the helmet-like pilidium, four amniotic invaginations form. They consist of 'ciliated ectoderm and other deeper
vaginations form. They consist of 'ciliated ectoderm and other deeper
parts and are known as the imaginal discs. Their continued inward
parts and are known as the imaginal discs. Their continued inward
growth upward and over the alimentary tract finally results in their
growth upward and over the alimentary tract finally results in their
fusion. The inner parts, or the imaginal discs, form the outer covering
fusion. The inner parts, or the imaginal discs, form the outer covering
of the little worms while the remaining portions of the coalesced in-
of the little worms while the remaining portions of the coalesced invagination make up the amnion which is a temporary covering entirely
vagination make up the amnion which is a temporary covering entirely
lost with metamorphosis.
lost with metamorphosis.


The second appearance of the amnion is seen in the metamorphosis
The second appearance of the amnion is seen in the metamorphosis
of the annelid, Polygordius. This structure superficially resembles that
of the annelid, Polygordius. This structure superficially resembles that
of the pilidium, for here also four invaginations appear arising from a
of the pilidium, for here also four invaginations appear arising from a
circular groove which is known as the amniotic fold. It serves as a
circular groove which is known as the amniotic fold. It serves as a
covering for the folded portion of the worm which remains in this con-
covering for the folded portion of the worm which remains in this con228 EGG AND EMBRYONIC MEMBRANES
228 EGG AND EMBRYONIC MEMBRANES


dition until the time of metamorphosis when, by severe contraction,
dition until the time of metamorphosis when, by severe contraction,
Line 8,537: Line 7,885:
echinopluteus of the sea-urchin. It occurs on the left side of the larva as
echinopluteus of the sea-urchin. It occurs on the left side of the larva as
a pit which deepens and broadens until it comes in contact with the
a pit which deepens and broadens until it comes in contact with the
wall of the hydrocoele. The tissue which lies between the amniotic in-
wall of the hydrocoele. The tissue which lies between the amniotic in
 
   
   


FIG. 161. Transverse sections of embryos of Clytia. (Redrawn from Folsom after
fiG. 161. Transverse sections of embryos of Clytia. (Redrawn from Folsom after
Lecaillon.)
Lecaillon.)


Line 8,554: Line 7,901:


In the scorpion, according to Brauer, an amnion is formed shortly
In the scorpion, according to Brauer, an amnion is formed shortly
after the two-layered stage shown in Fig. 39. At the edge of the blaste-
after the two-layered stage shown in fig. 39. At the edge of the blastederm a sheet of cells arises and grows backward and presently a second
derm a sheet of cells arises and grows backward and presently a second
layer is formed over the first. The outer is the serosa and the inner the
layer is formed over the first. The outer is the serosa and the inner the
amnion. Underneath these the embryo develops.
amnion. Underneath these the embryo develops.


Line 8,563: Line 7,909:
THE AMNION 229
THE AMNION 229


really two types of development with respect to the relations of forma-
really two types of development with respect to the relations of formative area. and of yolk shown in the insects. In the one type, called by
tive area. and of yolk shown in the insects. In the one type, called by


some “overgrown,” the germ band retains its original position in the
some “overgrown,” the germ band retains its original position in the
blastoderm and the folds of the amnion and serosa arise at its sides and
blastoderm and the folds of the amnion and serosa arise at its sides and


FIG. 162. Diagrammntie sagittal sections of Calopteryx. (From Folsom, after Brandt.)
fiG. 162. Diagrammntie sagittal sections of Calopteryx. (From Folsom, after Brandt.)


A-D, illustrate invaginution of germ band; E-F, illustrate rex olution of embryo. a.,
A-D, illustrate invaginution of germ band; E-F, illustrate rex olution of embryo. a.,
anterior pole; a.c., amniotic cavity; am., amnion; z1iit., antenna; b. blastodcrm, d.,
anterior pole; a.c., amniotic cavity; am., amnion; z1iit., antenna; b. blastodcrm, d.,
dorsal; g.. germ band; h., head end of germ band; 1., laliriuin, l‘-l“, thoracic legs; m., man-
dorsal; g.. germ band; h., head end of germ band; 1., laliriuin, l‘-l“, thoracic legs; m., mandible; mx., maxilla; p., posterior pole; 5., sorosa; v., ventral; y , yolk.
dible; mx., maxilla; p., posterior pole; 5., sorosa; v., ventral; y , yolk.


grow over it. This occurs in the Coleoptera, and it is for this reason that
grow over it. This occurs in the Coleoptera, and it is for this reason that
the formation of the amnion is most clearly shown there. In the other
the formation of the amnion is most clearly shown there. In the other
type, called “invaginated,” the germ band invaginates at one end of the
type, called “invaginated,” the germ band invaginates at one end of the
egg, and is finally carried into a cavity formed within the yolk mass;
egg, and is finally carried into a cavity formed within the yolk mass;
after the closure of the opening of the invagination the formative portion
after the closure of the opening of the invagination the formative portion
develops entirely within the egg. Due to this invagination the ventral
develops entirely within the egg. Due to this invagination the ventral
Line 8,588: Line 7,932:
embryo at length resumes its original orientation. This type occurs in
embryo at length resumes its original orientation. This type occurs in
the Odonata. The relations of the folds of the amnion are shown in
the Odonata. The relations of the folds of the amnion are shown in
Fig. 116, which illustrates the development of Hydrophilus, and also
fig. 116, which illustrates the development of Hydrophilus, and also
in Fig. 161, which shows the formation of the amnion in the beetle
in fig. 161, which shows the formation of the amnion in the beetle
Clytra. Folds of the blastoderm arise at the side of the germ band and
Clytra. Folds of the blastoderm arise at the side of the germ band and
continue their growth until they meet above it and fuse. The membrane
continue their growth until they meet above it and fuse. The membrane
thus formed directly above the germ band is the amnion, and the outer
thus formed directly above the germ band is the amnion, and the outer
one, the serosa. The formation of the amnion and serosa in Calopterya:
one, the serosa. The formation of the amnion and serosa in Calopterya:
is shown in Fig. 162.
is shown in fig. 162.


Students of the embryology of the insects are not entirely in agree-
Students of the embryology of the insects are not entirely in agreement in regard to the morphological relations of the embryonic membranes found throughout the group and several types of classification
ment in regard to the morphological relations of the embryonic mem-
branes found throughout the group and several types of classification
have been proposed. It hardly seems necessary to consider the various
have been proposed. It hardly seems necessary to consider the various
classifications or the points upon which they have been based. Serosa
classifications or the points upon which they have been based. Serosa
and amnion occur together in the Coleoptera, Lepidoptera, Diptera,
and amnion occur together in the Coleoptera, Lepidoptera, Diptera,
Dcrmoptera, Isoptera, and Odonata. An amnion only is found in Xenos,
Dcrmoptera, Isoptera, and Odonata. An amnion only is found in Xenos,
Line 8,609: Line 7,951:
B. VERTEBRATES EXCEPT MAMMALS
B. VERTEBRATES EXCEPT MAMMALS


Embryonic membranes are especially well developed in the verte-
Embryonic membranes are especially well developed in the vertebrates where they serve for protection, nutrition, and respiration. These
brates where they serve for protection, nutrition, and respiration. These
are the yolk sac, amnion,serosa or chcrion,allantois, and its derivative,
are the yolk sac, amnion,serosa or chcrion,allantois, and its derivative,
the placenta. Since the name “chorion” is also correctly used for the
the placenta. Since the name “chorion” is also correctly used for the
Line 8,632: Line 7,973:


mesoderm divides into two layers, and the investments of the yolk are
mesoderm divides into two layers, and the investments of the yolk are
first the splanchnopleure (endoderm and mesoderm), then the extra-
first the splanchnopleure (endoderm and mesoderm), then the extra
 
Fra 163 Diagrams of the extraemhryomc membranes of the chick (From Duv9.l’s
Fra 163 Diagrams of the extraemhryomc membranes of the chick (From Duv9.l’s
Atlas)
Atlas)
Line 8,639: Line 7,979:
A, 2-day embryo, B, 3-day embryo a , air space, of , ammotlc fold, a c , amniotic cavity,
A, 2-day embryo, B, 3-day embryo a , air space, of , ammotlc fold, a c , amniotic cavity,
all , allantois, alb , albumen, e , embryo e e c , extruembryomc eoelome, ect , ectoderm,
all , allantois, alb , albumen, e , embryo e e c , extruembryomc eoelome, ect , ectoderm,
end , endoderm, In , mesoderm, ser. serosn; s , shell, sm . shell membrane, so. soma.to-
end , endoderm, In , mesoderm, ser. serosn; s , shell, sm . shell membrane, so. soma.topleure. sp , splanchnopleure, v , vltellmo membrane, y , yolk, y s . yolk sac
pleure. sp , splanchnopleure, v , vltellmo membrane, y , yolk, y s . yolk sac


embryonic coelome, and last the somatopleure (mesoderm and ecto-
embryonic coelome, and last the somatopleure (mesoderm and ectoderm). The anterior and posterior parts of the gut are the first to develop
derm). The anterior and posterior parts of the gut are the first to develop
232 EGG AND EMBRYONIC MEMBRANES
232 EGG AND EMBRYONIC MEMBRANES


a cellular floor. The midgut remains open to the yolk for some time. As
a cellular floor. The midgut remains open to the yolk for some time. As
the embryo becomes constricted off from the yolk the two ends of the
the embryo becomes constricted off from the yolk the two ends of the
gut enlarge further, and the extent of the opening of the midgut is de-
gut enlarge further, and the extent of the opening of the midgut is decreased. finally, the latter is connected to the yolk only by a narrow
creased. Finally, the latter is connected to the yolk only by a narrow


a1l.c.
a1l.c.


Flu 164 (‘ontmuation of Fig 163
flu 164 (‘ontmuation of fig 163
A, 5—day embryo, B, 14-day embryo
A, 5—day embryo, B, 14-day embryo


am , amnion, all e . allantoie cavity, all s , allantolc stalk, u , umbilical stalk
am , amnion, all e . allantoie cavity, all s , allantolc stalk, u , umbilical stalk
neck called the yolk stalk. At the yolk stalk the inner and the extra-
neck called the yolk stalk. At the yolk stalk the inner and the extraembryonic splanchnopleure are continuous. The absorption of yolk
embryonic splanchnopleure are continuous. The absorption of yolk
material through the yolk stalk probably does not occur directly but
material through the yolk stalk probably does not occur directly but
is brought about by the vitelline circulation. Deep yolk sac septa which
is brought about by the vitelline circulation. Deep yolk sac septa which
Line 8,666: Line 8,002:
absorbing cells aid in its digestion and in passing it to the vitelline
absorbing cells aid in its digestion and in passing it to the vitelline
circulation. The yolk mass decreases toward the end of the incubation
circulation. The yolk mass decreases toward the end of the incubation
period, and finally the entire structure is drawn into the body.
period, and finally the entire structure is drawn into the body.


During the early growth of the blastoderm over the yolk the amnion
During the early growth of the blastoderm over the yolk the amnion
and the serosa are being formed. The amnion arises by folds of the
and the serosa are being formed. The amnion arises by folds of the
extraembryonic somatopleure near the anterior region of the embryo.
extraembryonic somatopleure near the anterior region of the embryo.
First to form is the head fold of ectoderm and endoderm, for the meso-
first to form is the head fold of ectoderm and endoderm, for the mesoderm has not yet reached this region, and this is joined by lateral folds
derm has not yet reached this region, and this is joined by lateral folds
of somatopleure so that the entire region is covered. Later a similar tail
of somatopleure so that the entire region is covered. Later a similar tail
fold covers that region and is continued forward until it meets the
fold covers that region and is continued forward until it meets the
Line 8,680: Line 8,015:
the embryo in two membranes of similar nature although of inverted
the embryo in two membranes of similar nature although of inverted
order. The inner membrane or amnion consists of ectoderm continuous
order. The inner membrane or amnion consists of ectoderm continuous
with that ‘over the embryo and of somatic mesoderm. The outer mem-
with that ‘over the embryo and of somatic mesoderm. The outer membrane or serosa consists of somatic mesoderm and of ectoderm continuous with the outer covering of the yolk. Between the amnion and the
brane or serosa consists of somatic mesoderm and of ectoderm continu-
ous with the outer covering of the yolk. Between the amnion and the
serosa is the extraembryonic coelome which is connected with the body
serosa is the extraembryonic coelome which is connected with the body
cavity of the embryo. The serosa is merely a continuation of the soma-
cavity of the embryo. The serosa is merely a continuation of the somatopleure which has made its way nearly around the yolk. It also covers
topleure which has made its way nearly around the yolk. It also covers
the allantois which later develops within the extraembryonic coelome.
the allantois which later develops within the extraembryonic coelome.
Thus it comes to line the shell and covers the embryo and the other
Thus it comes to line the shell and covers the embryo and the other
Line 8,699: Line 8,031:
outer wall, splanchnic on the inside and somatic from the serosa on the
outer wall, splanchnic on the inside and somatic from the serosa on the
outside, and over all is the ectoderm of the serosa. The rapid growth of
outside, and over all is the ectoderm of the serosa. The rapid growth of
the allantois carries it first over the amnion, with which it fuses, and
the allantois carries it first over the amnion, with which it fuses, and
then over the yolk sac. Finally, pushing the serosa before it, it extends
then over the yolk sac. finally, pushing the serosa before it, it extends
even over the albumen, which has become dense from loss of water,
even over the albumen, which has become dense from loss of water,
forming an albumen sac which is lined by the ectoderm of the serosa.
forming an albumen sac which is lined by the ectoderm of the serosa.
The allantois has a rich blood supply in a network lying close to the
The allantois has a rich blood supply in a network lying close to the
porous shell, through which the exchange of gases is made easy. The
porous shell, through which the exchange of gases is made easy. The
chief function of the allantois is respiratory but it also serves as a re-
chief function of the allantois is respiratory but it also serves as a receptacle for the excretory wastes from the kidney of the embryo. Shortly
ceptacle for the excretory wastes from the kidney of the embryo. Shortly
before the chick hatches, its beak breaks through into the air space of
before the chick hatches, its beak breaks through into the air space of
234 EGG AND EMBRYONIC MEMBRANES
234 EGG AND EMBRYONIC MEMBRANES


the egg, pulmonary respiration begins, and the circulation of the allan-
the egg, pulmonary respiration begins, and the circulation of the allantois becomes slower and slower, until at hatching time the dried allantois
tois becomes slower and slower, until at hatching time the dried allantois
remains inside the shell.
remains inside the shell.


With conditions as found in the chick as a starting point, the develop-
With conditions as found in the chick as a starting point, the development of the various vertebrate membranes may be appropriately
ment of the various vertebrate membranes may be appropriately
taken up.
taken up.


Line 8,726: Line 8,055:
   
   


FIG. 165. Embryo of toad fish showing large yolk sac attached.
fiG. 165. Embryo of toad fish showing large yolk sac attached.


pole. (See Chapters IV and V.) The eggs are markedly telolecithal
pole. (See Chapters IV and V.) The eggs are markedly telolecithal
whether the cleavage is holoblastic or meroblastic. The relation be-
whether the cleavage is holoblastic or meroblastic. The relation between discoidal and holoblastic eggs is discussed and illustrated earlier
tween discoidal and holoblastic eggs is discussed and illustrated earlier
(fig. 51) where it is shown that the condition of the large yolk-laden
(Fig. 51) where it is shown that the condition of the large yolk-laden
endoderm cells of the bilateral type is gradually converted into the
endoderm cells of the bilateral type is gradually converted into the
yolk mass of the discoidal type. The latter is incapable of segmentation,
yolk mass of the discoidal type. The latter is incapable of segmentation,
Line 8,739: Line 8,067:
antecedent of the yolk sac of the meroblastic vertebrates. They do not
antecedent of the yolk sac of the meroblastic vertebrates. They do not
constitute a true yolk sac, but the mass of cells is the equivalent of an
constitute a true yolk sac, but the mass of cells is the equivalent of an
internal one and corresponds in a general way to the outer sac of fishes,
internal one and corresponds in a general way to the outer sac of fishes,
reptiles, birds, and mammals. For all of these it is an important nutritive
reptiles, birds, and mammals. For all of these it is an important nutritive
structure.
structure.
Line 8,759: Line 8,087:
the absorption of the yolk is brought about exclusively by the vitelline
the absorption of the yolk is brought about exclusively by the vitelline
vessels. In addition to its nutritive function, the yolk sac often acts
vessels. In addition to its nutritive function, the yolk sac often acts
as a respiratory organ. It functions in this manner in the lower verte-
as a respiratory organ. It functions in this manner in the lower vertebrates whcre an exchange of gases takes
brates whcre an exchange of gases takes
place between the blood vessels of the yolk
place between the blood vessels of the yolk
sac and the surrounding water and also in
sac and the surrounding water and also in
Line 8,766: Line 8,093:
the exchange takes place between its blood
the exchange takes place between its blood
vessels and the medium surrounding the
vessels and the medium surrounding the
egg. Even in mammals the yolk sac may -
egg. Even in mammals the yolk sac may have a respiratory function. In the mono- ‘
have a respiratory function. In the mono- ‘
tremes it still retains its yolk and hence its
tremes it still retains its yolk and hence its
nutritive function. In the placental mam-
nutritive function. In the placental mammals, however, it is devoid of yolk but
mals, however, it is devoid of yolk but
may still be functional in early stages when
may still be functional in early stages when
it is quite vascular and helps to absorb FIG 166 Embryo of Torpedo
it is quite vascular and helps to absorb fiG 166 Embryo of Torpedo
nourishment from the maternal tissues. §l;?,Y,‘“§sb?:“:f0r,;°:  
nourishment from the maternal tissues. §l;?,Y,‘“§sb?:“:f0r,;°:  


Line 8,788: Line 8,113:
The Amnion
The Amnion


In the Sauropsida (reptiles and birds), we have the first appearance
In the Sauropsida (reptiles and birds), we have the first appearance
of the amnion, serosa, and allantois. This group and the mammals make
of the amnion, serosa, and allantois. This group and the mammals make
up the Amniota, which possess the amnion and are contrasted with the
up the Amniota, which possess the amnion and are contrasted with the
Line 8,794: Line 8,119:
236 EGG AND EMBRYONIC MEMBRANES
236 EGG AND EMBRYONIC MEMBRANES


fluid medium, usually water, the developing embryos are not subjected
fluid medium, usually water, the developing embryos are not subjected
to injury through violent motion or through changes in temperature or
to injury through violent motion or through changes in temperature or
in humidity, and thus no special covering of the embryo is necessary.
in humidity, and thus no special covering of the embryo is necessary.
Line 8,811: Line 8,136:
   
   


FIG 167 Diagrammatxe transverse section through a (‘helonian embryo (Cl€m"l1I8)-
fiG 167 Diagrammatxe transverse section through a (‘helonian embryo (Cl€m"l1I8)(Redrawn from Kerr. based on a figure of Mitsukuri.)
(Redrawn from Kerr. based on a figure of Mitsukuri.)


has split into its two layers. In the Chelonia the amnion is at flrst formed
has split into its two layers. In the Chelonia the amnion is at flrst formed
of ectoderm and endoderm, the mid-dorsal part being of solid ectoderm.
of ectoderm and endoderm, the mid-dorsal part being of solid ectoderm.
Later after the mesoderm has split it is drawn up into the amniotic
Later after the mesoderm has split it is drawn up into the amniotic
Line 8,825: Line 8,149:
the scro-amniotic isthmus in the amniotic roof of the chick. This latter
the scro-amniotic isthmus in the amniotic roof of the chick. This latter
may be considered as the remains of the broader layer of the reptiles.
may be considered as the remains of the broader layer of the reptiles.
The amniotic fold in the Chelonia begins at the head end and pro-
The amniotic fold in the Chelonia begins at the head end and proceeds backward until the whole embryo is covered. By the backward
ceeds backward until the whole embryo is covered. By the backward
growth of this flap there is formed a long tunnel-like cavity covering
growth of this flap there is formed a long tunnel-like cavity covering
the embryo and extending posterior to it. Later this posterior extension
the embryo and extending posterior to it. Later this posterior extension
becomes partly obliterated and the cavity is closed. This again is quite
becomes partly obliterated and the cavity is closed. This again is quite
Line 8,835: Line 8,158:
lateral fold, and a tail fold take part. In some reptiles, however, as the
lateral fold, and a tail fold take part. In some reptiles, however, as the
chameleons, amnion formation is similar to that of birds, from lateral
chameleons, amnion formation is similar to that of birds, from lateral
folds around the embryo, and is not due to the elongation of one an-
folds around the embryo, and is not due to the elongation of one an
 
5
5
FIG 168 A and B Chelonnn blastodorms showing stages in the formation of the
fiG 168 A and B Chelonnn blastodorms showing stages in the formation of the
amnion A, Cheli/dra, B, Clemmys (Redrawn from Kerr after Mitsukuri)
amnion A, Cheli/dra, B, Clemmys (Redrawn from Kerr after Mitsukuri)


Line 8,848: Line 8,170:
there is no need for the amniotic folds to grow upward as in the chick.
there is no need for the amniotic folds to grow upward as in the chick.
The development of the amnion in the birds as a group offers nothing
The development of the amnion in the birds as a group offers nothing
different in principle from the type already described, that is, from thfi
different in principle from the type already described, that is, from this conditions in the chick. The amnion of the mammals presents new
2381 EGG AND EMBRYONIC MEMBRANES
 
conditions in the chick. The amnion of the mammals presents new
features, however. Their character has already been discussed in the
features, however. Their character has already been discussed in the
chapter on the formation of the mammalian embryo, Chapter X, to
chapter on the formation of the mammalian embryo, Chapter X, to
which the student is referred, and the chief facts regarding it are again
which the student is referred, and the chief facts regarding it are again
mentioned a little later in this chapter under the head of the mem-
mentioned a little later in this chapter under the head of the membranes of the mammalian embryo.
branes of the mammalian embryo.


The Allantois
The Allantois


The allantois appears first in reptiles and is developed in all amniota.
The allantois appears first in reptiles and is developed in all amniota.
It always originates as an outgrowth of the hind gut and has therefore
It always originates as an outgrowth of the hind gut and has therefore
an endodermal lining and an outer layer of mesoderm. In amphibians
an endodermal lining and an outer layer of mesoderm. In amphibians
it is represented by the urinary bladder. In reptiles the outgrowth has
it is represented by the urinary bladder. In reptiles the outgrowth has
been described as solid, but it has also been maintained that the con-
been described as solid, but it has also been maintained that the contracted space in which it develops causes it to be collapsed and so to
tracted space in which it develops causes it to be collapsed and so to
take on the appearance of a solid structure. In birds it has a three-fold
take on the appearance of a solid structure. In birds it has a three-fold
function. It increases in size, probably on account of the large amount
function. It increases in size, probably on account of the large amount
Line 8,878: Line 8,195:
The allantois of mammals acquires no further function. It aids the
The allantois of mammals acquires no further function. It aids the
trophoblast in the formation of the placenta which is for the mammal
trophoblast in the formation of the placenta which is for the mammal
an embryonic organ of nutrition, respiration, and the removal of ex-
an embryonic organ of nutrition, respiration, and the removal of excretion. It thus becomes the most important embryonic membrane of
cretion. It thus becomes the most important embryonic membrane of
mammals, for through the participation of its blood vessels it has the
mammals, for through the participation of its blood vessels it has the
chief part in the formation of the placenta.
chief part in the formation of the placenta.
Line 8,887: Line 8,203:
membranes are also employed in bringing about this mode of caring
membranes are also employed in bringing about this mode of caring
for the embryo. Viviparity occurs in all the vertebrate groups, beginning
for the embryo. Viviparity occurs in all the vertebrate groups, beginning
with the fishes, except the ganoids, lung fishes, and birds. It is possible
with the fishes, except the ganoids, lung fishes, and birds. It is possible
that it may have been characteristic of some fossil ganoids, but probably
that it may have been characteristic of some fossil ganoids, but probably
the birds because of their habit of flight have never been able to develop
the birds because of their habit of flight have never been able to develop
this method of caring for their young. There are many parallel methods
this method of caring for their young. There are many parallel methods
of relating the embryo to the maternal tissues, and functional placentae
of relating the embryo to the maternal tissues, and functional placentae
are not confined to the mammals. In all forms below the mammals the
are not confined to the mammals. In all forms below the mammals the
embryo is chiefly nourished by the yolk sac even though other structural
embryo is chiefly nourished by the yolk sac even though other structural
modifications supply additional sources of food. Development within
modifications supply additional sources of food. Development within
the body of the mother always serves the same function, protection in
the body of the mother always serves the same function, protection in
THE ALLANTOIS 239
THE ALLANTOIS 239
Line 8,901: Line 8,217:
genera in which there is intra—uterine development. In Acanthias the
genera in which there is intra—uterine development. In Acanthias the
typical egg membranes are formed but the horny egg-shell is thin and
typical egg membranes are formed but the horny egg-shell is thin and
disappears in later stages. The uterine wall contributes to the nourish-
disappears in later stages. The uterine wall contributes to the nourishment of the embryo by supplying the albuminous fluid which is enclosed
ment of the embryo by supplying the albuminous fluid which is enclosed
in the egg-shell. In this form the lining of the uterus during later stages
in the egg-shell. In this form the lining of the uterus during later stages
of development is thrown into folds which are brought into contact
of development is thrown into folds which are brought into contact
Line 8,917: Line 8,232:


the yolk sac and, as both are highly vascular, they form a functional
the yolk sac and, as both are highly vascular, they form a functional
yolk sac placenta. A placenta used in this broad sense means any struc-
yolk sac placenta. A placenta used in this broad sense means any structure which brings about, by means of an abundant vascular supply, an
ture which brings about, by means of an abundant vascular supply, an
intimate relation between maternal and embryonic tissue, for the purpose
intimate relation between maternal and embryonic tissue, for the purpose
of conveying nourishment from the one to the other. Here the yolk sac
of conveying nourishment from the one to the other. Here the yolk sac
Line 8,933: Line 8,247:
the uterine wall.
the uterine wall.


Viviparity is uncommon among the amphibia. In one of the sala-
Viviparity is uncommon among the amphibia. In one of the salamanders (Salamandra atra), however, development takes place in the
manders (Salamandra atra), however, development takes place in the
oviduct but usually only one of the eggs reaches maturity for the others
oviduct but usually only one of the eggs reaches maturity for the others
break up and are absorbed by the outer gills of the developing embryo.
break up and are absorbed by the outer gills of the developing embryo.
Line 8,942: Line 8,255:
   
   


FIG 170 Embryo of (‘hulcides tndactylus (Redrawn from Kerr after Giaconiine)
fiG 170 Embryo of (‘hulcides tndactylus (Redrawn from Kerr after Giaconiine)


A, 7-mm embryo, B, 15-16-mm embryo seen from apical pole all, allantois, pl,
A, 7-mm embryo, B, 15-16-mm embryo seen from apical pole all, allantois, pl,
Line 8,950: Line 8,263:
blind worm and the viper, there is a thin shell and the embryo is simply
blind worm and the viper, there is a thin shell and the embryo is simply
held in the uterus, the lining of which remains unchanged. In the lizard,
held in the uterus, the lining of which remains unchanged. In the lizard,
Chalczdes ocellatus, the shell breaks and finally disappears, the uterine
Chalczdes ocellatus, the shell breaks and finally disappears, the uterine
wall becomes vascularized, and 1S thrown into folds which fit other
wall becomes vascularized, and 1S thrown into folds which fit other
folds on the yolk sac. Both the allantois and the uterus adjoining it are
folds on the yolk sac. Both the allantois and the uterus adjoining it are
highly vascularized but the placenta-like folds develop only on the
highly vascularized but the placenta-like folds develop only on the
yolk sac. A type of placenta more nearly approaching that of the
yolk sac. A type of placenta more nearly approaching that of the
mammals is found in still another lizard, Chalczdes trzdactylus. The con-
mammals is found in still another lizard, Chalczdes trzdactylus. The condition of its allantois and yolk sac may be regarded as transitional from
dition of its allantois and yolk sac may be regarded as transitional from
that typical of the Sauropsida to that of the mammals, for both function
that typical of the Sauropsida to that of the mammals, for both function
as placenta and projections from both vascularized sacs interlock with
as placenta and projections from both vascularized sacs interlock with
Line 8,969: Line 8,281:
in the different groups of the vertebrates. In the mammals the wall of
in the different groups of the vertebrates. In the mammals the wall of
the uterus is highly developed as a special adaptation of the maternal
the uterus is highly developed as a special adaptation of the maternal
tissue to accomplish this function. In other forms the oviduct some-
tissue to accomplish this function. In other forms the oviduct sometimes takes care of the need so far as the mother is concerned, and even
times takes care of the need so far as the mother is concerned, and even
the ovary may serve in this capacity. On the part of the embryo, the
the ovary may serve in this capacity. On the part of the embryo, the
yolk sac of lower forms often carries on the function, while in the higher
yolk sac of lower forms often carries on the function, while in the higher
Line 8,983: Line 8,294:
rather general lack of structural homology with that of other classes of
rather general lack of structural homology with that of other classes of
vertebrates, and although similar results are reached convergently so far
vertebrates, and although similar results are reached convergently so far
as the structure of the embryonic membranes is concerned, their meth-
as the structure of the embryonic membranes is concerned, their methods of origin in some forms is very different.
ods of origin in some forms is very different.


There are two great types of development found in the mammals. The
There are two great types of development found in the mammals. The
Line 8,990: Line 8,300:
yolk-laden and their cleavage discoidal. The animals are oviparous, the
yolk-laden and their cleavage discoidal. The animals are oviparous, the
development of the embryo taking place within the egg-shell, as in the
development of the embryo taking place within the egg-shell, as in the
case of the Sauropsida. Cleavage, germ-layer formation, and the de-
case of the Sauropsida. Cleavage, germ-layer formation, and the development of the embryonic membranes is comparable to these processes
velopment of the embryonic membranes is comparable to these processes
in that group. The membranes are of the same kind and are probably
in that group. The membranes are of the same kind and are probably
formed in the same manner.
formed in the same manner.
Line 9,007: Line 8,316:


The marsupials include a number of forms which taken together make
The marsupials include a number of forms which taken together make
up a series similar to that described for the lower vertebrates and illus-
up a series similar to that described for the lower vertebrates and illus242 EGG AND EMBRYONIC MEMBRANES
242 EGG AND EMBRYONIC MEMBRANES


trate the change from a yolk sac placenta to an allantoic placenta. The
trate the change from a yolk sac placenta to an allantoic placenta. The
Line 9,038: Line 8,346:
in the series. The allantois is still small and the yolk sac large. The
in the series. The allantois is still small and the yolk sac large. The
trophoblast forms a syncytium with pseudopodial processes which
trophoblast forms a syncytium with pseudopodial processes which
attack the uterine wall and engulf uterine blood vessels. The nourish-
attack the uterine wall and engulf uterine blood vessels. The nourishment is passed on to the yolk sac which may be correctly called a yolk
ment is passed on to the yolk sac which may be correctly called a yolk
sac placenta, for the connection between the uterine wall and the yolk
sac placenta, for the connection between the uterine wall and the yolk
sac is very close. Parameles illustrates the last step in the series. In this
sac is very close. Parameles illustrates the last step in the series. In this
Line 9,045: Line 8,352:
nourishment. The allantois, however, grows larger, develops a richer
nourishment. The allantois, however, grows larger, develops a richer
blood supply, and reaches the trophoblast. The uterine wall, at the
blood supply, and reaches the trophoblast. The uterine wall, at the
place where the trophoblast touches it, develops a syneytium and be-
place where the trophoblast touches it, develops a syneytium and becomes vascular. The trophoblast disappears and the blood vessels of
comes vascular. The trophoblast disappears and the blood vessels of
the allantois and the uterus come into close contact. There are no true
the allantois and the uterus come into close contact. There are no true
villi as in the higher mammals. This is the first case we have met of a
villi as in the higher mammals. This is the first case we have met of a
Line 9,058: Line 8,364:
cell mass as is described in Chapter X. The embryo resembles a hollow
cell mass as is described in Chapter X. The embryo resembles a hollow
vesicle with a drop hanging from one spot on its inner surface. The
vesicle with a drop hanging from one spot on its inner surface. The
inner cell mass is the formative or embryonic portion. The tropho-
inner cell mass is the formative or embryonic portion. The trophoblast is non-formative and produces only ectoderm of the serosa. After
blast is non-formative and produces only ectoderm of the serosa. After
this stage the inner cell mass or embryonic knob differentiates into two
this stage the inner cell mass or embryonic knob differentiates into two
portions, an upper eetodermal layer from which will be derived the
portions, an upper eetodermal layer from which will be derived the
ectoderm and amnion of the embryo and a lower endodermal layer from
ectoderm and amnion of the embryo and a lower endodermal layer from
which will be derived the enteric canal, the yolk sac, and the allantois.
which will be derived the enteric canal, the yolk sac, and the allantois.
The embryo proper at this stage is called the embryonic shield and con-
The embryo proper at this stage is called the embryonic shield and consists of a layer of ectoderm covering a layer of endoderm. (See fig. 144.)
sists of a layer of ectoderm covering a layer of endoderm. (See Fig. 144.)


Jenkinson has offered an interesting suggestion about the significance
Jenkinson has offered an interesting suggestion about the significance
of the early development of the mammal. He compares the blastocyst
of the early development of the mammal. He compares the blastocyst
stage with the later stage of the reptile or bird in which the yolk sac has
stage with the later stage of the reptile or bird in which the yolk sac has
Line 9,092: Line 8,396:
closely applied to the inner side of the trophoblast and a large yolk sac
closely applied to the inner side of the trophoblast and a large yolk sac
is thus formed. In no case, however, does it contain yolk. It is therefore
is thus formed. In no case, however, does it contain yolk. It is therefore
an insignificant structure and the function which it serves in the lower
an insignificant structure and the function which it serves in the lower


   
   


Fro. 172. Diagram of a. section of rodent embryo. p., placenta; other letters as in Fig. 171.
Fro. 172. Diagram of a. section of rodent embryo. p., placenta; other letters as in fig. 171.


forms is presently taken over by the allantois. The completion of the
forms is presently taken over by the allantois. The completion of the
yolk sac comes only when in later stages the mesoderm is formed be-
yolk sac comes only when in later stages the mesoderm is formed between the endoderm and the trophoblast.
tween the endoderm and the trophoblast.


The formation of the mesoderm begins in the embryonic area and
The formation of the mesoderm begins in the embryonic area and
Line 9,106: Line 8,409:
out into the space between the endoderm and the trophoblast of the
out into the space between the endoderm and the trophoblast of the
vesicle; but at length it pushes out from the embryonic area and grows
vesicle; but at length it pushes out from the embryonic area and grows
between these two layers. An early split in this mesodermal layer com-
between these two layers. An early split in this mesodermal layer completes the yolk sac which thus consists of endoderm and splanchnic
pletes the yolk sac which thus consists of endoderm and splanchnic
mesoderm. The vitelline circulation develops to provide the usual
mesoderm. The vitelline circulation develops to provide the usual
vascular supply.
vascular supply.
Line 9,116: Line 8,418:
THE YOLK SAC 245
THE YOLK SAC 245


early stages it absorbs nutrirnent from the uterus. In these cases it be-
early stages it absorbs nutrirnent from the uterus. In these cases it becomes a yolk sac placenta. When this occurs, as in the ungulates, camivores, and rodents, the yolk sac is large and its blood supply is rich and
comes a yolk sac placenta. When this occurs, as in the ungulates, cami-
vores, and rodents, the yolk sac is large and its blood supply is rich and
comparable to that of the chick. In marsupials, in which the uterine
comparable to that of the chick. In marsupials, in which the uterine
development is of short duration, the yolk sac placenta often functions
development is of short duration, the yolk sac placenta often functions
Line 9,164: Line 8,464:
a, *3"
a, *3"


FIG. 173. Area vasculosa of the yolk sac of the rabbit (After Jenkinson.)
fiG. 173. Area vasculosa of the yolk sac of the rabbit (After Jenkinson.)


later as in the rabbit and squirrel. In some cases the lower wall of the
later as in the rabbit and squirrel. In some cases the lower wall of the
yolk sac is never formed. In others it disappears along with the tropho-
yolk sac is never formed. In others it disappears along with the trophoblast, and the cavity of the yolk sac is in communication with the cavity
blast, and the cavity of the yolk sac is in communication with the cavity
of the uterus. The upper wall of the yolk sac absorbs the material secreted
of the uterus. The upper wall of the yolk sac absorbs the material secreted
by the uterus and its supply of blood vessels carries this to the embryo.
by the uterus and its supply of blood vessels carries this to the embryo.
Thus the yolk sac acts as an accessory placenta.
Thus the yolk sac acts as an accessory placenta.


In the rabbit the yolk sac, which contains a nourishing fluid, is very
In the rabbit the yolk sac, which contains a nourishing fluid, is very
large and in early stages practically fills the blastodermic vesicle. A
large and in early stages practically fills the blastodermic vesicle. A
rich supply of blood vessels develops in the side of the yolk sac which
rich supply of blood vessels develops in the side of the yolk sac which
is toward the embryo. The opposite side contains no mesoderm and
is toward the embryo. The opposite side contains no mesoderm and
Line 9,181: Line 8,480:
246 EGG AND EMBRYONIC MEMBRANES
246 EGG AND EMBRYONIC MEMBRANES


membrane. The two walls of the shrunken vesicle thus come close to-
membrane. The two walls of the shrunken vesicle thus come close together and later they fuse. Since the inner wall of the yolk sac was highly
gether and later they fuse. Since the inner wall of the yolk sac was highly
vascularized its blood vessels continue to supply a large part of the
vascularized its blood vessels continue to supply a large part of the
blastoderm. The rest of the blastoderm is fed by blood vessels of the
blastoderm. The rest of the blastoderm is fed by blood vessels of the
Line 9,210: Line 8,508:


Fm. 174. Diagram of 11 section of embryo of insectivore. u., wall of uterus; other letters
Fm. 174. Diagram of 11 section of embryo of insectivore. u., wall of uterus; other letters
as in Fig. 171.
as in fig. 171.


some insectivores the mesoderm never covers the lower wall of the yolk
some insectivores the mesoderm never covers the lower wall of the yolk
Line 9,240: Line 8,538:
The allantois arises as a diverticulum from the gut in the same manner
The allantois arises as a diverticulum from the gut in the same manner
as in the chick. In the rabbit this diverticulum extends out into the
as in the chick. In the rabbit this diverticulum extends out into the
extraembryonic eoelome and soon comes into relation with the tropho-
extraembryonic eoelome and soon comes into relation with the trophoblast. In many rodents, as the mouse and guinea pig, it is often small
blast. In many rodents, as the mouse and guinea pig, it is often small
and its endoderm may not grow beyond the body of the embryo. In Tarsius and in man the vesicle never extends freely into the extraembryonic
and its endoderm may not grow beyond the body of the embryo. In Tar-
sius and in man the vesicle never extends freely into the extraembryonic
eoelome but is enclosed as a vestigial structure in the body stalk. This
eoelome but is enclosed as a vestigial structure in the body stalk. This
latter is an enlargement of the primitive connection between the embryo
latter is an enlargement of the primitive connection between the embryo
Line 9,265: Line 8,561:
A placenta is any organ which brings about an intimate relation and
A placenta is any organ which brings about an intimate relation and
vascular connection between maternal and foetal tissues. The formation
vascular connection between maternal and foetal tissues. The formation
of a yolk sac placenta has been described for some of the fishes and
of a yolk sac placenta has been described for some of the fishes and
reptiles and is again found among the marsupial mammals. Among the
reptiles and is again found among the marsupial mammals. Among the
higher mammals, however, it is always the allantois which brings about
higher mammals, however, it is always the allantois which brings about
Line 9,289: Line 8,585:


The placentae of mammals are of two general types, deciduate and
The placentae of mammals are of two general types, deciduate and
non—deciduate. The non—deciduate placenta is sometimes called a semi-
non—deciduate. The non—deciduate placenta is sometimes called a semiplacenta. The name deciduate was given to indicate the loss, at birth,
placenta. The name deciduate was given to indicate the loss, at birth,
of the lining of the uterus. Although this loss is not significant in all socalled deciduate forms, the name has still been retained. The following
of the lining of the uterus. Although this loss is not significant in all so-
brief classification of types of placentae of the Placentalia is partly based
called deciduate forms, the name has still been retained. The following
brief classification of types of placentae of the Placentalia is partly based
on the conception of Jenkinson. The types are closely related to the
on the conception of Jenkinson. The types are closely related to the
method of implantation of the ovum in the uterine wall. Of implantation
method of implantation of the ovum in the uterine wall. Of implantation
there are three types, central, eccentric, and interstitial, as mentioned in
there are three types, central, eccentric, and interstitial, as mentioned in
Chapter X. Implantation is central if the embryo becomes attached
Chapter X. Implantation is central if the embryo becomes attached
superficially to the uterine wall; eccentric if it is enclosed by folds of
superficially to the uterine wall; eccentric if it is enclosed by folds of
the uterus; or it is interstitial if the embryo burrows down into the
the uterus; or it is interstitial if the embryo burrows down into the
uterine wall. The classes of placentae are as follows:
uterine wall. The classes of placentae are as follows:


The non—deciduate type is that in which the surface of the tropho-
The non—deciduate type is that in which the surface of the trophoblast develops villi which fit into crypts or depressions in the uterine
blast develops villi which fit into crypts or depressions in the uterine
wall. In the simplest cases, the uterine epithelium persists in these
wall. In the simplest cases, the uterine epithelium persists in these
crypts and at birth the villi are drawn out without damage to the uterus.
crypts and at birth the villi are drawn out without damage to the uterus.
In other cases, the uterine epithelium is destroyed and there is a closer
In other cases, the uterine epithelium is destroyed and there is a closer
union between foetal and maternal tissues. This type of placenta is
union between foetal and maternal tissues. This type of placenta is
characteristic of the ungulates, but is also found in the Cetacea, Eden-
characteristic of the ungulates, but is also found in the Cetacea, Edentata, Sirenia, and Lemuroidea except Tarsius.
tata, Sirenia, and Lemuroidea except Tarsius.


The second type is the deciduate in which the uterine epithelium
The second type is the deciduate in which the uterine epithelium
Line 9,328: Line 8,620:
trophoblast and they are the chief part of the placenta contributed by
trophoblast and they are the chief part of the placenta contributed by
uterus. Blood is the principal maternal tissue lost at birth, and the
uterus. Blood is the principal maternal tissue lost at birth, and the
deciduae are thin and more or less degenerate. The portion of the tropho-
deciduae are thin and more or less degenerate. The portion of the trophoblast which is involved in the placenta is disc-shaped. Placentae of this
blast which is involved in the placenta is disc-shaped. Placentae of this
type are found among rodents, insectivores, bats, in Tarsius, monkeys,
type are found among rodents, insectivores, bats, in Tarsius, monkeys,
and man. These three types of placentae require a more detailed
and man. These three types of placentae require a more detailed
description.
description.


Non—decz'duate Placenta. The non—deciduate placenta may be illus-
Non—decz'duate Placenta. The non—deciduate placenta may be illustrated by that of the ungulates. In these forms the allantois enlarges
trated by that of the ungulates. In these forms the allantois enlarges
rapidly and occupies the length of the trophoblast. The surface of the
rapidly and occupies the length of the trophoblast. The surface of the
trophoblast forms villi into which extend the mesoderm and blood
trophoblast forms villi into which extend the mesoderm and blood
Line 9,352: Line 8,642:
around the trophoblast.
around the trophoblast.


The trophoblastic villi fit into crypts or corresponding depressions in
The trophoblastic villi fit into crypts or corresponding depressions in
the uterine wall. When the villi are in groups or cotyledons, the corre-
the uterine wall. When the villi are in groups or cotyledons, the corresponding groups of crypts on the maternal side are called maternal
sponding groups of crypts on the maternal side are called maternal
cotyledons. These latter are in some cases stalked and the foetal cotyledons are then concave.
cotyledons. These latter are in some cases stalked and the foetal coty-
ledons are then concave.


In the difiuse placenta, the uterine epithelium persists as the lining
In the difiuse placenta, the uterine epithelium persists as the lining
of the crypts and at birth the villi are withdrawn with no injury to the
of the crypts and at birth the villi are withdrawn with no injury to the
uterus. In the cotyledonous placenta the uterine epithelium, except that
uterus. In the cotyledonous placenta the uterine epithelium, except that
Line 9,366: Line 8,654:


In the diffuse placenta the uterine and trophoblastic epithelia are in
In the diffuse placenta the uterine and trophoblastic epithelia are in
contact, but in the cotylcdonary placenta the contact of the tropho-
contact, but in the cotylcdonary placenta the contact of the tropho250 EGG AND EMBRYONIC MEMBRANES
250 EGG AND EMBRYONIC MEMBRANES


blastic epithelium is with a highly modified and vascular subepithelial
blastic epithelium is with a highly modified and vascular subepithelial
connective tissue. In the latter case, however, there is no true fusion of
connective tissue. In the latter case, however, there is no true fusion of
foetal and maternal tissue as is true of the deciduate placentae. The
foetal and maternal tissue as is true of the deciduate placentae. The
maternal connective tissue and trophoblastic villi are both rich in capil-
maternal connective tissue and trophoblastic villi are both rich in capillaries. Nourishment is obtained by the trophoblast in two Ways. Both
laries. Nourishment is obtained by the trophoblast in two Ways. Both
the villi and the trophoblastic cells at their base absorb nourishment
the villi and the trophoblastic cells at their base absorb nourishment
(“uterine milk”) from the maternal tissues, and extravasted blood and
(“uterine milk”) from the maternal tissues, and extravasted blood and
Line 9,384: Line 8,670:
5:".
5:".


F10. 176. Cross sections of placentae. A, pig; B, cow; C, out. (Modified from Grosser.)
F10. 176. Cross sections of placentae. A, pig; B, cow; C, out. (Modified from Grosser.)


d.. degenerating uterine epithelium; 0., embryonic capillary; m., maternal capillary;
d.. degenerating uterine epithelium; 0., embryonic capillary; m., maternal capillary;
Line 9,394: Line 8,680:
blood in these vessels is separated by very thin layers of tissue only.
blood in these vessels is separated by very thin layers of tissue only.
The placental layer consists, on the foetal side, of the capillary walls,
The placental layer consists, on the foetal side, of the capillary walls,
connective tissue, and trophoblast, and on the maternal side of con-
connective tissue, and trophoblast, and on the maternal side of connective tissue, eapillary walls and, in the diffuse placentae, of uterine
nective tissue, eapillary walls and, in the diffuse placentae, of uterine
epithelium also. Thus diffusion between foetal and maternal blood
epithelium also. Thus diffusion between foetal and maternal blood
vessels is easily carried on.
vessels is easily carried on.
DECIDUATE PLACENTA 251
DECIDUATE PLACENTA 251


In the allantoic fluid of ungulates are found bodies of queer shapes
In the allantoic fluid of ungulates are found bodies of queer shapes
called hippomanes. These are formed as accumulations of coagulable
called hippomanes. These are formed as accumulations of coagulable
material from the uterine milk and become saturated with calcium ox-
material from the uterine milk and become saturated with calcium oxalate crystals. They push, pocket-like, into the trophoblastic wall between the cotyledons and later are pinched off into the cavity of the
alate crystals. They push, pocket-like, into the trophoblastic wall be-
tween the cotyledons and later are pinched off into the cavity of the
allantois, surrounded by trophoblast and allantoic wall.
allantois, surrounded by trophoblast and allantoic wall.


Line 9,414: Line 8,697:
Deciduate Placenta. In deciduate placentae the union of maternal
Deciduate Placenta. In deciduate placentae the union of maternal
and foetal tissues is closer than in placentae of the non-deciduate type.
and foetal tissues is closer than in placentae of the non-deciduate type.
In deciduate placentae, part or all of the trophoblast, called the tropho-
In deciduate placentae, part or all of the trophoblast, called the trophoderm, becomes specialized and, by the aid of enzymes, erodes the
derm, becomes specialized and, by the aid of enzymes, erodes the
uterine wall. At birth the lining of the uterus is removed as part of the
uterine wall. At birth the lining of the uterus is removed as part of the
placenta. In the zonary deciduate type, this lining or decidua is in close
placenta. In the zonary deciduate type, this lining or decidua is in close
Line 9,429: Line 8,711:
between the naon-deciduate and the discoidal deciduate types. In the
between the naon-deciduate and the discoidal deciduate types. In the
Carnivora, the trophoblast destroys the uterine epithelium (but not the
Carnivora, the trophoblast destroys the uterine epithelium (but not the
subepithelium) and eats its way into the wall of the uterus. Here tropho-
subepithelium) and eats its way into the wall of the uterus. Here trophoblastic villi invade the connective tissue of the
blastic villi invade the connective tissue of the
uterus and come in contact with the maternal
uterus and come in contact with the maternal
capillaries which are much richer than in the
capillaries which are much richer than in the
Line 9,444: Line 8,725:
maternal blood is separated from the foetal
maternal blood is separated from the foetal
blood only by these structures. The placenta
blood only by these structures. The placenta
is at first thin, but becomes thicker owing to
is at first thin, but becomes thicker owing to
the elongation and branching of the villi and
the elongation and branching of the villi and
the growth of the connective tissue. When
the growth of the connective tissue. When
birth takes place the blood vessels and con-
birth takes place the blood vessels and connective tissue of the uterus are removed along
nective tissue of the uterus are removed along
with the foetal vessels and the connective
with the foetal vessels and the connective
tissue. It is possible that this placenta may
tissue. It is possible that this placenta may
Line 9,458: Line 8,738:
showing band-shaped placenta wall_
showing band-shaped placenta wall_
11 te ' t' fth ' . . . .
11 te ' t' fth ' . . . .
((:R:iui*(:a.wrtisfIl'(dxl)1 Co:§ill.:.1)vorcs The placenta of the dzscozdal deczduate type
((:R:iui*(:a.wrtisfil'(dxl)1 Co:§ill.:.1)vorcs The placenta of the dzscozdal deczduate type


differs from the carnivorous placenta in that
differs from the carnivorous placenta in that
Line 9,464: Line 8,744:


capillaries but broad laeunar spaces which have formed in the walls
capillaries but broad laeunar spaces which have formed in the walls
of the trophoblast itself. The tissue of the placenta is almost en-
of the trophoblast itself. The tissue of the placenta is almost entirely of foetal origin. The placenta of the mouse may be taken as
tirely of foetal origin. The placenta of the mouse may be taken as
typical of this type. In this form the trophoblast erodes the uterine
typical of this type. In this form the trophoblast erodes the uterine
epithelium and attaches itself to the subepithelial tissues of the
epithelium and attaches itself to the subepithelial tissues of the
Line 9,476: Line 8,755:
from ruptured vessels of the eroded uterine wall circulates in the lacunae.
from ruptured vessels of the eroded uterine wall circulates in the lacunae.
The maternal and foetal blood, however, are separated from each other
The maternal and foetal blood, however, are separated from each other
only by the walls of the trophoblastic lacunae, a small amount of con-
only by the walls of the trophoblastic lacunae, a small amount of connective tissue, and the walls of the capillaries themselves. As these
nective tissue, and the walls of the capillaries themselves. As these
lacunae are in such close relation to the allantoic capillaries, diffusion
lacunae are in such close relation to the allantoic capillaries, diffusion
is easily possible between them. The placenta of the mouse is typical
is easily possible between them. The placenta of the mouse is typical
Line 9,484: Line 8,762:
   
   


FIG. 179. Diz1.gr:un of embryo of carnivore enclosed in uterus. Band—shuped placenta
fiG. 179. Diz1.gr:un of embryo of carnivore enclosed in uterus. Band—shuped placenta
IS represented as if transparent, showing embryo in section below. Letters as in Fig. 171.
IS represented as if transparent, showing embryo in section below. Letters as in fig. 171.


circulates in lacunar spaces in the trophoblast one can readily under-
circulates in lacunar spaces in the trophoblast one can readily understand why the uterus loses only blood and a slight amount of connective
stand why the uterus loses only blood and a slight amount of connective
tissue at birth.
tissue at birth.


Line 9,500: Line 8,777:
cytotrophoblast or layer of Langhans, which consists of distinct cubical
cytotrophoblast or layer of Langhans, which consists of distinct cubical
cells. The plasrnotrophoblast at its place of attachment to the uterus
cells. The plasrnotrophoblast at its place of attachment to the uterus
erodes the uterine epithelium and dissolves the wall. The outer tropho-
erodes the uterine epithelium and dissolves the wall. The outer trophoblast has a spongy character and the spaces become filled with maternal
blast has a spongy character and the spaces become filled with maternal
254 EGG AND EMBRYONIC MEMBRANES
254 EGG AND EMBRYONIC MEMBRANES


blood from the eroded uterine wall. Later the spongy network is trans-
blood from the eroded uterine wall. Later the spongy network is transformed into villi which are surrounded by the trophoblastic spaces that
formed into villi which are surrounded by the trophoblastic spaces that
now have the character of lacunae. These villi are at first solid, with
now have the character of lacunae. These villi are at first solid, with
the syncytial layer on the outside and cells within except in late stages
the syncytial layer on the outside and cells within except in late stages
when the cellular layer disappears. Some of the villi branch freely into
when the cellular layer disappears. Some of the villi branch freely into
Line 9,518: Line 8,793:


Fro. 180. Diagram of human embryo 1n utero.
Fro. 180. Diagram of human embryo 1n utero.
d.r., decidua reflcxa; c.u., cavity of uterus, um., umbilical cord.
d.r., decidua reflcxa; c.u., cavity of uterus, um., umbilical cord.


villi of ungulates, which are projections from the wall of the trophoblast.
villi of ungulates, which are projections from the wall of the trophoblast.
They are not villi at all in this sense but are more like the foetal capil-
They are not villi at all in this sense but are more like the foetal capillaries of rodents which are covered by the trophoblast into which they
laries of rodents which are covered by the trophoblast into which they
have pushed. They are merely the irregular walls of the lacunae of the
have pushed. They are merely the irregular walls of the lacunae of the
trophoblast.
trophoblast.


The villi are at first over the whole surface of the trophoblast (diffuse
The villi are at first over the whole surface of the trophoblast (diffuse
placenta), but later, those nearest to the cavity of the uterus degenerate
placenta), but later, those nearest to the cavity of the uterus degenerate
so that here the surface is smooth. The villi of the other side remain
so that here the surface is smooth. The villi of the other side remain
Line 9,535: Line 8,809:
is attached is known as the decidua basalis or serotina, and the opposite
is attached is known as the decidua basalis or serotina, and the opposite
wall the decidua Vera. In man the decidua capsularis comes in contact
wall the decidua Vera. In man the decidua capsularis comes in contact
with the decidua vera in the fifth month and the uterine cavity is
with the decidua vera in the fifth month and the uterine cavity is
obliterated. Later the capsularis becomes non-vascular and gradually
obliterated. Later the capsularis becomes non-vascular and gradually
DECIDUATE PLACENTA 255
DECIDUATE PLACENTA 255
Line 9,542: Line 8,816:
This in turn, becomes degenerate, as only the inner portion of the
This in turn, becomes degenerate, as only the inner portion of the
uterine lining remains. The decidua basalis, on the other hand, takes
uterine lining remains. The decidua basalis, on the other hand, takes
an important part in the formation of the placenta. The uterine capil-
an important part in the formation of the placenta. The uterine capillaries increase and maternal blood from this region supplies the placenta.
laries increase and maternal blood from this region supplies the placenta.
In late stages, the basalis is reduced to a very thin membrane.
In late stages, the basalis is reduced to a very thin membrane.


When birth takes place the amnion is ruptured, the amniotic fluid
When birth takes place the amnion is ruptured, the amniotic fluid
escapes and contractions of the uterus expel the embryo, the break
escapes and contractions of the uterus expel the embryo, the break
taking place across the degenerate deciduae. Later, there is discharged
taking place across the degenerate deciduae. Later, there is discharged
Line 9,555: Line 8,828:
    
    


FIG. 181.
fiG. 181.
e.h., capillary of the decidua basalis; e.v., capillary of a villus; i, inter-villous cavity
e.h., capillary of the decidua basalis; e.v., capillary of a villus; i, inter-villous cavity


filled with maternal blood; L., Langhan's cells (cytotrophoblast); m., mesoderm of the
filled with maternal blood; L., Langhan's cells (cytotrophoblast); m., mesoderm of the
serosa; s., syncitial layer (plasmotrophoblast); v.f.. fixation or anchoring villus.
serosa; s., syncitial layer (plasmotrophoblast); v.f.. fixation or anchoring villus.


only maternal tissue which is lost is uterine blood and a small amount
only maternal tissue which is lost is uterine blood and a small amount
Line 9,569: Line 8,842:
only one umbilical cord, but the two placentae are connected by blood
only one umbilical cord, but the two placentae are connected by blood
vessels. In the orang and gibbon there is a single placenta. The lower
vessels. In the orang and gibbon there is a single placenta. The lower
monkeys have no decidua reflexa.
monkeys have no decidua reflexa.


The following outline lists the characteristics of the embryonic
The following outline lists the characteristics of the embryonic
Line 9,595: Line 8,868:
Large well-developed, but
Large well-developed, but


contains no yolk No extra-
contains no yolk No extraembryonic coelome in
embryonic coelome in
blastoderm opposite embryo During uterine life
blastoderm opposite em-
bryo During uterine life
there is yolk sac placenta
there is yolk sac placenta
with exception of Pera—
with exception of Pera—
Line 9,610: Line 8,881:
Aiimion
Aiimion


Has sero—amniotic connec-
Has sero—amniotic connection and is probably
tion and is probably
formed :13 in Sauropeida
formed :13 in Sauropeida


Probably formed by folds
Probably formed by folds


Inner cell mass moves up-
Inner cell mass moves upward pushing trophoblast
ward pushing trophoblast
away The folds from edge
away The folds from edge
of embryonic shield form
of embryonic shield form
Line 9,634: Line 8,903:
As in artiodact) ls
As in artiodact) ls


Large amnion of Orca ob-
Large amnion of Orca obIiteratc-s exttaembry onic
Iiteratc-s exttaembry onic
cavity
cavity


Amnion obliterates extra-
Amnion obliterates extra
 
embryonic coelome in Elephas
embryonic coelome in Ele-
phas


ALLANTOIB
ALLANTOIB
Line 9,655: Line 8,921:
inches long has allantoia 2
inches long has allantoia 2
feet long Hippomanea in
feet long Hippomanea in
allantoic fluid
allantoic fluid


As in artiodactyls
As in artiodactyls
Line 9,661: Line 8,927:
In Halicore is large. as in
In Halicore is large. as in
8|’tl0d8.Cl.\lS Hippomanea
8|’tl0d8.Cl.\lS Hippomanea
in allantoic fluid
in allantoic fluid


PLACENTA
PLACENTA
Line 9,676: Line 8,942:


Oviparoifa egga with hard
Oviparoifa egga with hard
shell Young fed milky se-
shell Young fed milky secretion from primitive abdominal mammary glands
cretion from primitive ab-
dominal mammary glands


Series of forms through
Series of forms through
Line 9,686: Line 8,950:
yolk sac and allantoia
yolk sac and allantoia


.\on—deciduate Most ru-
.\on—deciduate Most ruminants cotyledonary
minants cotyledonary
Pig diffuse unbranched
Pig diffuse unbranched
villi Deer hippopotamus
villi Deer hippopotamus
earrel, girafle intermedi-
earrel, girafle intermediate
ate


l\on-deciduate placenta
l\on-deciduate placenta
Hfirse branched difiused
Hfirse branched difiused
V] l
V] l


Line 9,701: Line 8,963:


‘Ion-deciduate W itli
‘Ion-deciduate W itli
branched difiuae villi ar-
branched difiuae villi arranged in band around
ranged in band around
tropboblast (Really zonary non-deciduate )
tropboblast (Really zon-
ary non-deciduate )


fuse villi \ot classified
fuse villi \ot classified
yet as to deciduate or non-
yet as to deciduate or nondeciduate but villi seem to
deciduate but villi seem to
be like those of articdactyls
be like those of artic-
dactyls


Central implantation
Central implantation
Line 9,717: Line 8,975:
described
described


Zonary placenta Vlltll dif-
Zonary placenta Vlltll dif
 
Embryology not Sufi
Embryology not Sufi-
 
ciently investigated
ciently investigated


Line 9,746: Line 9,002:
Disappears
Disappears


Large Invagination of up-
Large Invagination of upper wall gives apparent inversion of germ layers
per wall gives apparent in-
version of germ layers


Lpper wall acts as acces-
Lpper wall acts as accessory placenta That of rabbits is more important nutn tive organ than allant ois
sory placenta That of rab-
bits is more important nu-
tn tive organ than allant ois


Functional onl
Functional onl
Line 9,760: Line 9,011:


in early
in early
by allian-
by allian
 
Large Yolk sac placenta
Large Yolk sac placenta
formed in Tupaija Meso-
formed in Tupaija Mesoderm restricted to upper
derm restricted to upper
wall in Talpa and Sore:
wall in Talpa and Sore:
Persists until birth
Persists until birth
Line 9,773: Line 9,022:
folds
folds


Large amniotic cavity ob-
Large amniotic cavity oblitcrating extraembryonic
litcrating extraembryonic
coelomc
coelomc


folds formed after embry-
folds formed after embryonic shield has taken superficial place on blastoderm
onic shield has taken super-
ficial place on blastoderm
\/louse, rat giunea pig
\/louse, rat giunea pig
closed sac inside inner cell
closed sac inside inner cell
mass
mass


Vespertillw confluence of
Vespertillw confluence of
irregular spaces in embry-
irregular spaces in embryonic knob forms amnion
onic knob forms amnion


Extremely large Grown
Extremely large Grown
between 5 olk sac and troph-
between 5 olk sac and trophoblast completely lining serosa
oblast completely lin-
ing serosa


Small
Small


Often small and endo-
Often small and endoderm does not grow out
derm does not grow out
beyond body as in mouse
beyond body as in mouse
and giinea pig
and giinea pig
Line 9,803: Line 9,045:


Hedgehog forms a closed Groves out prominently
Hedgehog forms a closed Groves out prominently
cavity in embryonic knob dwarfing yolk sac
cavity in embryonic knob dwarfing yolk sac


Talpa Sore: Tupaua
Talpa Sore: Tupaua
formed by folds
formed by folds


Small yolk sac early dis-
Small yolk sac early disappears (Tarnus small
appears (Tarnus small
vascular)
vascular)


Line 9,821: Line 9,062:
inner cell mass
inner cell mass


Very large fills extraem-
Very large fills extraembryonic space Tarsms
bryonic space Tarsms
small outgrowth of gut remains in base of umbilical
small outgrowth of gut re-
mains in base of umbilical
cord
cord


Line 9,834: Line 9,073:
Zonary deciduate
Zonary deciduate


May be zonary oval bell-
May be zonary oval bellshaped or difluse Marius
shaped or difluse Marius
non-decidiiate with simple
non-decidiiate with simple
diffuse villi Tatusm mod-
diffuse villi Tatusm modfied discoidal deciduate
fied discoidal deciduate


Discoidal deciduate
Discoidal deciduate
Line 9,846: Line 9,083:
shaped or bell shaped
shaped or bell shaped


Discoidal deciduate usu-
Discoidal deciduate usuallv concave In hedgehog
allv concave In hedgehog
is decidua reflexa like that
is decidua reflexa like that
of man but formed differently In mole acontradeciduate condition (allantoic capillaries separated at birth from placental trophoblast which
of man but formed differ-
ently In mole acontra-
deciduate condition (all-
antoic capillaries separ-
ated at birth from pla-
cental trophoblast which
is absorbed by uterine
is absorbed by uterine
walls)
walls)


Non-deciduate diffuse
Non-deciduate diffuse
(Tarsius discoidal decidu-
(Tarsius discoidal deciduate)
ate)


Deciduate. discoidal
Deciduate. discoidal
Line 9,866: Line 9,096:
Central implantation
Central implantation


Little known about mem-
Little known about mem
 
branes of edentates Central implantation in Ta!usm
branes of edentates Cen-
tral implantation in Ta!-
usm


Implantation is central in
Implantation is central in
Line 9,917: Line 9,144:


X =0ccurrence in
X =0ccurrence in
Smaller Divi-
Smaller Divisions of Phyla
sions of Phyla


Larval Forms
Larval Forms
Line 9,994: Line 9,220:
Hex
Hex


afiéjé xx _T
afiéjé xx _T
Hex
Hex


Line 10,004: Line 9,230:
He x x__
He x x__


akatéxxxxfié
akatéxxxxfié


. -— *  
. -— *  
lak fie s ' I l\Iu1ler 5, Sporocyst, l\I1nc1d:um, Cysticel--
lak fie s ' I l\Iu1ler 5, Sporocyst, l\I1nc1d:um, Cysticel-
 
‘ cug. Pilzajum, Redia. Cercaria. Larva of
‘ cug. Pilzajum, Redia. Cercaria. Larva of
Depot
Depot
Line 10,047: Line 9,272:


X
X
iexv-flex
iexv-flex


   
   
Line 10,175: Line 9,400:
Scorpionida. . . .
Scorpionida. . . .


Chordata . . . . . . . . . . fié
Chordata . . . . . . . . . . fié
Enteropncusta
Enteropncusta
Tumcata . . .
Tumcata . . .
Line 10,222: Line 9,447:
Tadpole and others
Tadpole and others


#xx fixxxxxxxxxx
#xx fixxxxxxxxxx
#xxx
#xxx


Line 10,249: Line 9,474:
APPENDIX TO PART ONE
APPENDIX TO PART ONE


TABLE OF ANIMAL CLASSIFICATION INCLUDING EXAMPLES OF
TABLE OF ANIMAL CLASSIfiCATION INCLUDING EXAMPLES OF


EMBRYOLOGICAL SIGNIFICANCE
EMBRYOLOGICAL SIGNIfiCANCE


(None: This table does not include the forms listed in certain chapters in
(None: This table does not include the forms listed in certain chapters in
Line 10,302: Line 9,527:


Order 6. Siphonophors.
Order 6. Siphonophors.
Physophom, Nanomia, Diphyes, Physalia, Porpita, Velella, Hali-
Physophom, Nanomia, Diphyes, Physalia, Porpita, Velella, Halistemma
stemma


Class 2. Scyphozoa.
Class 2. Scyphozoa.
Line 10,312: Line 9,536:
Order 2. Peromedusae
Order 2. Peromedusae
Pericolpa, Periphylla
Pericolpa, Periphylla
ANIMAL CLASSIFICATION 261
ANIMAL CLASSIfiCATION 261


Order 3. Cubomedusae
Order 3. Cubomedusae
Line 10,318: Line 9,542:


Order 4. Discomcdusae
Order 4. Discomcdusae
Aurelia, Pelagia, Cassiopea, Cg/anea, Ulmaria, Stomolophus, Poly-
Aurelia, Pelagia, Cassiopea, Cg/anea, Ulmaria, Stomolophus, Polyclonia
clonia


Class 3. Anthozoa (Actinozoa)
Class 3. Anthozoa (Actinozoa)
Line 10,347: Line 9,570:


Order 3. Madreporaria
Order 3. Madreporaria
Sclerophylla, Oculi/La, Aslrangirc, Aslrca, Faira, Fungia, Madre-
Sclerophylla, Oculi/La, Aslrangirc, Aslrca, Faira, Fungia, Madrepora, Porites, Astroides, Mcandrina
pora, Porites, Astroides, Mcandrina


Order 4. Antipatharia
Order 4. Antipatharia
Line 10,370: Line 9,592:


Order 2. Tricladida
Order 2. Tricladida
Poly/scelis, Planaria, Dendrocoelzmz, Bipalizzm, I2’(.’elloum, Gunda, Poly-
Poly/scelis, Planaria, Dendrocoelzmz, Bipalizzm, I2’(.’elloum, Gunda, Poly
 
chaerus, Syncoelidium, Phagocata
chaerus, Syncoelidium, Phagocata
Order 3. Polycladida
Order 3. Polycladida
Line 10,383: Line 9,604:
Order 2. Digenea (Distomeae)
Order 2. Digenea (Distomeae)


Distomum (Fasciolaria), Monostomum, Bilharzia, Clonorchis, Paragon-
Distomum (Fasciolaria), Monostomum, Bilharzia, Clonorchis, Paragonimus
imus


Class 3. Cestoda.
Class 3. Cestoda.
Line 10,404: Line 9,624:


Class 1. Nematoda
Class 1. Nematoda
Ascaris, Ancylostoma, Trichinella, Filaria
Ascaris, Ancylostoma, Trichinella, filaria


Class 2. Gordiacea
Class 2. Gordiacea
Line 10,434: Line 9,654:


Order 1. Gymnolaemata
Order 1. Gymnolaemata
Gemmellaria, Bugula, Flustra, Flustrella, Eschara, Crisia, Tubulipora,
Gemmellaria, Bugula, flustra, flustrella, Eschara, Crisia, Tubulipora,
Alcyanidium, Valkeria, Paludicella
Alcyanidium, Valkeria, Paludicella
Order 2. Phylactolaemata.
Order 2. Phylactolaemata.
Line 10,441: Line 9,661:


Terebratula, Terebratulina, Lingula, Waldheimia, Rhynchonella
Terebratula, Terebratulina, Lingula, Waldheimia, Rhynchonella
ANIMAL CLASSIFICATION 263
ANIMAL CLASSIfiCATION 263


Supplementary group of uncertain position, showing some relations to En-
Supplementary group of uncertain position, showing some relations to Entero pneusta:
tero pneusta:


Pterobranchia
Pterobranchia
Line 10,456: Line 9,675:
Subclass 1. Polychaeta
Subclass 1. Polychaeta
Order 1. Phanerocephala
Order 1. Phanerocephala
Nereis, Podarke, Aphrodite, Lepidonotus, Autolytus, Polymie, Dio-
Nereis, Podarke, Aphrodite, Lepidonotus, Autolytus, Polymie, Diopatra, N othria, Eunice, Syllis, Trypanosyllis
patra, N othria, Eunice, Syllis, Trypanosyllis
Order 2. Cryptocephala
Order 2. Cryptocephala
Eupomatus, Hydroides, Spiroides, Arenicola, Amphitrite, Terebella,
Eupomatus, Hydroides, Spiroides, Arenicola, Amphitrite, Terebella,
Line 10,479: Line 9,697:
Ophiura, Ophiothrzlt, Ophiopholis, Amphiura, Astrophyton
Ophiura, Ophiothrzlt, Ophiopholis, Amphiura, Astrophyton
Class 3. Echinoidea
Class 3. Echinoidea
Cidaris, Arbacia, Toxapneustes, Strcmgylocentrotus, Coelopleurus, Spawn-
Cidaris, Arbacia, Toxapneustes, Strcmgylocentrotus, Coelopleurus, Spawngus, Echinocardium, Brissus, Echinarachnius, Clypeasler, M ellita
gus, Echinocardium, Brissus, Echinarachnius, Clypeasler, M ellita
Class 4. Holothuroidea
Class 4. Holothuroidea
Holothuria, Cucumaria, Psolus, Thyone, Caudina, M olpadia, Synapta
Holothuria, Cucumaria, Psolus, Thyone, Caudina, M olpadia, Synapta
Line 10,500: Line 9,717:
N ucula, Leda, Yoldia, Solenomya
N ucula, Leda, Yoldia, Solenomya


Order 2. Filibranchia
Order 2. filibranchia
Arca, M ytilus, M odiola, Anemia, Trigonia
Arca, M ytilus, M odiola, Anemia, Trigonia


Line 10,519: Line 9,736:
Suborder 2. Pectinibranchia
Suborder 2. Pectinibranchia


Littorina, Strombus, Sycotypus, Busycon (Fulgur), Crepidula, Urosal-
Littorina, Strombus, Sycotypus, Busycon (Fulgur), Crepidula, Urosalpinx, Murex, Paludina, Carinaria, Pleurobranchidimn
pinx, Murex, Paludina, Carinaria, Pleurobranchidimn


Order 2. Opisthobranchia
Order 2. Opisthobranchia
Line 10,530: Line 9,746:
Suborder 3. N udibranchia
Suborder 3. N udibranchia


Doris, Asolidia, Fiona, Staurodoris
Doris, Asolidia, fiona, Staurodoris


Order 3. Pulmonata
Order 3. Pulmonata
Line 10,554: Line 9,770:
Suborder 1. Branchiopoda
Suborder 1. Branchiopoda
Branchipus, Artemia, Apus
Branchipus, Artemia, Apus
ANIMAL CLASSIFICATION 265
ANIMAL CLASSIfiCATION 265


Suborder 2. Cladocera
Suborder 2. Cladocera
Line 10,627: Line 9,843:
Class 4. Insecta.
Class 4. Insecta.
Macrotoma, 9. thysanuran; Hydrophilus, the water beetle; M iastor, the
Macrotoma, 9. thysanuran; Hydrophilus, the water beetle; M iastor, the
fly; Leptinotarsa, the potato beetle; Copidosoma, parasitic hvmenoptera
fly; Leptinotarsa, the potato beetle; Copidosoma, parasitic hvmenoptera
Class 5. Arachnida
Class 5. Arachnida
Order 1. Araneida
Order 1. Araneida
Line 10,665: Line 9,881:
Balanoglossus, Dol2'choglossu.s, Ilarrimania
Balanoglossus, Dol2'choglossu.s, Ilarrimania
Subphylum 2. Tunicata
Subphylum 2. Tunicata
Cynthia, (Hana, Molgula, Appcndicularia, Distaplia, Botryllus, Salpa, Pyro-
Cynthia, (Hana, Molgula, Appcndicularia, Distaplia, Botryllus, Salpa, Pyrosoma, Doliolum
soma, Doliolum
Subphylum 3. Cephalochordata
Subphylum 3. Cephalochordata
Amphioxus, Branchiostoma
Amphioxus, Branchiostoma
Line 10,679: Line 9,894:
Subclass 1. Elasmobranchii
Subclass 1. Elasmobranchii
Superorder 1. Selachii
Superorder 1. Selachii
Squalus, M ustelus, Galeus, Raia, Acanthias, Scyllium, Car-
Squalus, M ustelus, Galeus, Raia, Acanthias, Scyllium, Carcharias, Cestracion, H exanchus, N otodanus, Pristiurus, Torpedo
charias, Cestracion, H exanchus, N otodanus, Pristiurus, Torpedo
ANIMAL CLASSIfiCATION 267
ANIMAL CLASSIFICATION 267


Superordcr 2. Holocephali
Superordcr 2. Holocephali
Line 10,709: Line 9,923:
Farm. 4. Salmnandridac
Farm. 4. Salmnandridac


Ambystoma (Amblystoma, Siredon), Diemyctylus, Salaman-
Ambystoma (Amblystoma, Siredon), Diemyctylus, Salamandra, Triton, Plcthmlon, Eurycea (Hpelerpes), Desmognathus
dra, Triton, Plcthmlon, Eurycea (Hpelerpes), Desmognathus


Order 3. Anura
Order 3. Anura
Line 10,759: Line 9,972:
Vespertilio, Pteropus, Desmodus, M yotis
Vespertilio, Pteropus, Desmodus, M yotis
Order 4. Carnivore.
Order 4. Carnivore.
Suborder 1. Fissipedia.
Suborder 1. fissipedia.
Canis, Hyaemz, Procyon, Felis
Canis, Hyaemz, Procyon, Felis
Suborder 2. Pinnipedia.
Suborder 2. Pinnipedia.
Line 10,804: Line 10,017:
cause of much controversy, at least as regards certain of its aspects.
cause of much controversy, at least as regards certain of its aspects.
There are really three important phases of the problem; the place of
There are really three important phases of the problem; the place of
origin of the germ cells, the path of their migration to the definitive
origin of the germ cells, the path of their migration to the definitive
gonads, and the subsequent history after reaching the germ glands.
gonads, and the subsequent history after reaching the germ glands.


Line 10,827: Line 10,040:
In 1880 Nussbaum, as a result of his observations on the development
In 1880 Nussbaum, as a result of his observations on the development
of the trout and the frog, reached the conclusion that the germ cells
of the trout and the frog, reached the conclusion that the germ cells
were of blastomeric origin, being segregated in the early stages of de-
were of blastomeric origin, being segregated in the early stages of deVelopment in a region outside that which will see the formation of the
Velopment in a region outside that which will see the formation of the
embryonic body. They actively migrate or else are carried into the
embryonic body. They actively migrate or else are carried into the
body proper and into the germ gland by the growth forces which operate
body proper and into the germ gland by the growth forces which operate
Line 10,845: Line 10,057:
Swift, 1914, 1915, 1916; Jordan, 1917; Okkelberg, 1921; Richards and
Swift, 1914, 1915, 1916; Jordan, 1917; Okkelberg, 1921; Richards and
Thompson, 1921; Swingle, 1926; Hahn, 1927) have failed to reveal any
Thompson, 1921; Swingle, 1926; Hahn, 1927) have failed to reveal any
conditions not in accord with Nussbaum’s theory. It has been demon-
conditions not in accord with Nussbaum’s theory. It has been demonstrated that the primordial germ cells arise widely scattered in the
strated that the primordial germ cells arise widely scattered in the


   
   
Line 10,868: Line 10,079:
VERTEBRATES 273
VERTEBRATES 273


the formation of the axial region of the body brings about the trans-
the formation of the axial region of the body brings about the translocation of the germ cells as well as the somatic cells. Along the path
location of the germ cells as well as the somatic cells. Along the path
of migration there is no difficulty in recognizing the germ cells for they
of migration there is no difficulty in recognizing the germ cells for they
have clearly marked characteristics. On these points there is rather
have clearly marked characteristics. On these points there is rather
Line 10,878: Line 10,088:
investigators claim that some of these. cells never find their way into
investigators claim that some of these. cells never find their way into
the gonad, but undergo degeneration in various parts of the body.
the gonad, but undergo degeneration in various parts of the body.
Some (Firket, von Berenberg—Gossler, Ilargitt, and others) claim also
Some (firket, von Berenberg—Gossler, Ilargitt, and others) claim also
that the primordial cells which may have arrived in the gonad by
that the primordial cells which may have arrived in the gonad by


   
   


Flu. 183. 'l‘rans\'(-rse section through the hind gut of l).l—mm. larva of Amid crzlva.
flu. 183. 'l‘rans\'(-rse section through the hind gut of l).l—mm. larva of Amid crzlva.
(After Allen.)
(After Allen.)


coel., coelomie cavity; gut end., gut endodorm; mes., mesentery; s.e., sex cells; Wolfi’.d..
coel., coelomie cavity; gut end., gut endodorm; mes., mesentery; s.e., sex cells; Wolfi’.d..
Wolffian duct.
Wolffian duct.


migration in the manner indicated _do not actually give rise to the
migration in the manner indicated _do not actually give rise to the
definitive germ cells, for they find degeneration of these cells along
definitive germ cells, for they find degeneration of these cells along
with proliferation of a second group of germ cells derived directly from
with proliferation of a second group of germ cells derived directly from
the genital epithelium. These latter, or even in certain cases a third
the genital epithelium. These latter, or even in certain cases a third
proliferation, are the source of the definitive germ cells. The primordial
proliferation, are the source of the definitive germ cells. The primordial
germ cells in these cases may pass far through their cycle before de-
germ cells in these cases may pass far through their cycle before degenerating, as shown by Kingery for the mouse and Swinglc for the
generating, as shown by Kingery for the mouse and Swinglc for the
tadpole, in both of which the maturation cycle is practically completed
tadpole, in both of which the maturation cycle is practically completed
before the degeneration occurs.
before the degeneration occurs.


In a recent account Swingle has reviewed the progress of the investi-
In a recent account Swingle has reviewed the progress of the investigations on the Anura, He has shown from embryological studies that
gations on the Anura, He has shown from embryological studies that
there are in various parts of the United States “local races which differ
there are in various parts of the United States “local races which differ
274 THE ORIGIN AND DEVELOPMENT OF GERM CELLS
274 THE ORIGIN AND DEVELOPMENT OF GERM CELLS


markedly in regard to the time of occurrence and character of the
markedly in regard to the time of occurrence and character of the
developmental processes involved in the formation of the definitive
developmental processes involved in the formation of the definitive
testes.” He is convinced that the sex cells appear first in the endoderm,
testes.” He is convinced that the sex cells appear first in the endoderm,
and give origin to those cells which produce ripe sex products. Every
and give origin to those cells which produce ripe sex products. Every
stage from the origin of the primordial sex cells to the fully developed
stage from the origin of the primordial sex cells to the fully developed
Line 10,914: Line 10,122:
urocleles from differentiated mesoderm, the peritoneum. Swingle sug—
urocleles from differentiated mesoderm, the peritoneum. Swingle sug—
gests that the discrepancy is due to an origin and segregation earlier
gests that the discrepancy is due to an origin and segregation earlier
than their appearance in the peritoneum, and that after their segrega-
than their appearance in the peritoneum, and that after their segregation they wait in the layer where they are later seen for an appropriate
tion they wait in the layer where they are later seen for an appropriate
time for development. This is in agreement with his finding that local
time for development. This is in agreement with his finding that local
races differ in the time of development of the sex cells. In the urodeles
races differ in the time of development of the sex cells. In the urodeles
they are incorporated in the mesoderm in an early stage whereas in
they are incorporated in the mesoderm in an early stage whereas in
Line 10,923: Line 10,130:
the one or the other.
the one or the other.


It is to be noted that none of the writers who find degeneration have
It is to be noted that none of the writers who find degeneration have
satisfactorily proven that all the primordial germ cells degenerate or
satisfactorily proven that all the primordial germ cells degenerate or
that none of them are left to produce definitive germ cells. It is also
that none of them are left to produce definitive germ cells. It is also
noteworthy that recently certain evidence has been found which in-
noteworthy that recently certain evidence has been found which indicates that in an ordinary course of events the definitive germ cells are
dicates that in an ordinary course of events the definitive germ cells are
derived from the primordial cells. However, owing to the power of
derived from the primordial cells. However, owing to the power of
regulation which animals possess under the stress of unusual and harm-
regulation which animals possess under the stress of unusual and harmful circumstances which bring about the degeneration of the primordial
ful circumstances which bring about the degeneration of the primordial
cells, secondary sex cells may be proliferated from the germinal epithelium and produce the definite sperms or ova. At the present time the
cells, secondary sex cells may be proliferated from the germinal epi-
thelium and produce the definite sperms or ova. At the present time the
safest interpretation seems to be that as a rule the primordial germ
safest interpretation seems to be that as a rule the primordial germ
cells thus early segregated in the vertebrates give rise to the definitive
cells thus early segregated in the vertebrates give rise to the definitive
germ cells, but that in exceptional cases, where the regular events are
germ cells, but that in exceptional cases, where the regular events are
interrupted and the primordial cells so disturbed as to cause their
interrupted and the primordial cells so disturbed as to cause their
degeneration, the organism responds by proliferating from the germinal
degeneration, the organism responds by proliferating from the germinal
epithelium new cells which take their place. It must never be forgotten
epithelium new cells which take their place. It must never be forgotten
that the chief characteristic of protoplasm, especially embryonic proto-
that the chief characteristic of protoplasm, especially embryonic protoplasm, is its plasticity, its power of regulation and of adaptation to new
plasm, is its plasticity, its power of regulation and of adaptation to new
conditions. “Life is a constant adjustment of internal and external
conditions. “Life is a constant adjustment of internal and external
conditions.”
conditions.”
Line 10,946: Line 10,149:
Although the matter is still involved in controversy, some important
Although the matter is still involved in controversy, some important
theoretical conclusions have already resulted from the investigations.
theoretical conclusions have already resulted from the investigations.
First of all, it is an obvious fact of major importance that heredity is
first of all, it is an obvious fact of major importance that heredity is
a matter of germ cells, and that the germ cells contain organized material
a matter of germ cells, and that the germ cells contain organized material
THE INVERTEBRATES 275
THE INVERTEBRATES 275
Line 10,954: Line 10,157:
is there continuity of germ cells but of the organized system (germ
is there continuity of germ cells but of the organized system (germ
plasm) which they convey. Secondly, the distinction between germ cells
plasm) which they convey. Secondly, the distinction between germ cells
and somatic cells is often more or less artificial and has in many cases
and somatic cells is often more or less artificial and has in many cases
been emphasized unduly. Weismann himself spoke with less certainty
been emphasized unduly. Weismann himself spoke with less certainty
about the continuity of germ plasm than many of his followers have
about the continuity of germ plasm than many of his followers have
Line 10,982: Line 10,185:
soma one of cytoplasmic specialization. The general problem of the
soma one of cytoplasmic specialization. The general problem of the
germ-cell cycle is thus given its proper place as one of embryology,
germ-cell cycle is thus given its proper place as one of embryology,
where it is of great interest, and it is no longer one of theoretical signifi-
where it is of great interest, and it is no longer one of theoretical significance to geneticists.
cance to geneticists.


B. THE INVERTEBRATES
B. THE INVERTEBRATES


In the invertebrates there are many forms in which no suchMun-
In the invertebrates there are many forms in which no suchMuncertainty prevails as in the case of the vertebrates. There are two chief
certainty prevails as in the case of the vertebrates. There are two chief
methods by which germ path is recognizable: 1.e., chromatin diminution
methods by which germ path is recognizable: 1.e., chromatin diminution
and germ-cell determinants. There are of course many cases in which
and germ-cell determinants. There are of course many cases in which
Line 10,994: Line 10,195:
in several groups of the invertebrates cases in which the germ path
in several groups of the invertebrates cases in which the germ path
(Keimbahn) has been-worked out in practical completeness. In the
(Keimbahn) has been-worked out in practical completeness. In the
coelenterates primordial germ cells were found by Weismann, Kleinen-
coelenterates primordial germ cells were found by Weismann, Kleinen276 THE ORIGIN AND DEVELOPMENT OF GERM CELLS
276 THE ORIGIN AND DEVELOPMENT OF GERM CELLS


berg, and others in a wandering condition early in the development
berg, and others in a wandering condition early in the development
Line 11,002: Line 10,202:
are recognizable long before the sexual individuals appear. The case
are recognizable long before the sexual individuals appear. The case


FIG. 184. The dexelopment of the germ cells of Sagilta. (After Elpatiewsky.)
fiG. 184. The dexelopment of the germ cells of Sagilta. (After Elpatiewsky.)


A, fertilized egg showimz the “germ cell determinant,” B, 2-cell stage, germ cell de-
A, fertilized egg showimz the “germ cell determinant,” B, 2-cell stage, germ cell determinant in one blastomere only; (‘, H—cell stage; D, szastrula with two primordial germ
terminant in one blastomere only; (‘, H—cell stage; D, szastrula with two primordial germ
cells. '
cells. '


Line 11,017: Line 10,216:
'rm«: INVERTEBRATES 277
'rm«: INVERTEBRATES 277


FIG 185 Early stages In the development of Cyclops fuscus (After Amma)
fiG 185 Early stages In the development of Cyclops fuscus (After Amma)


A, first cleavage nucleus, 13, (laughter nuelex reconstructed with the ectosomes or germ
A, first cleavage nucleus, 13, (laughter nuelex reconstructed with the ectosomes or germ
cell determrnants 1n one blastomere only, 0, second elenvage dnmon wrth the germ cell
cell determrnants 1n one blastomere only, 0, second elenvage dnmon wrth the germ cell
determmants agmn l1m1ted to one blmtomere, D, l()-cell stage All the blustomeres m the
determmants agmn l1m1ted to one blmtomere, D, l()-cell stage All the blustomeres m the
Line 11,028: Line 10,227:


of these cells has been fully described by Boveri. They are distinguishable
of these cells has been fully described by Boveri. They are distinguishable
by means of a process known as chromatin diminution, part of the chro-
by means of a process known as chromatin diminution, part of the chromatin (the thick ends of the chromosomes) of the somatic cell being
matin (the thick ends of the chromosomes) of the somatic cell being
cast from the nucleus into the cytoplasm, because of which process the
cast from the nucleus into the cytoplasm, because of which process the


1
1


FIG. 186 A, longitudinal section through an oocyte of M iastor americami. (After Hegncr )
fiG. 186 A, longitudinal section through an oocyte of M iastor americami. (After Hegncr )


n c , nurse chamber, g v . germinal vesicle, p Pl , pole plusm, f ep , follicular epithelium
n c , nurse chamber, g v . germinal vesicle, p Pl , pole plusm, f ep , follicular epithelium
B, later stage of same in which somatic cells are beginning to form and blastoderm and
B, later stage of same in which somatic cells are beginning to form and blastoderm and
the two pl'll‘flB.!’y germ cells containing the pole plasm are already cut of?
the two pl'll‘flB.!’y germ cells containing the pole plasm are already cut of?


somatic nuclei in subsequent cell generations are both lighter in color
somatic nuclei in subsequent cell generations are both lighter in color
and smaller than the germ cells. All the chromatin of the stem cell is
and smaller than the germ cells. All the chromatin of the stem cell is
retained in this second division, but of the daughter blastomeres pro-
retained in this second division, but of the daughter blastomeres produced from it, one undergoes the diminution process while the other
duced from it, one undergoes the diminution process while the other
divides directly in the regular manner and becomes again a stem cell.
divides directly in the regular manner and becomes again a stem cell.
Of the products of its division the same relation holds, for the process
Of the products of its division the same relation holds, for the process
Line 11,049: Line 10,246:


is repeated four times. Thus, at the end of the fourth cleavage there
is repeated four times. Thus, at the end of the fourth cleavage there
are fifteen somatic cells (which will give rise only to somatic cells
are fifteen somatic cells (which will give rise only to somatic cells
ordinarily) and one cell which is the primoridal germ cell and the
ordinarily) and one cell which is the primoridal germ cell and the
ancestor of all the germ cells. At the next division this divides again
ancestor of all the germ cells. At the next division this divides again


Fm. 187. Continuation of Fig. 186. A, similar stage of eight germ cells, blastoderm
Fm. 187. Continuation of fig. 186. A, similar stage of eight germ cells, blastoderm
complete; B, sagittal section through embryo with eight germ cells near the end of the
complete; B, sagittal section through embryo with eight germ cells near the end of the
tail fold.
tail fold.
Line 11,062: Line 10,259:
In Sagitta, Elpatiewsky recognized in the fertilized egg a structure,
In Sagitta, Elpatiewsky recognized in the fertilized egg a structure,
called a “germ-cell determinant,” which does not divide with the egg.
called a “germ-cell determinant,” which does not divide with the egg.
(Fig. 184.) The blastomere containing it becomes a stem cell. In the fifth
(fig. 184.) The blastomere containing it becomes a stem cell. In the fifth
division the stem cell produces a somatic cell and a primordial germ cell.
division the stem cell produces a somatic cell and a primordial germ cell.
280 THE ORIGIN AND DEVELOPMENT OF GERM CELLS
280 THE ORIGIN AND DEVELOPMENT OF GERM CELLS
Line 11,068: Line 10,265:
In an early gastrula four cells have resulted
In an early gastrula four cells have resulted
from two divisions of the primordial cell. The
from two divisions of the primordial cell. The
subsequent divisions of the four are respon-
subsequent divisions of the four are responsible for the formation of both male and female
sible for the formation of both male and female
germ cells (for the animal is hermaphroditic).
germ cells (for the animal is hermaphroditic).
It is said that the two anterior give rise to
It is said that the two anterior give rise to
Line 11,076: Line 10,272:
Among the arthropods there are many cases
Among the arthropods there are many cases
of the early segregation of germ cells, and their
of the early segregation of germ cells, and their
recognition is possible either through cyto-
recognition is possible either through cytoplasinic inclusions (germ-cell determinants) or
plasinic inclusions (germ-cell determinants) or
by distinctive characteristics, particularly
by distinctive characteristics, particularly
chromatin diminution. In the Entomostraea
chromatin diminution. In the Entomostraea
Line 11,084: Line 10,279:
stem cells are distinguished from the first
stem cells are distinguished from the first
cleavage onwards. In the unsegmented egg
cleavage onwards. In the unsegmented egg
of (71/claps (Fig. 185) certain granules (ecto-
of (71/claps (fig. 185) certain granules (ectosomes) are to be found accumulating at one
somes) are to be found accumulating at one
pole of the spindle as the cleavage mitosis
pole of the spindle as the cleavage mitosis
advances. These granules are thus segre-
advances. These granules are thus segregated into one of the
gated into one of the
blastomeres which becomes the stem cell.
blastomeres which be-
comes the stem cell.
This process continues
This process continues
through the fourth divi-
through the fourth division and results in the
sion and results in the
segregation of the primordial germ cells.
segregation of the primordial germ cells.


Line 11,119: Line 10,310:
is variously called, are present in the uncleaved
is variously called, are present in the uncleaved
egg and enter the pole cells. In addition to this
egg and enter the pole cells. In addition to this
in M iastor (Figs. 186, 187) the pole cells are pro-
in M iastor (figs. 186, 187) the pole cells are provided with two nuelei from the third cleavage
vided with two nuelei from the third cleavage
which have not undergone chromatin diminution
which have not undergone chromatin diminution
as distinguished from the other six. In the Hy-
as distinguished from the other six. In the Hymenoptera. (fig. 188) an “oosome” is present in
menoptera. (Fig. 188) an “oosome” is present in


FIG. 189. Longitudi-
fiG. 189. Longitudinal section through the
nal section through the
egg of Leptinotarsa drmlvnlirieata. (After Hegner.) The'posterior end
egg of Leptinotarsa dr-
mlvnlirieata. (After Heg-
ner.) The'posterior end
was killed with :1. hot
was killed with :1. hot
needle just after the
needle just after the
Line 11,136: Line 10,322:
develop for 24 hours.
develop for 24 hours.
bl., blastoderm; g.c.d.,
bl., blastoderm; g.c.d.,
germ cell determi-
germ cell determinants; k.. portion of
nants; k.. portion of
the egg killed.
the egg killed.
THE INVERTEBRATES 281
THE INVERTEBRATES 281


the unscgmented egg which in the 4—eell stage becomes associated at
the unscgmented egg which in the 4—eell stage becomes associated at
the posterior end with the forming primordial germ cells. Finally, in the
the posterior end with the forming primordial germ cells. finally, in the
chrysomelid beetles (Fig. 189), Hegner found a “polar disc” composed
chrysomelid beetles (fig. 189), Hegner found a “polar disc” composed
of germ-cell determinants which participate in the formation of the
of germ-cell determinants which participate in the formation of the
primordial germ cells. This relationship was made more certain by an
primordial germ cells. This relationship was made more certain by an
experiment which he performed. With a hot needle he killed the poste-
experiment which he performed. With a hot needle he killed the posterior end of the egg, l)ut allowed the remainder of the egg to develop. A
rior end of the egg, l)ut allowed the remainder of the egg to develop. A
blastoderm was formed which was normal in every particular (up to
blastoderm was formed which was normal in every particular (up to
a certain stage) except that it was entirely lacking in germ cells.
a certain stage) except that it was entirely lacking in germ cells.
Line 11,162: Line 10,346:
GERM-LAYER THEORY
GERM-LAYER THEORY


It will be recalled that the old issue between preformation and epi-
It will be recalled that the old issue between preformation and epigenesis finally resulted in the overthrow of the cruder type of preforn1ation which held that development was simply an unfolding of parts
genesis finally resulted in the overthrow of the cruder type of preforn1a-
tion which held that development was simply an unfolding of parts
already existing in egg or sperm. As better understanding of the facts of
already existing in egg or sperm. As better understanding of the facts of
development was obtained it became clear that, although preformation
development was obtained it became clear that, although preformation
did not occur, there were definite signs of organization within the egg.
did not occur, there were definite signs of organization within the egg.
The developing organs could be traced farther and farther back until
The developing organs could be traced farther and farther back until
it was evident that in general they came from what might be called
it was evident that in general they came from what might be called
Line 11,180: Line 10,362:
kingdom had not as yet been made and it had proven impossible to
kingdom had not as yet been made and it had proven impossible to
explain the origin of the layers in terms of any other lower units of
explain the origin of the layers in terms of any other lower units of
organization. It is not surprising, therefore, that these early embry-
organization. It is not surprising, therefore, that these early embryologists should have looked upon the formation and subsequent development of the germ layers as the most critical processes of embryonic
ologists should have looked upon the formation and subsequent de-
velopment of the germ layers as the most critical processes of embryonic
life.
life.


Line 11,189: Line 10,369:
all biological speculations. After the true nature of cells and their
all biological speculations. After the true nature of cells and their
methods of reproduction and growth came to be understood, the theory
methods of reproduction and growth came to be understood, the theory
acquired new significance and, in the hands of Oscar and Richard
acquired new significance and, in the hands of Oscar and Richard
Hertwig, had attained the status of a full-fledged theory of development
Hertwig, had attained the status of a full-fledged theory of development
by the early eighties. Through a great variety of forms, blastulae and
by the early eighties. Through a great variety of forms, blastulae and
gastrulae were identified, their methods of origin understood, and the
gastrulae were identified, their methods of origin understood, and the
remarkably uniform character of all the processes involved in germ-
remarkably uniform character of all the processes involved in germlayer formation and in the laying down of the fundaments of the organs
layer formation and in the laying down of the fundaments of the organs
was made out. Exceptions occur; indeed, some of them are of great
was made out. Exceptions occur; indeed, some of them are of great
importance, but considered as a whole there is striking uniformity in
importance, but considered as a whole there is striking uniformity in
Line 11,204: Line 10,383:
developing organs.
developing organs.


The essential point of the theory is that the three layers are homol-
The essential point of the theory is that the three layers are homologous throughout the animal kingdom above the Porifera. In the
ogous throughout the animal kingdom above the Porifera. In the
coelenterates, as in the gastrulae, there are present only ectoderm and
coelenterates, as in the gastrulae, there are present only ectoderm and
endoderm. Since the layers are homologous, the organs which arise
endoderm. Since the layers are homologous, the organs which arise
Line 11,213: Line 10,391:
stage called the gastrula, of which the two component layers are known
stage called the gastrula, of which the two component layers are known
as primary germ layers, the outer being the primary ectoderm (epiblast,
as primary germ layers, the outer being the primary ectoderm (epiblast,
ectoblast), and the inner the primary endoderm (hypoblast or endo-
ectoblast), and the inner the primary endoderm (hypoblast or endoblast). The primary ectoderm in etenophores, turbellarians, rotifers,
blast). The primary ectoderm in etenophores, turbellarians, rotifers,
annelids, and molluses contributes with the primary endoderm to the
annelids, and molluses contributes with the primary endoderm to the
formation of the middle germ layer, the mesoderm (mesoblast) giving
formation of the middle germ layer, the mesoderm (mesoblast) giving
rise to the distinction of ectomesodcrm and cndomesoderm respectively.
rise to the distinction of ectomesodcrm and cndomesoderm respectively.
From the outer layer also come: (a) the covering tissues with all their
From the outer layer also come: (a) the covering tissues with all their
modifications and appendages including hair, horns, nails, scales, skin,
modifications and appendages including hair, horns, nails, scales, skin,
glands, (b) the nervous system and sensory epithelium, and (c) in many
glands, (b) the nervous system and sensory epithelium, and (c) in many
cases the stomodaeum and proctodacum (extreme anterior and posterior
cases the stomodaeum and proctodacum (extreme anterior and posterior
Line 11,237: Line 10,414:
formation. Isolated endoderm cells may push into a space between the
formation. Isolated endoderm cells may push into a space between the
two layers at the same time with the secretion of a jelly-like substance,
two layers at the same time with the secretion of a jelly-like substance,
thus giving rise to a filling-in layer known as mesenchyme from which
thus giving rise to a filling-in layer known as mesenchyme from which
certain organs or parts of organs take their origin. In a second method
certain organs or parts of organs take their origin. In a second method
the typical epithelial character of the primary germ layers is preserved
the typical epithelial character of the primary germ layers is preserved
Line 11,261: Line 10,438:
great importance of the germ-layer theory as outlined by the Hertwigs.
great importance of the germ-layer theory as outlined by the Hertwigs.
Probably no other theory or working hypothesis, with the exception of
Probably no other theory or working hypothesis, with the exception of
Darwin’s own contributions, has been so fruitful as a stimulus for con-
Darwin’s own contributions, has been so fruitful as a stimulus for constructive zoological work. The germ-layer theory has to its credit much
structive zoological work. The germ-layer theory has to its credit much
of the most important embryological accomplishment. As a working
of the most important embryological accomplishment. As a working
hypothesis it is of the greatest importance.
hypothesis it is of the greatest importance.
Line 11,279: Line 10,455:
and mesenchymous connective cells in different chordate groups; the
and mesenchymous connective cells in different chordate groups; the
composite nature of some organs, for example the nephridia, from
composite nature of some organs, for example the nephridia, from
more than one germ layer; the identification of the mesoderm as the
more than one germ layer; the identification of the mesoderm as the
4d cell, not a layer at all, in the individuals with spiral cleavage; and
4d cell, not a layer at all, in the individuals with spiral cleavage; and
especially the facts of budding, differentiation, and regeneration. Some
especially the facts of budding, differentiation, and regeneration. Some
Line 11,285: Line 10,461:
should not make us underestimate the value of this conception as a
should not make us underestimate the value of this conception as a
whole. However, it is now known that there are many evidences of
whole. However, it is now known that there are many evidences of
organization appearing long before germ layers are formed. The pro-
organization appearing long before germ layers are formed. The promorphology of the ovum in the eggs with determinative cleavage and
morphology of the ovum in the eggs with determinative cleavage and
the possibility of tracing out the cell lineage during cleavage and organ
the possibility of tracing out the cell lineage during cleavage and organ
formation in embryos of this class distinctly minimize the importance
formation in embryos of this class distinctly minimize the importance
Line 11,298: Line 10,473:


steps. It is an essential stage in most cases through which the course
steps. It is an essential stage in most cases through which the course
of development must pass, but in special cases adaptive modifications
of development must pass, but in special cases adaptive modifications
have arisen. Homologies exist between blastomeres—sometimes, as
have arisen. Homologies exist between blastomeres—sometimes, as
in the 4d cell and the “cross” of the annelids and molluscs, of very
in the 4d cell and the “cross” of the annelids and molluscs, of very
Line 11,304: Line 10,479:
and between organ systems. All are important, perhaps equally so.
and between organ systems. All are important, perhaps equally so.
But the germ layers are probably best regarded as temporary embryonic
But the germ layers are probably best regarded as temporary embryonic
organs which play their part and give rise to subsequent stages of de-
organs which play their part and give rise to subsequent stages of development rather than as units of organization which determine the
velopment rather than as units of organization which determine the
future course of development.
future course of development.
CHAPTER III
CHAPTER III
Line 11,315: Line 10,489:
the fundamental law of biogenesis. To it was due much laborious and
the fundamental law of biogenesis. To it was due much laborious and
painstaking research, and the interpretations based upon it have had
painstaking research, and the interpretations based upon it have had
far-reaching significance. Yet during the last decade critical studies
far-reaching significance. Yet during the last decade critical studies
have dethroned this doctrine so that as a “law” it is now of value only
have dethroned this doctrine so that as a “law” it is now of value only
historically. As a tendency, however, recapitulation is still a useful
historically. As a tendency, however, recapitulation is still a useful
conception for it unquestionably expresses a partial truth, a fact to
conception for it unquestionably expresses a partial truth, a fact to
which is due the long-continued interest in the doctrine and the stimu-
which is due the long-continued interest in the doctrine and the stimulating effect it has had upon embryological studies.
lating effect it has had upon embryological studies.


Recapltulation refers to the parallel which exists between the history
Recapltulation refers to the parallel which exists between the history
Line 11,332: Line 10,505:
series of legless apoda and the salamanders. This series begins with the
series of legless apoda and the salamanders. This series begins with the
lower urodeles which have external gills and weak legs, then comes
lower urodeles which have external gills and weak legs, then comes
Amphzuma with small posterior legs, the Salamandridae in which ex-
Amphzuma with small posterior legs, the Salamandridae in which external gills are lost, the legs are about equally developed, and the tail
ternal gills are lost, the legs are about equally developed, and the tail
is about equal to the body in length, and finally the Anura which have
is about equal to the body in length, and finally the Anura which have
no gills or tail and the hind legs are the better developed. (Fig. 190.)
no gills or tail and the hind legs are the better developed. (fig. 190.)


The development of the decapod Crustacea, in which the larvae
The development of the decapod Crustacea, in which the larvae
pass through stages comparable to those characteristic of some other
pass through stages comparable to those characteristic of some other
orders of the Malacostraca (Fig. 191), is an often-cited case to illustrate
orders of the Malacostraca (fig. 191), is an often-cited case to illustrate
the biogenetic law. Another illustration involves the ascidians (Fig.
the biogenetic law. Another illustration involves the ascidians (fig.
192) which superficially resemble shapeless jelly-like masses, and whose
192) which superficially resemble shapeless jelly-like masses, and whose
relationships are therefore difficult to decipher. A study of their embry-
relationships are therefore difficult to decipher. A study of their embryology revealed the fact that they pass through a tadpole stage with
ology revealed the fact that they pass through a tadpole stage with
dorsal nerve chord, notochord, etc., all recognizable as vertebrate char
dorsal nerve chord, notochord, etc., all recognizable as vertebrate char-
 
acters, but when they settle down and become sessile these structures
acters, but when they settle down and become sessile these structures
286
286
Line 11,354: Line 10,524:


d 8
d 8
FIG. 190. Early stages in the development of a frog tadpole compared with adults of
fiG. 190. Early stages in the development of a frog tadpole compared with adults of
Siren (e), Amphiuma. (f), Desmoonathus (0), and an adult frog (h).
Siren (e), Amphiuma. (f), Desmoonathus (0), and an adult frog (h).


Cirripedia or barnacles. Barnacles have heavy shells, are sessile, and in
Cirripedia or barnacles. Barnacles have heavy shells, are sessile, and in
general are quite unlike the ordinary Crustacea to which their develop-
general are quite unlike the ordinary Crustacea to which their developZ66 'l‘l'1l!2 RECAPITULAT ION THEORY
Z66 'l‘l'1l!2 RECAPITULAT ION THEORY


inent clearly shows them to be allied. A second suborder of the Cirri-
inent clearly shows them to be allied. A second suborder of the Cirripedia doubtless presents the most extreme case of modification to be
pedia doubtless presents the most extreme case of modification to be
found in the animal kingdom. This is Rhizocephala to which the parasitic Sacculina belongs. (fig. 193.) During its larval stages Sacculina is
found in the animal kingdom. This is Rhizocephala to which the para-
sitic Sacculina belongs. (Fig. 193.) During its larval stages Sacculina is
a free-swimming form having about the usual external features of a
a free-swimming form having about the usual external features of a
young braiichiopod crustacean. It attaches itself to the abdomen of a
young braiichiopod crustacean. It attaches itself to the abdomen of a
Line 11,377: Line 10,544:
adult is so degenerate that it has no crustacean characteristics but is
adult is so degenerate that it has no crustacean characteristics but is
merely a tumor-like sac on the abdomen of the crab in which even the
merely a tumor-like sac on the abdomen of the crab in which even the
usual internal organs are scarcely present, the body being chiefly filled
usual internal organs are scarcely present, the body being chiefly filled
with the gonads and their products. Only its life cycle reveals its re-
with the gonads and their products. Only its life cycle reveals its relation to the other Cirripedia. The anatomical relationships by means
lation to the other Cirripedia. The anatomical relationships by means
of which its phylogenetic position is determined are made clear by a
of which its phylogenetic position is determined are made clear by a
study of its cmbryological development.
study of its cmbryological development.
Line 11,385: Line 10,551:
Vaguely foreshadowed by the writings of Meckel and others of the
Vaguely foreshadowed by the writings of Meckel and others of the
period, the recapitulation principle is first directly hinted at in the
period, the recapitulation principle is first directly hinted at in the
writings of von Baer. Indeed, by some von Baer’s laws have been con-
writings of von Baer. Indeed, by some von Baer’s laws have been conTHE RECAPITULATION THEORY 289
THE RECAPITULATION THEORY 289


fused with the recapitulation theory. These laws are, however, Inore
fused with the recapitulation theory. These laws are, however, Inore
Line 11,396: Line 10,561:


“2. From the most general features of structure arise those that are
“2. From the most general features of structure arise those that are
less general, and so on until the most specific features arise.
less general, and so on until the most specific features arise.


“3. The embryo of a definite species tends away from the specific
“3. The embryo of a definite species tends away from the specific
forms of other species, instead of passing through them.
forms of other species, instead of passing through them.


Line 11,413: Line 10,578:
enunciated germ-layer theory represented the last word in emhryological
enunciated germ-layer theory represented the last word in emhryological
knowledge of the time in the matter of early structural organization.
knowledge of the time in the matter of early structural organization.
The advances made possible by the cell doctrine resulted in the enuncia-
The advances made possible by the cell doctrine resulted in the enunciation by Fritz Muller in 1863 of the recapitulation doctrine as such.
tion by Fritz Muller in 1863 of the recapitulation doctrine as such.
Haeckel developed the theory and applied it in his famous blasteagastrea hypothesis.
Haeckel developed the theory and applied it in his famous blastea-
gastrea hypothesis.


Haeckel’s hypothesis lays stress on the importance of the universal
Haeckel’s hypothesis lays stress on the importance of the universal
Line 11,422: Line 10,585:
290 THE RECAPITULATION THEORY
290 THE RECAPITULATION THEORY


blastula, and the gastrula, and supposes that the phylogenetic develop-
blastula, and the gastrula, and supposes that the phylogenetic development has taken a similar course. The protozoa represent the first step
ment has taken a similar course. The protozoa represent the first step
and are comparable to the egg stage in individual development. No
and are comparable to the egg stage in individual development. No
animal is known which exactly corresponds to the blastula or the
animal is known which exactly corresponds to the blastula or the
Line 11,439: Line 10,601:
carcmt. (After Deluge.)
carcmt. (After Deluge.)


Haeckel also pointed out the significance of certain characters as
Haeckel also pointed out the significance of certain characters as
indicating phylogenetic history whereas others are to be regarded as
indicating phylogenetic history whereas others are to be regarded as
embryological adaptations of importance to the individual organism,
embryological adaptations of importance to the individual organism,
but not to the race. Characters of the first class are spoken of as palin-
but not to the race. Characters of the first class are spoken of as palingenetic; of the second, as cenogenetic. A chick embryo, for instance,
genetic; of the second, as cenogenetic. A chick embryo, for instance,
has a good many characters which recall fish or amphibian conditions,
has a good many characters which recall fish or amphibian conditions,
but it could not exist in the environment where these forms dwell, and
but it could not exist in the environment where these forms dwell, and
is different in numbers of other characteristics including the important
is different in numbers of other characteristics including the important
one that it will develop not into a fish or amphibian, but a bird. It can-
one that it will develop not into a fish or amphibian, but a bird. It cannot, therefore, in its development represent with entire correctness the
not, therefore, in its development represent with entire correctness the
ancestral forms. Some of its characters are those which adapt it to
ancestral forms. Some of its characters are those which adapt it to
development in a shell at a temperature of 37° C. and enable it to live
development in a shell at a temperature of 37° C. and enable it to live
Line 11,455: Line 10,615:
THE RECAPITULATION THEORY 291
THE RECAPITULATION THEORY 291


vesicles, and others, are supposed to be of ancestral significance and
vesicles, and others, are supposed to be of ancestral significance and
are, therefore, palingenetic.
are, therefore, palingenetic.


A critical consideration of many cases which may be cited, however,
A critical consideration of many cases which may be cited, however,
shows that the facts do not all easily fit into the biogenetic interpretation.
shows that the facts do not all easily fit into the biogenetic interpretation.
When one attempts to classify clear cases such as the shell tooth on the
When one attempts to classify clear cases such as the shell tooth on the
one hand or the aortic arches on the other as adaptive or ancestral
one hand or the aortic arches on the other as adaptive or ancestral
little difliculty is experienced, but the problem of applying the same
little difliculty is experienced, but the problem of applying the same
classification to a doubtful ease becomes much more complex, and as a
classification to a doubtful ease becomes much more complex, and as a
rule the results cannot be certainly relied upon. Indeed, recognition of
rule the results cannot be certainly relied upon. Indeed, recognition of
a particular character as palingenetic or cenogenetic may be quite an
a particular character as palingenetic or cenogenetic may be quite an
impossible task.
impossible task.


Other difficulties may be cited which require modification of the strict
Other difficulties may be cited which require modification of the strict
biogenetic way of looking at the animal kingdom. For example, there
biogenetic way of looking at the animal kingdom. For example, there
is a general tendency which becomes more marked the higher one goes
is a general tendency which becomes more marked the higher one goes
Line 11,483: Line 10,643:
if reeapitulation occurs even in the most sketchy fashion, an immense
if reeapitulation occurs even in the most sketchy fashion, an immense
contraction of stages must be thought to take place so that the necessary
contraction of stages must be thought to take place so that the necessary
abbreviation may be accomplished. To this shortening of the develop-
abbreviation may be accomplished. To this shortening of the developmental time, or tachygenesis, there are two aspects, the actual quickening of the rate of development and the fusion and omission of certain
mental time, or tachygenesis, there are two aspects, the actual quicken-
ing of the rate of development and the fusion and omission of certain
stages. The one aspect may occur without the other in special cases as
stages. The one aspect may occur without the other in special cases as
in the response of the developmental rate to rise in temperature, where
in the response of the developmental rate to rise in temperature, where
Line 11,491: Line 10,649:


Hcterochrony also presents an argument against the reeapitulation
Hcterochrony also presents an argument against the reeapitulation
doctrine, as was pointed out by Keibel, Mehnert, and others. By heter-
doctrine, as was pointed out by Keibel, Mehnert, and others. By heterochrony is meant the disturbances, which now are known to be of quite
ochrony is meant the disturbances, which now are known to be of quite
common occurrence, in the time of appearance of structures in a known
common occurrence, in the time of appearance of structures in a known
sequence of stages.
sequence of stages.


These modifications in the rates of development bring about results
These modifications in the rates of development bring about results
which cannot be interpreted either as of phyletic or adaptive significance.
which cannot be interpreted either as of phyletic or adaptive significance.
Stockard has lately pointed out the importance of the arrest of develop-
Stockard has lately pointed out the importance of the arrest of development, even over a small part of the germ ring, whereby various types
ment, even over a small part of the germ ring, whereby various types
of monsters are produced. Evidently, here are structural modifications
of monsters are produced. Evidently, here are structural modifications
not to be related to recapitulation. Furthermore, the normal develop292 THE RECAPITULATION THEORY
not to be related to recapitulation. Furthermore, the normal develop-
292 THE RECAPITULATION THEORY


ment of the organ systems of the embryos of different classes does not
ment of the organ systems of the embryos of different classes does not
preserve the same synchrony as may be noted by comparing tables of
preserve the same synchrony as may be noted by comparing tables of
the development, let us say, of the chick and pig (Keibel, N ormentafeln).
the development, let us say, of the chick and pig (Keibel, N ormentafeln).
In addition, there are extreme cases in which the actual order of de-
In addition, there are extreme cases in which the actual order of development is the reverse of what would be demanded by recapitulation,
velopment is the reverse of what would be demanded by recapitulation,
as, for example, in those cases in which the joints become rounded off
as, for example, in those cases in which the joints become rounded off
before movement is acquired. Another illustration is the formation of
before movement is acquired. Another illustration is the formation of
the tongue and the teeth. There is no question that in the phylogenetic
the tongue and the teeth. There is no question that in the phylogenetic
series teeth made their appearance before tongues, but in the embryo-
series teeth made their appearance before tongues, but in the embryological development of mammals the teeth are much later developed
logical development of mammals the teeth are much later developed
than the tongue. Ontogeny not only fails to recapitulate phylogeny
than the tongue. Ontogeny not only fails to recapitulate phylogeny
in this case, but completely misrepresents the facts.
in this case, but completely misrepresents the facts.
Line 11,521: Line 10,674:
structures in the individual with that in the ancestral forms. This
structures in the individual with that in the ancestral forms. This
summary with no further elaboration is sufficient to make clear that
summary with no further elaboration is sufficient to make clear that
some of the possible variations not only do not fit in with the conception
some of the possible variations not only do not fit in with the conception
of recapitulation but are actually opposed to it. The summary is as
of recapitulation but are actually opposed to it. The summary is as
follows 2*
follows 2*
Line 11,534: Line 10,687:


“B. In the young and adult stage, producing a substitution of the
“B. In the young and adult stage, producing a substitution of the
new adult condition for the old, resulting in a progressive dena-
new adult condition for the old, resulting in a progressive denation in the ontogeny of the descendant from that of the ancestor.
tion in the ontogeny of the descendant from that of the ancestor.


“C. In the adult, by a relative retardation of the development of
“C. In the adult, by a relative retardation of the development of
Line 11,550: Line 10,702:
stage of an ancestor may in the ontogeny of a descendant appear:
stage of an ancestor may in the ontogeny of a descendant appear:


“E. In the adult stage, resulting in those differences which dis-
“E. In the adult stage, resulting in those differences which distinguish individuals, varieties, and races: adult bariation.
tinguish individuals, varieties, and races: adult bariation.


* Reprinted from De Beer's “Embryology and Evolution,” by permission of Oxford
* Reprinted from De Beer's “Embryology and Evolution,” by permission of Oxford
Line 11,568: Line 10,719:
ancestral character and acceleration.
ancestral character and acceleration.


“Cases B and C which produce phylogenetic efiects by introducing
“Cases B and C which produce phylogenetic efiects by introducing
youthful characters into the line of adults may be combined under the
youthful characters into the line of adults may be combined under the
term paedonzorphosis. Cases E, G, and H which produce phylogenetic
term paedonzorphosis. Cases E, G, and H which produce phylogenetic
Line 11,574: Line 10,725:
of adults may conveniently be included under the term geront0morphos2's.”
of adults may conveniently be included under the term geront0morphos2's.”


In Inany forms the problem is further complicated by the prolonga-
In Inany forms the problem is further complicated by the prolongation of certain stages while internal processes are going on. If the
tion of certain stages while internal processes are going on. If the
gradual internal development of a caterpillar were accompanied by
gradual internal development of a caterpillar were accompanied by
gradual conversion of the biting type of mouth parts to the sucking
gradual conversion of the biting type of mouth parts to the sucking
type, the insect would starve, for during the transition the mouth parts
type, the insect would starve, for during the transition the mouth parts
would be adapted to neither the larval nor the adult method of nutri-
would be adapted to neither the larval nor the adult method of nutrition. By the prolongation of the biting stage until the internal parts
tion. By the prolongation of the biting stage until the internal parts
are ready for the metamorphosis, the animal’s relation to its surroundings are unchanged until the internal conditions are right when a sudden
are ready for the metamorphosis, the animal’s relation to its surround-
metamorphosis brings about the necessary adjustment to a new environment without loss to the insect. These facts are not in keeping
ings are unchanged until the internal conditions are right when a sudden
metamorphosis brings about the necessary adjustment to a new en-
vironment without loss to the insect. These facts are not in keeping
with the biogenetic law as usually interpreted.
with the biogenetic law as usually interpreted.


Line 11,590: Line 10,737:
bearing upon the doctrine of recapitulation. It is now possible to show
bearing upon the doctrine of recapitulation. It is now possible to show
that external factors reacting with the internal, inherited constitution
that external factors reacting with the internal, inherited constitution
of the organism can produce such effects upon the oflspring that its
of the organism can produce such effects upon the oflspring that its
entire ontogeny including the adult is modified. As stated elsewhere,
entire ontogeny including the adult is modified. As stated elsewhere,
Stockard has shown, for example, that developmental arrests will
Stockard has shown, for example, that developmental arrests will
produce many types of modifications in Fundulus, including two heads,
produce many types of modifications in Fundulus, including two heads,
trunks, or even two individuals where only one would have otherwise
trunks, or even two individuals where only one would have otherwise
been formed, and conversely that the age-old tendency of the egg to
been formed, and conversely that the age-old tendency of the egg to
produce two eyes on the fishes’ head can be changed by the simple
produce two eyes on the fishes’ head can be changed by the simple
addition of a little magnesium chloride. The internal, inherited control
addition of a little magnesium chloride. The internal, inherited control
of development is thus capable of modification. And Muller has shown
of development is thus capable of modification. And Muller has shown
that by exposure to X-rays the developing Drosophzla can be induced
that by exposure to X-rays the developing Drosophzla can be induced
to react in such a manner that entirely new mutations, that is, self-
to react in such a manner that entirely new mutations, that is, selfperpetuating strains, can be produced, even at will. Thus is phylogeny
perpetuating strains, can be produced, even at will. Thus is phylogeny
deceived by ontogeny’. For these reacting ontogenies have produced
deceived by ontogeny’. For these reacting ontogenies have produced
an entirely new series of adults which can undoubtedly become an-
an entirely new series of adults which can undoubtedly become an294 THE RECAPITULATION THEORY
294 THE RECAPITULATION THEORY


cestral to others later to appear. Now phylogeny means to most thinkers
cestral to others later to appear. Now phylogeny means to most thinkers
just a series of adult forms having racial significance. Hence it would
just a series of adult forms having racial significance. Hence it would
appear that such experiments as that of Muller have brought us face
appear that such experiments as that of Muller have brought us face
to face with an exact reversal of the usual causal role attributed to
to face with an exact reversal of the usual causal role attributed to
phylogeny, for here phylogeny is the direct result of ontogenetic modi-
phylogeny, for here phylogeny is the direct result of ontogenetic modification and certainly not the controlling cause of it, as it is usually
fication and certainly not the controlling cause of it, as it is usually
considered to be by the adherents of recapitulation.
considered to be by the adherents of recapitulation.


From the criticisms which have been given the student can under-
From the criticisms which have been given the student can understand why the so-called “fundamental law of biogenesis” has passed
stand why the so-called “fundamental law of biogenesis” has passed
from the high position of a natural law, and is little more than a general
from the high position of a natural law, and is little more than a general
tendency. It is a tendency, furthermore, which is more valuable in
tendency. It is a tendency, furthermore, which is more valuable in
retrospect than as a means of prediction. And since prediction upon the
retrospect than as a means of prediction. And since prediction upon the
basis of known facts and postulates is the goal of science and the funda-
basis of known facts and postulates is the goal of science and the fundamental test of a “natural law,” this doctrine does not measure up to
mental test of a “natural law,” this doctrine does not measure up to
scientific expectation and cannot be regarded as a law.
scientific expectation and cannot be regarded as a law.


Yet the partial truths which are involved are of sufficient value in
Yet the partial truths which are involved are of sufficient value in
view of the widespread occurrence of the tendency represented to
view of the widespread occurrence of the tendency represented to
warrant a revaluation of the essential idea of the doctrine. We find an
warrant a revaluation of the essential idea of the doctrine. We find an
attempt of this kind expressed some years ago by Lillie in his work on
attempt of this kind expressed some years ago by Lillie in his work on
the embryology of the chick. His views appear to go far in the direction
the embryology of the chick. His views appear to go far in the direction
Line 11,631: Line 10,773:
to avoid some of the contradictions which have been mentioned. He
to avoid some of the contradictions which have been mentioned. He
conceived that the entire life history of an organism is as necessary for
conceived that the entire life history of an organism is as necessary for
the definition of species as any other character. Ontogenies are inherited
the definition of species as any other character. Ontogenies are inherited
also and are subjected to variation with resulting modification. Ontog-
also and are subjected to variation with resulting modification. Ontogenies of closely related species are more nearly alike than those less
enies of closely related species are more nearly alike than those less
related. In the evolution of a species those stages of ontogeny latest to
related. In the evolution of a species those stages of ontogeny latest to
have arisen (those found in the adult) are the ones most easily to be
have arisen (those found in the adult) are the ones most easily to be
modified and hence the embryo as a rule retains the ancestral resem-
modified and hence the embryo as a rule retains the ancestral resemblances the longest. This is not because these have phylogenetic, that
blances the longest. This is not because these have phylogenetic, that
is palingenetic, significance, but because the embryo is less susceptible
is palingenetic, significance, but because the embryo is less susceptible
to outside influences and therefore its characters are less the material
to outside influences and therefore its characters are less the material
upon which selection may operate. Embryonic resemblances being more
upon which selection may operate. Embryonic resemblances being more
conservative and actually older are nearer the ancestral condition.
conservative and actually older are nearer the ancestral condition.
They are statements of historical facts rather than causes of recapitula-
They are statements of historical facts rather than causes of recapitulation. But because of the chronological sequence of stages in a great
tion. But because of the chronological sequence of stages in a great
many observed cases, the older recapitulationists came to regard each
many observed cases, the older recapitulationists came to regard each
stage as strictly causal to the succeeding ones and thus to look upon
stage as strictly causal to the succeeding ones and thus to look upon
Line 11,667: Line 10,806:
really a mass division, due especially to the cells of some particular area
really a mass division, due especially to the cells of some particular area
undergoing a proliferation which presently results in the constriction
undergoing a proliferation which presently results in the constriction
and cutting ofi” of a greater or lesser portion of the animal. If the portions
and cutting ofi” of a greater or lesser portion of the animal. If the portions
are approximately equal the process is spoken of as fission; if unequal,
are approximately equal the process is spoken of as fission; if unequal,
as budding. These, with sporulation, are the common forms of asexual
as budding. These, with sporulation, are the common forms of asexual
reproduction, but each shows many variants in the animals in which
reproduction, but each shows many variants in the animals in which
Line 11,674: Line 10,813:


Sexual reproduction, involving the participation of two individuals,
Sexual reproduction, involving the participation of two individuals,
is known as amphigony; asexual, since only a single individual is neces-
is known as amphigony; asexual, since only a single individual is necessary, is monogony. In the former, germ cells or their equivalents are
sary, is monogony. In the former, germ cells or their equivalents are
produced; in the latter, there are no special cells employed for the purpose. The alternation of a sexual with an asexual generation is called
produced; in the latter, there are no special cells employed for the pur-
pose. The alternation of a sexual with an asexual generation is called
metagenesis. The alternation of a biparental sexual generation, that is,
metagenesis. The alternation of a biparental sexual generation, that is,
a case of amphigony, with a uniparental, a parthenogenetic, generation
a case of amphigony, with a uniparental, a parthenogenetic, generation
Line 11,683: Line 10,820:
or cytogony by Hartman, and asexual, agamocytogony (also agamogony).
or cytogony by Hartman, and asexual, agamocytogony (also agamogony).


Fission is the division of an organism into two parts which are approxi-
fission is the division of an organism into two parts which are approximately equal and into whose formation very little new material has
mately equal and into whose formation very little new material has
gone. The parent organism is lost in the production of the daughters,
gone. The parent organism is lost in the production of the daughters,


Line 11,692: Line 10,828:


what may be termed accidental death. It occurs when growth has taken
what may be termed accidental death. It occurs when growth has taken
place in excess of the needs of the individual. Contrasted to the con-
place in excess of the needs of the individual. Contrasted to the condition in sexual reproduction, the new organism is at once provided
dition in sexual reproduction, the new organism is at once provided
with at least part of the organs which characterize the adult, and differentiation is always well advanced, considering that the organism is
with at least part of the organs which characterize the adult, and differ-
entiation is always well advanced, considering that the organism is
seldom high in the scale of animal life. Two categories were distinguished
seldom high in the scale of animal life. Two categories were distinguished
by F. von Wagner for organisms undergoing fission: in the one, paratomy,
by F. von Wagner for organisms undergoing fission: in the one, paratomy,
a special zone, in which the constriction will occur, is prepared before
a special zone, in which the constriction will occur, is prepared before
fission begins; in the other, architomy, no preparation is made, constric-
fission begins; in the other, architomy, no preparation is made, constriction taking place more primitively with little bodily reorganization. It
tion taking place more primitively with little bodily reorganization. It
should be noted that both of these categories may apply to either longitudinal or cross fission. Under the general head of fission may also be
should be noted that both of these categories may apply to either longi-
tudinal or cross fission. Under the general head of fission may also be
placed those cases of fragmentation, such as occur in oligochaetes and
placed those cases of fragmentation, such as occur in oligochaetes and
starfish, due to external influences, which may, if conditions are suitable,
starfish, due to external influences, which may, if conditions are suitable,
develop into mature individuals. These cases are also spoken of as
develop into mature individuals. These cases are also spoken of as
autotomy, and sometimes as augmentation.
autotomy, and sometimes as augmentation.


Budding, although not much more complex as a process than fission,
Budding, although not much more complex as a process than fission,
is productive of much more complicated organisms and life cycles. It
is productive of much more complicated organisms and life cycles. It
often is the means by which colonies are formed, and results in marked
often is the means by which colonies are formed, and results in marked
polymorphism with some of the individuals of the colony being special-
polymorphism with some of the individuals of the colony being specialized for nutritive and vegetative purposes and others for reproduction.
ized for nutritive and vegetative purposes and others for reproduction.
Commonly where a considerable degree of specialization follows the
Commonly where a considerable degree of specialization follows the
budding processes the life cycle includes a sexual as well as an asexual
budding processes the life cycle includes a sexual as well as an asexual
phase and we have alternation of generations. A bud is a small portion
phase and we have alternation of generations. A bud is a small portion
of the parent organism which has begun to grow actively and to pro-
of the parent organism which has begun to grow actively and to proliferate and from which will be derived a new individual having the full
liferate and from which will be derived a new individual having the full
degree of differentiation characteristic of the species. There are buds
degree of differentiation characteristic of the species. There are buds
in some triploblastic animals which involve only one of the germ layers,
in some triploblastic animals which involve only one of the germ layers,
Line 11,731: Line 10,861:
buds” of certain forms are also of the external type. As buds they break
buds” of certain forms are also of the external type. As buds they break
off and become for a time at least free swimming. A second type includes
off and become for a time at least free swimming. A second type includes
the internal buds among which are the gemmulae of sponges, the stato-
the internal buds among which are the gemmulae of sponges, the statoblasts of the bryozoa, the germ balls of trematodes and others. A group
blasts of the bryozoa, the germ balls of trematodes and others. A group
of proliferating cells becomes isolated within the mother organism and
of proliferating cells becomes isolated within the mother organism and
in time results in a new organism. A third type involves the formation
in time results in a new organism. A third type involves the formation
Line 11,739: Line 10,868:
of a stolen or a “runner” from which numerous buds arise. This might
of a stolen or a “runner” from which numerous buds arise. This might
seem to be really a kind of external budding but it is sufficiently distinct
seem to be really a kind of external budding but it is sufficiently distinct
from the usual cases of this kind to warrant special mention. Finally a
from the usual cases of this kind to warrant special mention. finally a
fourth series of processes should be included under budding, although
fourth series of processes should be included under budding, although
they are often overlooked; they are the processes known as frustulation
they are often overlooked; they are the processes known as frustulation
Line 11,745: Line 10,874:
organism, when unfavorable conditions arise, and form new individuals.
organism, when unfavorable conditions arise, and form new individuals.


Closely related to asexual reproduction and of much significance to
Closely related to asexual reproduction and of much significance to
the comparative embryologist are the phenomena of regeneration.
the comparative embryologist are the phenomena of regeneration.
Morphogenic processes are involved in the reorganization of portions
Morphogenic processes are involved in the reorganization of portions
Line 11,762: Line 10,891:
is a dominant method. It may be taken as a general rule (not, however,
is a dominant method. It may be taken as a general rule (not, however,
without exception), that whenever individuals are found organized into
without exception), that whenever individuals are found organized into
colonies, either asexual reproduction, or polyembryony, or partheno-
colonies, either asexual reproduction, or polyembryony, or parthenogenesis will be found to occur in the same groups. The simple sexual
genesis will be found to occur in the same groups. The simple sexual
mode of reproduction seems not usually adequate to produce enough
mode of reproduction seems not usually adequate to produce enough
individuals to be associated together in a permanent colony, and one of
individuals to be associated together in a permanent colony, and one of
Line 11,773: Line 10,901:
The first examples of asexual reproduction to be found in the animal
The first examples of asexual reproduction to be found in the animal
kingdom are in the protozoa, but the process here is one of single cells
kingdom are in the protozoa, but the process here is one of single cells
and perhaps is thus somewhat outside the general problems of embry-
and perhaps is thus somewhat outside the general problems of embryology. We may begin our study therefore with the Porifera.
ology. We may begin our study therefore with the Porifera.


Porzfera. In the phylum Porifera, asexual reproduction predominates;
Porzfera. In the phylum Porifera, asexual reproduction predominates;
here are to be found fission, budding, formation of free buds, and of
here are to be found fission, budding, formation of free buds, and of
gemmulae. Since most sponges exist as colonies it is easy to see how the
gemmulae. Since most sponges exist as colonies it is easy to see how the
dividing processes have lacked completion resulting in a degree of union
dividing processes have lacked completion resulting in a degree of union
that is more or less extensive. Asexual reproduction commonly leads to
that is more or less extensive. Asexual reproduction commonly leads to
formation of colonies rather than to independence of organisms. But
formation of colonies rather than to independence of organisms. But
budding and fission are shown to advantage in Leucosolenia. Some of
budding and fission are shown to advantage in Leucosolenia. Some of
298 ASEXUAL REPRODUCTION
298 ASEXUAL REPRODUCTION


the individuals indicate fission as their mode of reproduction for the
the individuals indicate fission as their mode of reproduction for the
products are equal in size although they remain attached at the basal
products are equal in size although they remain attached at the basal
end. However, the presence of small immature individuals on certain
end. However, the presence of small immature individuals on certain
Line 11,791: Line 10,918:
   
   


Fm 194 Budding and fission in Leucosolema blanca. (From Korsehelt and Heider)
Fm 194 Budding and fission in Leucosolema blanca. (From Korsehelt and Heider)


specimens as well as the mode of colonial formation shows that budding
specimens as well as the mode of colonial formation shows that budding
is often the actual method of their origin. When fission does occur it
is often the actual method of their origin. When fission does occur it
begins as a split at the osculum and progresses toward the base. When
begins as a split at the osculum and progresses toward the base. When


   
   


FIG. 195. A, Budding in Leucosolema botryozdes B, A bud which has become free and
fiG. 195. A, Budding in Leucosolema botryozdes B, A bud which has become free and
attached to an algal filament. (From Korschelt and Heider, after Vasseur.)
attached to an algal filament. (From Korschelt and Heider, after Vasseur.)


it is not complete the beginning of a colony is seen and these colonies
it is not complete the beginning of a colony is seen and these colonies
Line 11,809: Line 10,936:


found free bud formation. The buds form from an indifferent group of
found free bud formation. The buds form from an indifferent group of
cells, grow irregularly from the parent individual, undergo differentia-
cells, grow irregularly from the parent individual, undergo differentiation to a considerable extent, and at length break off, the ruptured end
tion to a considerable extent, and at length break off, the ruptured end
forming the osculum of the new little sponge; they then settle down to
forming the osculum of the new little sponge; they then settle down to
produce young sponges.
produce young sponges.


The sponges show what is perhaps their highest degree of asexual
The sponges show what is perhaps their highest degree of asexual
reproductive activity in the formation of gemmulae, seen to best ad-
reproductive activity in the formation of gemmulae, seen to best advantage in the Hexactinellidae. They are derived from parenchymal
vantage in the Hexactinellidae. They are derived from parenchymal
cells which have wandered into the mesoglea and become separated
cells which have wandered into the mesoglea and become separated
from their original layers. Aggregates of these “archeocytes” (also
from their original layers. Aggregates of these “archeocytes” (also
Line 11,834: Line 10,959:
really an internal bud with a protective covering, tides over the organism
really an internal bud with a protective covering, tides over the organism
until a more suitable time. Thus this form of reproduction is a device
until a more suitable time. Thus this form of reproduction is a device
which enables these sponges to adapt themselves to changing environ-
which enables these sponges to adapt themselves to changing environments. The parental tissue degenerates and dies after the gemmules are
ments. The parental tissue degenerates and dies after the gemmules are
formed. When the gemmules begin to grow, the cells multiply rapidly,
formed. When the gemmules begin to grow, the cells multiply rapidly,
those at the surface arrange themselves in a layer, and from the gem-
those at the surface arrange themselves in a layer, and from the gemmules a larva issues which is strikingly similar to the sexually produced
mules a larva issues which is strikingly similar to the sexually produced
young in form, structure, and ciliation.
young in form, structure, and ciliation.


Division among sponges is often accidental so far as the organism is
Division among sponges is often accidental so far as the organism is
concerned, and the animals offer opportunity for experimental frag-
concerned, and the animals offer opportunity for experimental fragmentation as well as normal. H. V. Wilson’s work and that of J. S.
mentation as well as normal. H. V. Wilson’s work and that of J. S.
300 ASEXUAL REPRODUCTION
300 ASEXUAL REPRODUCTION


Huxley give illustrations of the extent to which sponges may be dis-
Huxley give illustrations of the extent to which sponges may be dismembered (in these cases by being squeezed through bolting cloth) and
membered (in these cases by being squeezed through bolting cloth) and
subsequent regeneration serve to produce new sponges. Often cell
subsequent regeneration serve to produce new sponges. Often cell
masses come together, fuse, and grow into a new individual from which
masses come together, fuse, and grow into a new individual from which
Line 11,857: Line 10,978:
as those which have already been shown for the various types of embryos,
as those which have already been shown for the various types of embryos,
cleavage patterns, and methods of gastrulation. Nearly all types of
cleavage patterns, and methods of gastrulation. Nearly all types of
asexual reproduction are exhibited somewhere in the phylum. In addi-
asexual reproduction are exhibited somewhere in the phylum. In addi
 
   
   


Fm. 197. Trunsversc fission in Protohydra. (From Korschclt and Heider. ufter Aders.)
Fm. 197. Trunsversc fission in Protohydra. (From Korschclt and Heider. ufter Aders.)


tion there is often manifested an extreme polymorphism in the forms
tion there is often manifested an extreme polymorphism in the forms
which are thus produced, and the details of the manner of their pro-
which are thus produced, and the details of the manner of their production especially where a compound type of budding is involved are
duction especially where a compound type of budding is involved are
often extremely complicated. Mention here can be made of only a few
often extremely complicated. Mention here can be made of only a few
cases which constitute a very meager outline indeed. Fission, both
cases which constitute a very meager outline indeed. fission, both
transverse and longitudinal, budding both larval and adult, and colony
transverse and longitudinal, budding both larval and adult, and colony
formation by the production of permanent buds, metagenesis, stolen
formation by the production of permanent buds, metagenesis, stolen
Line 11,874: Line 10,993:
group.
group.


The Hydrozoa exhibit only a few types of asexual reproduction. Trans-
The Hydrozoa exhibit only a few types of asexual reproduction. Transverse fission occurs in Protohydra, according to Aders, and consists in
verse fission occurs in Protohydra, according to Aders, and consists in
THE HYDROZOA 301
THE HYDROZOA 301


Line 11,886: Line 11,004:
Protohydra, the chief points of difference between the two being in the
Protohydra, the chief points of difference between the two being in the
simpler structure and the lack of tentacles on the part of the latter.
simpler structure and the lack of tentacles on the part of the latter.
Longitudinal fission has been described for Polypodium only among
Longitudinal fission has been described for Polypodium only among
hydrozoa.
hydrozoa.


Line 11,912: Line 11,030:
Among adult hydrozoans budding occurs in both polyps and medusae.
Among adult hydrozoans budding occurs in both polyps and medusae.
In Hydra and the colonial hydroids it is of such common occurrence
In Hydra and the colonial hydroids it is of such common occurrence
that mere reference to it is suflicient. The bud of Hydra consists of a
that mere reference to it is suflicient. The bud of Hydra consists of a
protuberance which grows, develops tentacles, a hypostone, and at
protuberance which grows, develops tentacles, a hypostone, and at
length a mouth, after which it is ready for separation from the parent.
length a mouth, after which it is ready for separation from the parent.
Line 11,919: Line 11,037:
until the time of complete constriction of the latter. Budding is much
until the time of complete constriction of the latter. Budding is much
more common than sexual reproduction. In hydroids the process is
more common than sexual reproduction. In hydroids the process is
essentially the same except that it is usually incomplete, the bud re-
essentially the same except that it is usually incomplete, the bud remaining in connection _with the parent stalk; in this manner a colony is
maining in connection _with the parent stalk; in this manner a colony is
formed. ’
formed. ’
302 ASEXUAL REPRODUCTION
302 ASEXUAL REPRODUCTION
Line 11,928: Line 11,045:
There are cases, to be sure, where the ontogeny is so abridged that the
There are cases, to be sure, where the ontogeny is so abridged that the
polyp stage is extremely rudimentary or even entirely lacking, unless
polyp stage is extremely rudimentary or even entirely lacking, unless
the planula be regarded as representing it, and the egg develops con-
the planula be regarded as representing it, and the egg develops continuously into the medusa. But in general the medusoid generation is
tinuously into the medusa. But in general the medusoid generation is
produced by budding from the hydroid generation or the polyp. The
produced by budding from the hydroid generation or the polyp. The
main stalk, or hydrocaulus, has attached to it in Obelia, modified
main stalk, or hydrocaulus, has attached to it in Obelia, modified
hydranths, called gonangia, which bud to produce medusae. In Obelia
hydranths, called gonangia, which bud to produce medusae. In Obelia
these become detached to swim freely. In the Narcomedusae a prolif-
these become detached to swim freely. In the Narcomedusae a proliferating stolon buds off medusae which may remain in clusters or may
erating stolon buds off medusae which may remain in clusters or may
separate off completely. In the siphonophore, Halistemma, the planula
separate off completely. In the siphonophore, Halistemma, the planula
develops an ectodermal thickening at the aboral pole which develops
develops an ectodermal thickening at the aboral pole which develops
into the pneumatophore or float. Part of the planula becomes the
into the pneumatophore or float. Part of the planula becomes the
eoenosarcal axis from which spring buds which become several different
eoenosarcal axis from which spring buds which become several different
kinds of individuals. Those near the float are bell-shaped medusae,
kinds of individuals. Those near the float are bell-shaped medusae,
through whose efforts the colony is enabled to swim. Next come a series
through whose efforts the colony is enabled to swim. Next come a series
of covering scales which seem to be retrogressed medusae; they are pro-
of covering scales which seem to be retrogressed medusae; they are protective in function. At various places along the coenosarc are feeding
tective in function. At various places along the coenosarc are feeding
tubes in general similar to a hydranth. The tentacles and feelers also
tubes in general similar to a hydranth. The tentacles and feelers also
are probably to be looked upon as hydranths. Finally there are the
are probably to be looked upon as hydranths. finally there are the
reproductive individuals which resemble certain types of medusae.
reproductive individuals which resemble certain types of medusae.


Line 11,950: Line 11,064:
the hydrozoa directly results in the formation of colonies. All hydroids
the hydrozoa directly results in the formation of colonies. All hydroids
which bud form colonies. Usually the planula develops directly into
which bud form colonies. Usually the planula develops directly into
the first hydranth and the colony is formed by the subsequent branching
the first hydranth and the colony is formed by the subsequent branching
and budding. This brings about in all except the simplest cases a very
and budding. This brings about in all except the simplest cases a very
considerable degree of polymorphism. There are defensive and sensory
considerable degree of polymorphism. There are defensive and sensory
individuals and in these the cnidoblasts are well developed. The gonanth
individuals and in these the cnidoblasts are well developed. The gonanth
or gonangium has for its purpose the function of reproduction, and
or gonangium has for its purpose the function of reproduction, and
various modifications of gonangia are to be found throughout the group.
various modifications of gonangia are to be found throughout the group.
Medusae which are free swimming show a greater degree of differentia-
Medusae which are free swimming show a greater degree of differentiation than any of the other types of individuals produced in a hydroid
tion than any of the other types of individuals produced in a hydroid
colony. There are, however, numbers of medusa forms in which the
colony. There are, however, numbers of medusa forms in which the
development is incomplete, and some of them are quite simple in
development is incomplete, and some of them are quite simple in
structure. As an accompaniment to the more complex polymorphism
structure. As an accompaniment to the more complex polymorphism
which we find in these colonies metagenesis, the alternation of genera-
which we find in these colonies metagenesis, the alternation of generations, is perhaps shown here to a degree of completeness that scarcely
tions, is perhaps shown here to a degree of completeness that scarcely
exists elsewhere in the animal kingdom. The sexual functions are transferred to certain individuals while others specialize along the lines of
exists elsewhere in the animal kingdom. The sexual functions are trans-
ferred to certain individuals while others specialize along the lines of
feeding and protecting the colony. Hydroid colonies not uncommonly
feeding and protecting the colony. Hydroid colonies not uncommonly
reproduce by another asexual method, namely stolonization. From the
reproduce by another asexual method, namely stolonization. From the
Line 11,970: Line 11,081:


hydrorhiza of the original polyp cylindrical projections grow out which
hydrorhiza of the original polyp cylindrical projections grow out which
elongate, creep about on the bottom and may branch or even anasto-
elongate, creep about on the bottom and may branch or even anastomose. These are stolons or runners upon which new hydranth buds
mose. These are stolons or runners upon which new hydranth buds
appear to produce new individuals. Bougainvillia and Clavularia both
appear to produce new individuals. Bougainvillia and Clavularia both
serve as illustrations of colonies which grow by stolon formation.
serve as illustrations of colonies which grow by stolon formation.


In the second class of coelenterates, the Anthozoa, transverse fission
In the second class of coelenterates, the Anthozoa, transverse fission
occasionally occurs in young animals which have not yet developed sex
occasionally occurs in young animals which have not yet developed sex
organs. In Fungia as described by Bourne, the development of the larva
organs. In Fungia as described by Bourne, the development of the larva
at a certain stage results in the separation of its distal part and after a
at a certain stage results in the separation of its distal part and after a
complicated series of processes two individuals are produced. Longi-
complicated series of processes two individuals are produced. Longitudinal fission is common among the Anthozoa. It is a slow process
tudinal fission is common among the Anthozoa. It is a slow process
beginning at the oral pole in some cases, although in Actinia it may take
beginning at the oral pole in some cases, although in Actinia it may take
place simultaneously from the aboral as well. In the adult Sagartia and
place simultaneously from the aboral as well. In the adult Sagartia and
Line 11,986: Line 11,095:
course of twenty-four hours to the oral region. In some others it is much
course of twenty-four hours to the oral region. In some others it is much
more rapid. Furthermore the constriction of one individual to produce
more rapid. Furthermore the constriction of one individual to produce
several at the same time may take place. In this case the resulting in-
several at the same time may take place. In this case the resulting individuals will be of varying size, and it has been observed that one
dividuals will be of varying size, and it has been observed that one
division may not even be completed before a new one begins. Strange
division may not even be completed before a new one begins. Strange
complications thus arise in which the individuals may have several
complications thus arise in which the individuals may have several
mouths or several systerrs of septa at the same time owing to this
mouths or several systerrs of septa at the same time owing to this
multiple fission. In the Anthozoa irregular longitudinal fission sometimes
multiple fission. In the Anthozoa irregular longitudinal fission sometimes
gives the appearance of budding. True budding, however, is rarely met
gives the appearance of budding. True budding, however, is rarely met
with in the sea anemones. In the alcyonarians, however, much-branched
with in the sea anemones. In the alcyonarians, however, much-branched
colonies are formed by budding and the individuals undergo modifica-
colonies are formed by budding and the individuals undergo modification and even produce a very considerable polymorphism. The Zoantharia likewise owe their extremely complicated type of development
tion and even produce a very considerable polymorphism. The Zoan-
to both fission and budding. In both these latter groups stolon formation
tharia likewise owe their extremely complicated type of development
to both fission and budding. In both these latter groups stolon formation
and subsequent budding are commonly observed.
and subsequent budding are commonly observed.


One of the most striking forms of asexual reproduction is that mani-
One of the most striking forms of asexual reproduction is that manifested by the scyphozoa in the process of strobilization. This has already
fested by the scyphozoa in the process of strobilization. This has already
been described in the chapter on “Types of Invertebrate Larvae.” The
been described in the chapter on “Types of Invertebrate Larvae.” The
planula develops into a hydranth-like form called the scyphistoma. By
planula develops into a hydranth-like form called the scyphistoma. By
Line 12,017: Line 11,122:
already indicated by constrictions before the upper ones have progressed
already indicated by constrictions before the upper ones have progressed
to any considerable degree of independence. It would seem that the
to any considerable degree of independence. It would seem that the
distinction between terminal budding and transverse fission in this
distinction between terminal budding and transverse fission in this
case is a difligult one to draw. The scyphistoma also for a considerable
case is a difligult one to draw. The scyphistoma also for a considerable
part of the year produces other scyphistomae by lateral budding in a
part of the year produces other scyphistomae by lateral budding in a
manner similar to that in Hydra. All at length, however, undergo strobili—
manner similar to that in Hydra. All at length, however, undergo strobili—
zation and produce ephyrae which gradually develop into adult jellyfish.
zation and produce ephyrae which gradually develop into adult jellyfish.
In certain scyphozoans another type of asexual reproduction occurs in
In certain scyphozoans another type of asexual reproduction occurs in
the formation of stolons from the original hydranth. They grow out
the formation of stolons from the original hydranth. They grow out
Line 12,037: Line 11,142:
anemones may at length regenerate, although the ability to do so is
anemones may at length regenerate, although the ability to do so is
dependent upon the number of septa present. Frustulation occurs in
dependent upon the number of septa present. Frustulation occurs in
the hydroids. Occasionally a small bud-like branch is observed to con-
the hydroids. Occasionally a small bud-like branch is observed to constrict off from the parent colony, to settle down on the bottom in which
strict off from the parent colony, to settle down on the bottom in which
condition it is called the frustulum, to grow and to produce a hydranth.
condition it is called the frustulum, to grow and to produce a hydranth.
In hydranths also a process somewhat similar to laceration has been
In hydranths also a process somewhat similar to laceration has been
Line 12,044: Line 11,148:
basal portion of the polyp is cut off and may develop into a young polyp.
basal portion of the polyp is cut off and may develop into a young polyp.


A final question in connection with the coelenterates naturally arises
A final question in connection with the coelenterates naturally arises
as to which condition is the more primitive. There are three possibilities:
as to which condition is the more primitive. There are three possibilities:
one, that budding is the primitive type of asexual reproduction; two,
one, that budding is the primitive type of asexual reproduction; two,
that fission is primitive; and three, that both arose independently of
that fission is primitive; and three, that both arose independently of
each other. There have been interesting discussions of this question
each other. There have been interesting discussions of this question
and transitions between them have been pointed out. It need only be
and transitions between them have been pointed out. It need only be
Line 12,053: Line 11,157:


Platyhelminthes. In the phylum Platyhelminthes the dominant type
Platyhelminthes. In the phylum Platyhelminthes the dominant type
of asexual reproduction is fission, although there are also causes of
of asexual reproduction is fission, although there are also causes of
budding. It is most common among the Turbellaria, although the poly-
budding. It is most common among the Turbellaria, although the polyclads have not been shown to reproduce asexually. Undoubtedly the
clads have not been shown to reproduce asexually. Undoubtedly the
phenomenon of asexual reproduction in this division of the animal
phenomenon of asexual reproduction in this division of the animal
kingdom is closely concerned with the ability which all members of the
kingdom is closely concerned with the ability which all members of the
phylum have for extensive regeneration. In its simplest form, as for
phylum have for extensive regeneration. In its simplest form, as for
example, in the triclads, Planaria abissima and P. alpina, the reproduc-
example, in the triclads, Planaria abissima and P. alpina, the reproducPLATYHELMINTHES 305
PLATYHELMINTHES 305


tion really consists in the separating of the animal by transverse fission
tion really consists in the separating of the animal by transverse fission
into two portions each of which proceeds to regenerate the missing head
into two portions each of which proceeds to regenerate the missing head
or tail. In Planaria all the species described show that regeneration may
or tail. In Planaria all the species described show that regeneration may
take place at various levels proceed-
take place at various levels proceeding from the anterior to the posterior.
ing from the anterior to the posterior.
An area of regenerating tissue
An area of regenerating tissue
appears which enlarges and then
appears which enlarges and then
differentiates. Sometimes a second
differentiates. Sometimes a second
fission makes its appearance before
fission makes its appearance before
the complete regeneration following
the complete regeneration following
the first, and indeed there are re-
the first, and indeed there are recorded cases of several divisions with
corded cases of several divisions with
the appropriate organs already developing before the first is completed.
the appropriate organs already de-
veloping before the first is completed.


Among the rhabdocoels fission is
Among the rhabdocoels fission is
an even more general phenomenon.
an even more general phenomenon.
The small fresh-water M zcrostoma
The small fresh-water M zcrostoma
reproduces mainly by fission. Com-
reproduces mainly by fission. Commonly this process occurs before the
monly this process occurs before the
young have developed sex organs in
young have developed sex organs in
this form and in Stentostoma, and the
this form and in Stentostoma, and the
Line 12,090: Line 11,188:
very slowly, that is, a zone of division
very slowly, that is, a zone of division
is prepared and the organs of the new
is prepared and the organs of the new
portion of the animal are already de-
portion of the animal are already developed to a considerable extent
veloped to a considerable extent
when constriction occurs. If the constrictions follow each other more
when constriction occurs. If the con-
strictions follow each other more
rapidly they come under the category
rapidly they come under the category
of architomy, no special region being A
of architomy, no special region being A
prepared in advance. The distinction pm 195
prepared in advance. The distinction pm 195


S\l(‘('(“§‘\l\(‘ lI‘f'lH§V€l'EaC fis-
S\l(‘('(“§‘\l\(‘ lI‘f'lH§V€l'EaC fis
 
betwcon pal-altolny and 3'1-chit/Oxny sions 111 (A) Stuwstmnum SM-boldi, and
betwcon pal-altolny and 3'1-chit/Oxny sions 111 (A) Stuwstmnum SM-boldi, and


. (B) '11 trrnslomum lmcarr (From Kor-
. (B) '11 trrnslomum lmcarr (From Kormay perhaps be made clear by Saylng schelt and Holder after v Grofi )
may perhaps be made clear by Saylng schelt and Holder after v Grofi )


that the regeneration Of the new Pharvnx is shown for each single in-
that the regeneration Of the new Pharvnx is shown for each single inorgans precedes the actual fission in dividual, and the dn 131 111 planes of the
organs precedes the actual fission in dividual, and the dn 131 111 planes of the


_ different ranks are numbered
_ different ranks are numbered
paratomy, no great change in the
paratomy, no great change in the


organization of the animal taking place at the exact moment of di-
organization of the animal taking place at the exact moment of division. On the other hand, in architomy, regeneration and subsequent
vision. On the other hand, in architomy, regeneration and subsequent
reorganization follow the constriction.
reorganization follow the constriction.
306 ASEXU AL REPRODUCTION
306 ASEXU AL REPRODUCTION
Line 12,119: Line 11,211:
never occurs in any individuals which have a complete set of sex organs.
never occurs in any individuals which have a complete set of sex organs.
The situation with regard to the germ balls which produce the rediae
The situation with regard to the germ balls which produce the rediae
has already been referred to in connection with the chapter on in-
has already been referred to in connection with the chapter on in
 
vertebrate larvae and also that on polyembryony. It is still looked upon
vertebrate larvae and also that on polyembryony. It is still looked upon
as an open question as to whether parthenogenesis or asexual repro-
as an open question as to whether parthenogenesis or asexual reproduction is the method by which the germ ball that forms the new rediae
duction is the method by which the germ ball that forms the new rediae
is produced. It has been pointed out that originally they
is produced. It has been pointed out that originally they
were regarded as asexually produced, more recently as
were regarded as asexually produced, more recently as
developed in parthenogcnie ova, and finally that the
developed in parthenogcnie ova, and finally that the
cytological study of these supposed ova has not yet
cytological study of these supposed ova has not yet
shown evidence of a reduction division such as would
shown evidence of a reduction division such as would
be necessary to establish surely the fact of their parthen-
be necessary to establish surely the fact of their parthenogenic nature. If we are to regard them as asexually
ogenic nature. If we are to regard them as asexually
produced then this type becomes of much more widespread occurrence among the trematodes than is usually
produced then this type becomes of much more wide-
spread occurrence among the trematodes than is usually
considered.
considered.


Line 12,138: Line 11,226:
question of asexual reproduction. One has to do with the
question of asexual reproduction. One has to do with the
formation of the proglottids from the scolex, the other
formation of the proglottids from the scolex, the other
with multiplication of the eysticercus. The first of these
with multiplication of the eysticercus. The first of these
involves a decision as to the fundamental nature of the
involves a decision as to the fundamental nature of the
proglottids. Is the tapeworm to be looked upon as a
proglottids. Is the tapeworm to be looked upon as a
colony of individuals or as a single one? If the latter
colony of individuals or as a single one? If the latter


FIG 199 * view is taken there eanof course be noquestion of asexual
fiG 199 * view is taken there eanof course be noquestion of asexual


fzvsli::;:::;;::)‘lf,? reproduction involved. If on the other hand the pro~
fzvsli::;:::;;::)‘lf,? reproduction involved. If on the other hand the pro~
Line 12,151: Line 11,239:
S°°l°°°5 “"3 to live at least for some time after the separation from
S°°l°°°5 “"3 to live at least for some time after the separation from
present in both _ _
present in both _ _
(From Korschelt the remainder of the worm, then its method of forma-
(From Korschelt the remainder of the worm, then its method of forma;‘3';‘:tI){°'d°" “Mr tion must be looked upon as budding, it being thus
;‘3';‘:tI){°'d°" “Mr tion must be looked upon as budding, it being thus


. produced from the scolex. It is the writer’s opinion that
. produced from the scolex. It is the writer’s opinion that
Line 12,166: Line 11,253:
cavity and later this bud-like structure is cverted to form the little worm.
cavity and later this bud-like structure is cverted to form the little worm.


It occasionally happens that two or more scoleces are formed by bud-
It occasionally happens that two or more scoleces are formed by budPOLYZOA 307
POLYZOA 307


like thickenings on the wall of the same bladder. This multiple produc-
like thickenings on the wall of the same bladder. This multiple production of scolices is rather rare but occurs regularly as is well known in
tion of scolices is rather rare but occurs regularly as is well known in
Taenia echinococcus with disastrous results to the host. This is of course
Taenia echinococcus with disastrous results to the host. This is of course
reproduction by budding. In some forms the bladders themselves may
reproduction by budding. In some forms the bladders themselves may
Line 12,179: Line 11,264:
borne out. Three asexual methods, as well as polyembryony, are found
borne out. Three asexual methods, as well as polyembryony, are found
here. They are budding, stolonization, and the formation of statoblasts.
here. They are budding, stolonization, and the formation of statoblasts.
As a manifestation of the complicated condition which asexual repro-
As a manifestation of the complicated condition which asexual reproduction may reach in a single group, the Bryozoa probably exceed any
duction may reach in a single group, the Bryozoa probably exceed any
other branch of the animal kingdom. A student of the subject will find
other branch of the animal kingdom. A student of the subject will find
much to interest him in the group and may expect to see an everchanging variety of detail as he studies the different divisions of it. For
much to interest him in the group and may expect to see an ever-
changing variety of detail as he studies the different divisions of it. For


   
   
Line 12,191: Line 11,274:
ee , ectoderm, m., mesoderm.
ee , ectoderm, m., mesoderm.


the general student of comparative embryology, however, it seems un-
the general student of comparative embryology, however, it seems unnecessary to give more than a very brief consideration to the general
necessary to give more than a very brief consideration to the general
types of asexual reproduction as they are developed here. From a consultation of the table of classification on page 260 the student will
types of asexual reproduction as they are developed here. From a con-
sultation of the table of classification on page 260 the student will
observe that the phylum Molluscoidea, of which the Polyzoa are a
observe that the phylum Molluscoidea, of which the Polyzoa are a
portion, consists of animals very diverse in structure and in their
portion, consists of animals very diverse in structure and in their
Line 12,201: Line 11,282:
the simplest genera is Cristatella, coming under the ectoproct order,
the simplest genera is Cristatella, coming under the ectoproct order,
Phylactolaemata. All the individuals of a colony of this form can be
Phylactolaemata. All the individuals of a colony of this form can be
traced to the first one which develops from the larva. This individual
traced to the first one which develops from the larva. This individual
produces buds commonly as thickenings of the pharynx on the oral
produces buds commonly as thickenings of the pharynx on the oral
side, both ectoderm and mesoderm participating in the process, although
side, both ectoderm and mesoderm participating in the process, although
Line 12,213: Line 11,294:
is involved in the production of the colony. The development of buds in
is involved in the production of the colony. The development of buds in
the Endoprocta closely resembles that just described. The bud is first
the Endoprocta closely resembles that just described. The bud is first
an enlargement of eetoderinal cells which receives migrations of meso-
an enlargement of eetoderinal cells which receives migrations of meso
 
W
W


Line 12,249: Line 11,329:
to be expected. Special morphological changes take place so that some
to be expected. Special morphological changes take place so that some
of the individuals of the colony become very much changed from the
of the individuals of the colony become very much changed from the
typical form and have very different functions. The Bryozoa. always re-
typical form and have very different functions. The Bryozoa. always reproduce by sending out stolons which then bud many times. The formation
produce by sending out stolons which then bud many times. The formation
of the stolon itself is like that of the bud but it grows out as a stalk which
of the stolon itself is like that of the bud but it grows out as a stalk which


Line 12,264: Line 11,343:
winter buds, club-like swellings on the stolons which enclose themselves
winter buds, club-like swellings on the stolons which enclose themselves
in a cutaneous capsule during the period of severe winter. In the spring
in a cutaneous capsule during the period of severe winter. In the spring
their development continues to form new colonies. Accidental sub-
their development continues to form new colonies. Accidental subdivision of a colony is of course common, but the multiplication of the
division of a colony is of course common, but the multiplication of the
colony by fragmentation appears also to occur naturally.
colony by fragmentation appears also to occur naturally.


FIG. 203. Production of zooecia ns buds from stolons (st.) of Pedicellina erhinala.
fiG. 203. Production of zooecia ns buds from stolons (st.) of Pedicellina erhinala.
(From Korschelt and Heider, after Ehlors.)
(From Korschelt and Heider, after Ehlors.)


Line 12,274: Line 11,352:
According to an old view a statoblast is supposed to arise from a single
According to an old view a statoblast is supposed to arise from a single
cell and upon the basis of this it was thought to be a sort of winter egg.
cell and upon the basis of this it was thought to be a sort of winter egg.
It is now realized that the statoblasts are modified buds which have
It is now realized that the statoblasts are modified buds which have
become changed into reproductive buds. They vary in shape, but are
become changed into reproductive buds. They vary in shape, but are
enclosed in a cutaneous capsule and contain several cells. They are
enclosed in a cutaneous capsule and contain several cells. They are
Line 12,305: Line 11,383:
C
C
‘SIN! _
‘SIN! _
.. " ifl‘-Jijurvl
.. " ifl‘-Jijurvl
‘ .u1l1“‘L4“ .
‘ .u1l1“‘L4“ .


Line 12,323: Line 11,401:
   
   


FIG. 206. Germinating statoblasts of Cristatella. (From Korschelt and Heidcr, after
fiG. 206. Germinating statoblasts of Cristatella. (From Korschelt and Heidcr, after
Braem.)
Braem.)


Line 12,333: Line 11,411:
   
   


FIG. 207. Posterior end of Trypanosyllis misakiensis showing buds of difierent ranks.
fiG. 207. Posterior end of Trypanosyllis misakiensis showing buds of difierent ranks.
(From Korschelt and Heidor. after Johnson.)
(From Korschelt and Heidor. after Johnson.)


end is a reproductive zone where the budding oil’ of new individuals
end is a reproductive zone where the budding oil’ of new individuals
takes place. The first individual budded off is of course the most posterior
takes place. The first individual budded off is of course the most posterior
3 12 ASEXUAL REPROD1 'C'l‘ION
3 12 ASEXUAL REPROD1 'C'l‘ION


Line 12,349: Line 11,427:
produces numerous buds in all
produces numerous buds in all
directions differing in age but
directions differing in age but
,.,:‘:.:-as *;:::r;..:" Merwisc giving the W231‘-
,.,:‘:.:-as *;:::r;..:" Merwisc giving the W231‘(Fmm Komheltamui ance of a rosette of small zooids.
(Fmm Komheltamui ance of a rosette of small zooids.
after v. Kenr}x]<:)l.) Between these two extremes lie
after v. Kenr}x]<:)l.) Between these two extremes lie
gen‘: 0,  S ‘V various degreesof complication
gen‘: 0,  S ‘V various degreesof complication
in the forms produced. In many
in the forms produced. In many
marine polychaetes a differentiation with respect to
marine polychaetes a differentiation with respect to
reproductive capacity is observed between the (lif-
reproductive capacity is observed between the (lif
 
ferent parts of the animal. The anterior portion of
ferent parts of the animal. The anterior portion of


Line 12,371: Line 11,447:
El ‘ W _ out on them, developing
El ‘ W _ out on them, developing


lllllllll  them for rapid and exten-
lllllllll  them for rapid and exten
 
sive movement. This sexual
sive movement. This sexual


Line 12,381: Line 11,456:
this kind were earlier given
this kind were earlier given


special systematic descrip-
special systematic descrip
 
tions. It is now clear, how
tions. It is now clear, how-
ever, that N ereis, for ex— Fm- 209. Diu. grains to show the
 
ever, that N ereis, for ex— Fm- 209. Diu-
. grains to show the


ample; passes Over "Ito divisions zones in
ample; passes Over "Ito divisions zones in


H eteronereis or the epito— £0": hmlzaa. d(FIr{or}1
H eteronereis or the epito— £0": hmlzaa. d(fir{or}1
- . . t -
- . . t kous stage. In many po1.v- dfflfnir c‘L'how..,°.3
kous stage. In many po1.v- dfflfnir c‘L'how..,°.3
 
chaetes, the epitokous por-


chaetes, the epitokous por
tion separates from the remainder and swims
tion separates from the remainder and swims
  : ' , ' ' d t th —
  : ' , ' ' d t th —
Line 12,416: Line 11,486:
group may he based upon the degree of preparation which precedes
group may he based upon the degree of preparation which precedes


FIG. 211. J! yriamda fumata with 29 zooids. (From Korscholt and Heider. after
fiG. 211. J! yriamda fumata with 29 zooids. (From Korscholt and Heider. after
Maluquin.)
Maluquin.)


Line 12,428: Line 11,498:
pointed out this regeneration after division is known as architomy in
pointed out this regeneration after division is known as architomy in
contradistinction to paratomy where a. separation zone is developed
contradistinction to paratomy where a. separation zone is developed
before division. Such a zone is really the beginning of an early regenera-
before division. Such a zone is really the beginning of an early regeneration and may be present in variable degrees all the way from a simple
tion and may be present in variable degrees all the way from a simple
region of constriction to the formation of a well—developed head and
region of constriction to the formation of a well—developed head and
sensory apparatus.
sensory apparatus.
Line 12,437: Line 11,506:
by constriction and the lacking parts
by constriction and the lacking parts
are regenerated. Regeneration begins
are regenerated. Regeneration begins
at once, although the new worms con-
at once, although the new worms continue to creep about actively in spite of
tinue to creep about actively in spite of
the fact that they cannot for a short
the fact that they cannot for a short
while take in food. Architomy may be
while take in food. Architomy may be
Line 12,445: Line 11,513:
and oligochaetes have such great powers
and oligochaetes have such great powers
of regeneration that they are enabled
of regeneration that they are enabled
to separate without external stimula-
to separate without external stimulation. Lumbnculus is an annelid of this
tion. Lumbnculus is an annelid of this
type.
type.


Line 12,457: Line 11,524:


Fm 012 Tami”: mulomm with a back of the head, cellular prolrferations
Fm 012 Tami”: mulomm with a back of the head, cellular prolrferations
pnmaw" ,e;;(.,,e,a,,,,g Dome" and mo takeplacewhichgraduallyformthicken-
pnmaw" ,e;;(.,,e,a,,,,g Dome" and mo takeplacewhichgraduallyformthicken ings on the anterior side of each segment.
  ings on the anterior side of each segment.


' They become the head folds and give
' They become the head folds and give
rise to the organs of the head region in the new zooids. Thus a chain of
rise to the organs of the head region in the new zooids. Thus a chain of
zooids is formed asexually. Additions of this sort produce what is function-
zooids is formed asexually. Additions of this sort produce what is functionally an alternation of generations. It is scarcely developed with the
ally an alternation of generations. It is scarcely developed with the
regularity that characterizes this process in such forms as hydroids. The
regularity that characterizes this process in such forms as hydroids. The
original individual was developed from the egg. It produces asexually
original individual was developed from the egg. It produces asexually
a chain of zooids which separate from each other and when weather
a chain of zooids which separate from each other and when weather
conditions become suitable develop further into individuals which re-
conditions become suitable develop further into individuals which reproduce sexually. Of course second and third asexual generations may
produce sexually. Of course second and third asexual generations may
be produced in the same manner as the first one.
be produced in the same manner as the first one.
PTEROBRANCHIA 315
PTEROBRANCHIA 315


Echinodermata. Among the echinoderms asexual reproduction is
Echinodermata. Among the echinoderms asexual reproduction is
described, but it is certainly of rare occurrence and one has difliculty in
described, but it is certainly of rare occurrence and one has difliculty in
distinguishing it from an extreme type of regeneration. Spontaneous
distinguishing it from an extreme type of regeneration. Spontaneous
division of the arms and in some cases the splitting of the disc have been
division of the arms and in some cases the splitting of the disc have been
Line 12,479: Line 11,543:
have been seen to split and separate, beginning at the gullet, and then
have been seen to split and separate, beginning at the gullet, and then


Flu. 213. S1/Ilis ramosa showing anterior end of worm and the complex branching. The
flu. 213. S1/Ilis ramosa showing anterior end of worm and the complex branching. The
gut is stippled in the figure. (From Korsehelt and Heidor. after Maclntosh.)
gut is stippled in the figure. (From Korsehelt and Heidor. after Maclntosh.)


Line 12,486: Line 11,550:
of an echinoderm is brought about extensive regenerations follow and
of an echinoderm is brought about extensive regenerations follow and
theoretically there is no great difference between this and a natural
theoretically there is no great difference between this and a natural
type of division followed by regeneration. However, the latter is cer-
type of division followed by regeneration. However, the latter is certainly of earlier occurrence.
tainly of earlier occurrence.


Pterobranchia. The two genera Cephalodiscus and Rhabdopleura which
Pterobranchia. The two genera Cephalodiscus and Rhabdopleura which
compose the anomalous Pterobranchia both illustrate asexual reproduc-
compose the anomalous Pterobranchia both illustrate asexual reproduc316 ASEXUAL REPRODUCTION
316 ASEXUAL REPRODUCTION


tion by budding. Their doubtful position showing similarities both to
tion by budding. Their doubtful position showing similarities both to
Line 12,497: Line 11,559:
of reproduction. Cephalodiscus occurs as a single individual from the
of reproduction. Cephalodiscus occurs as a single individual from the
side of which a stalk grows out. This stalk bears a bud as is shown in
side of which a stalk grows out. This stalk bears a bud as is shown in
the well-known figure often copied from Maclntosh. The bud arises from
the well-known figure often copied from Maclntosh. The bud arises from
the apex of the ventral stalk and after a certain age breaks off. The
the apex of the ventral stalk and after a certain age breaks off. The
animal lives in a gelatinous coenoecium where a large number of free
animal lives in a gelatinous coenoecium where a large number of free
individuals may be found. The animal possesses practically all the
individuals may be found. The animal possesses practically all the
important organs found in Balanoglossus and structurally seems re-
important organs found in Balanoglossus and structurally seems related to that form. Its method of asexual reproduction, however, much
lated to that form. Its method of asexual reproduction, however, much
more strongly resembles that of the Polyzoa. Resemblance to the latter
more strongly resembles that of the Polyzoa. Resemblance to the latter
group is rather more striking in Rhabdopleura which lives in a tube and
group is rather more striking in Rhabdopleura which lives in a tube and
Line 12,508: Line 11,569:
of the stoloniferous Bryozoa. The general
of the stoloniferous Bryozoa. The general
anatomy, however, closely resembles that
anatomy, however, closely resembles that
of Cephalodiscus. In Rhabdopleura the in-
of Cephalodiscus. In Rhabdopleura the individuals derived from the buds remain
dividuals derived from the buds remain
close together and form small colonies
close together and form small colonies
living in branched tubes. They are con—
living in branched tubes. They are con—
Line 12,516: Line 11,576:
The cord is the narrowed proximal portion
The cord is the narrowed proximal portion
of the body. By its contraction the animal
of the body. By its contraction the animal
is retracted into a stalk. The stolen is de-
is retracted into a stalk. The stolen is developed as a bud from the original zooid,
veloped as a bud from the original zooid,


1«'.c.. 214. ('c1)Iw,lod£scus with but the details of the process are not well
1«'.c.. 214. ('c1)Iw,lod£scus with but the details of the process are not well
Line 12,532: Line 11,591:
divisions of this subphylum, the composite ascidians and the salps.
divisions of this subphylum, the composite ascidians and the salps.
The dominant type is budding but the details show various departures
The dominant type is budding but the details show various departures
from the simple form and even instances of fission are observed within
from the simple form and even instances of fission are observed within
this group. It will perhaps serve our purpose to limit our discussion to
this group. It will perhaps serve our purpose to limit our discussion to
the budding in the two cases mentioned, understanding that there are
the budding in the two cases mentioned, understanding that there are
some other minor examples to be met with in this group. The embry-
some other minor examples to be met with in this group. The embryology of the ascidians has been described in Part One of this book. The
ology of the ascidians has been described in Part One of this book. The
young embryo grows and in many cases begins its process of budding
young embryo grows and in many cases begins its process of budding
TUNICATA
TUNICATA
Line 12,542: Line 11,600:
317
317


before it has become attached and begun its metamorphosis. It is custom-
before it has become attached and begun its metamorphosis. It is customary to speak of the individual which is produced from the egg as an
ary to speak of the individual which is produced from the egg as an
oozooid whereas the individuals which are produced from buds are
oozooid whereas the individuals which are produced from buds are
blastozooids. However, the individuals so called may become modified
blastozooids. However, the individuals so called may become modified


in various ways and be given other names to in-
in various ways and be given other names to indicate functional and morphological differences
dicate functional and morphological differences
which later occur, for budding in the tunicates as in
which later occur, for budding in the tunicates as in
some other groups leads to polymorphism and to
some other groups leads to polymorphism and to
Line 12,565: Line 11,621:
symmetrical parts, but usually only one of them
symmetrical parts, but usually only one of them
develops. Mesoderm and germ cells migrate from
develops. Mesoderm and germ cells migrate from
the tissues of the mother into the bud which gradu-
the tissues of the mother into the bud which gradually becomes a complete individual. The processes
ally becomes a complete individual. The processes
are the same in the asexually produced blastozooid
are the same in the asexually produced blastozooid
and in the oozooid which are developed from the
and in the oozooid which are developed from the
egg, but the oozooid undergoes a retardation in de-
egg, but the oozooid undergoes a retardation in development and never reaches sexual maturity
velopment and never reaches sexual maturity
whereas the blastozooid develops fully although it
whereas the blastozooid develops fully although it
is to be noted that both may reproduce asexually
is to be noted that both may reproduce asexually
Line 12,598: Line 11,652:


been produced the mass takes on the form of buds united into a very
been produced the mass takes on the form of buds united into a very
definite system built upon the plan of concentric circles of buds. As
definite system built upon the plan of concentric circles of buds. As
the system becomes more and more complicated some of the individuals
the system becomes more and more complicated some of the individuals
become crowded out of their proper place and so become the center of
become crowded out of their proper place and so become the center of
a new irregular subdivision of buds. In this way a colony is formed.
a new irregular subdivision of buds. In this way a colony is formed.
The place of origin of the buds varies in difierent genera, a fact which
The place of origin of the buds varies in difierent genera, a fact which
318 ASEXUAL REPRODUCTION
318 ASEXUAL REPRODUCTION


Line 12,616: Line 11,670:
derived in the regular manner from the ectoderm. Pyloric budding is
derived in the regular manner from the ectoderm. Pyloric budding is
described chiefly in the didemnids and the diplosomids. Among the
described chiefly in the didemnids and the diplosomids. Among the
modifications of the general type of budding described for the compound
modifications of the general type of budding described for the compound
ascidians are the cases spoken of as pseudo-stolonial, occurring espe-
ascidians are the cases spoken of as pseudo-stolonial, occurring especially in the distomid Distaplia and in the polyclinids. Authorities differ
cially in the distomid Distaplia and in the polyclinids. Authorities differ
in the manner in which they regard the budding of these forms, some
in the manner in which they regard the budding of these forms, some
tracing it to the formation of a stolon and others regarding it as more
tracing it to the formation of a stolon and others regarding it as more
nearly related to the type already described. In Distaplia the formation
nearly related to the type already described. In Distaplia the formation
of the “primordial buds” has been described as coming from the epi-
of the “primordial buds” has been described as coming from the epicardium, but Salensky, Julin, Della Valle, and others have described
cardium, but Salensky, Julin, Della Valle, and others have described
this as a proliferating stolon from the intestine. The first generation
this as a proliferating stolon from the intestine. The first generation
of these buds never develops sex products but later generations of buds
of these buds never develops sex products but later generations of buds
may reproduce sexually. It may be noted that the epicardium is wrongly
may reproduce sexually. It may be noted that the epicardium is wrongly
Line 12,631: Line 11,683:
Actually it is the endodermal element of each bud. In the polyclinids
Actually it is the endodermal element of each bud. In the polyclinids
the budding of the posterior part of the animal resembles horizontal
the budding of the posterior part of the animal resembles horizontal
division, for the caudal part of the larva clongates and constricts, form-
division, for the caudal part of the larva clongates and constricts, forming thorax, abdomen, and post-abdomen; gonads and heart develop in
ing thorax, abdomen, and post-abdomen; gonads and heart develop in
the latter which subsequently segments to form buds. By some this
the latter which subsequently segments to form buds. By some this
entire caudal portion is regarded as a stolon.
entire caudal portion is regarded as a stolon.


As an example of stolonial budding reference may be made to Pero-
As an example of stolonial budding reference may be made to Perophora and to Clavellina. In Clavellina, after its attachment, root—like
phora and to Clavellina. In Clavellina, after its attachment, root—like
processes are sent out from the base giving it a more firm hold. At least
processes are sent out from the base giving it a more firm hold. At least
one of these processes becomes the proliferating stolon (stolo prolzfer).
one of these processes becomes the proliferating stolon (stolo prolzfer).
The stolon consists of the three germ layers in addition to the cellulose
The stolon consists of the three germ layers in addition to the cellulose
Line 12,670: Line 11,720:
      
      


F16. 216 An adult of Clavellma with a stolen and .i young individual budded ofi from
F16. 216 An adult of Clavellma with a stolen and .i young individual budded ofi from
it (From Korschelt and Hcider, after Secliger )
it (From Korschelt and Hcider, after Secliger )


In many respects the most interesting case of asexual reproduction
In many respects the most interesting case of asexual reproduction
in the tunicates is the formation of the Salpa chains from a proliferating
in the tunicates is the formation of the Salpa chains from a proliferating
stoloii. When investigators first began to study Salpa, solitary indi-
stoloii. When investigators first began to study Salpa, solitary individuals were found, and also others which appeared to have a significantly different structure and were connected together like a chain or
viduals were found, and also others which appeared to have a signifi-
cantly different structure and were connected together like a chain or
even a rosette were also occasionally discovered. At length the relation
even a rosette were also occasionally discovered. At length the relation
between the two was made out by the poet, Chamisso, who discovered
between the two was made out by the poet, Chamisso, who discovered
Line 12,689: Line 11,737:
which first arose from the pharyngeal endostyle and is therefore in its
which first arose from the pharyngeal endostyle and is therefore in its
beginning eiidodermal, grows out. As it enlarges, the mesoderm and
beginning eiidodermal, grows out. As it enlarges, the mesoderm and
ectoderm surround it, and finally it becomes a projection from the tunic
ectoderm surround it, and finally it becomes a projection from the tunic
as well. It is a direct continuation of the ectoderm and endoderm of the
as well. It is a direct continuation of the ectoderm and endoderm of the


Line 12,702: Line 11,750:
   
   


FIG 217. Nearly adult stages of Dolwlum dentwulatum (From Korschclt and H0|d(‘r,
fiG 217. Nearly adult stages of Dolwlum dentwulatum (From Korschclt and H0|d(‘r,
after Neumann.)
after Neumann.)


Line 12,717: Line 11,765:
familiar to students. As in the compound ascidians the oozooid produces
familiar to students. As in the compound ascidians the oozooid produces
no sexual organs but a great many buds arise from it in a complicated
no sexual organs but a great many buds arise from it in a complicated
manner and the chain thus produced exhibits a high degree of poly-
manner and the chain thus produced exhibits a high degree of polyVERTEBRATA 321
VERTEBRATA 321


morphism. Indeed, the oozooid itself degenerates until it becomes
morphism. Indeed, the oozooid itself degenerates until it becomes
Line 12,728: Line 11,775:
cells become specially suited for the attachment and nourishment of
cells become specially suited for the attachment and nourishment of
the migrating buds which will presently reach it. As a matter of fact,
the migrating buds which will presently reach it. As a matter of fact,
however, there are more buds in the dorsal cadophore than were pro-
however, there are more buds in the dorsal cadophore than were produced from the ventral stolon, multiplication in the form of a simple
duced from the ventral stolon, multiplication in the form of a simple
division having taken place during the migration. The cadophore continues its growth and more and more buds are attached to it. They
division having taken place during the migration. The cadophore con-
tinues its growth and more and more buds are attached to it. They
arrange themselves in two lateral rows and one dorsal median row.
arrange themselves in two lateral rows and one dorsal median row.
The lateral blastozooids which are attached by a short stalk are nu-
The lateral blastozooids which are attached by a short stalk are nutritive and respiratory. They are apparently unable to reproduce
tritive and respiratory. They are apparently unable to reproduce
and are morphologically independent of the rest of the colony. The
and are morphologically independent of the rest of the colony. The
median blastozooids are spoken of as nurse individuals, or phorozooids.
median blastozooids are spoken of as nurse individuals, or phorozooids.
Line 12,760: Line 11,804:
Here a blastocyst is formed as a result of the cleavage of the egg which
Here a blastocyst is formed as a result of the cleavage of the egg which
produces by budding four individuals. This is, of course, an asexual
produces by budding four individuals. This is, of course, an asexual
method of multiplication, and may be of general significance, as is
method of multiplication, and may be of general significance, as is
suggested by the production of identical twins in various other forms
suggested by the production of identical twins in various other forms
of mammals.
of mammals.
Line 12,780: Line 11,824:
cytological and genetical interest for we are here dealing with uniparcntal
cytological and genetical interest for we are here dealing with uniparcntal
inheritance and it is obvious that the chromosomal mechanism which
inheritance and it is obvious that the chromosomal mechanism which
explains the inheritance of bisexual forms must undergo some modifica-
explains the inheritance of bisexual forms must undergo some modification to account for the appearances in unisexual organisms. While the
tion to account for the appearances in unisexual organisms. While the
cytological and genetieal aspects of parthenogenesis are closely related
cytological and genetieal aspects of parthenogenesis are closely related
to the embryological, we can treat them only briefly and must devote
to the embryological, we can treat them only briefly and must devote
ourselves chiefly to the embryological problems.
ourselves chiefly to the embryological problems.


Confusion sometimes develops in the mind of the student in relation
Confusion sometimes develops in the mind of the student in relation
to parthenogencsis for at first thought one is apt to class all types of
to parthenogencsis for at first thought one is apt to class all types of
uniparental inheritance together and think of parthenogcnesis as a
uniparental inheritance together and think of parthenogcnesis as a
modified asexual type. The fallacy of this conclusion is easily seen,
modified asexual type. The fallacy of this conclusion is easily seen,
however, for parthenogenesis deals with the development of an egg
however, for parthenogenesis deals with the development of an egg
although without the cooperation of a spermatozoon. It is clearly a
although without the cooperation of a spermatozoon. It is clearly a
gametic form of reproduction; its relationships are perhaps more easily
gametic form of reproduction; its relationships are perhaps more easily
understood if we speak consistently of unisexual and bisexual reproduc-
understood if we speak consistently of unisexual and bisexual reproduction. It would perhaps be still clearer to use the terms monogametic
tion. It would perhaps be still clearer to use the terms monogametic
and digametie, although these are not commonly found in the literature.
and digametie, although these are not commonly found in the literature.
The critical point in the evidence that we are here dealing with a second
The critical point in the evidence that we are here dealing with a second
Line 12,809: Line 11,851:
occurrence of parthenogenesis along with the bisexual method in the
occurrence of parthenogenesis along with the bisexual method in the
same species of animal, as for example the bee, and the not uncommon
same species of animal, as for example the bee, and the not uncommon
alternation of the parthenogenetic mode with typical sexual reproduc-
alternation of the parthenogenetic mode with typical sexual reproduction in the course of several generations within the same animal all bear
tion in the course of several generations within the same animal all bear
out the same conclusion. Furthermore, the fact of artificial parthenogenesis, that is, the activation of an egg which would otherwise develop
out the same conclusion. Furthermore, the fact of artificial partheno-
genesis, that is, the activation of an egg which would otherwise develop
only by fertilization, shows that we are dealing with what must be a
only by fertilization, shows that we are dealing with what must be a
modification of the usual type of bisexual reproduction. Artificial par-
modification of the usual type of bisexual reproduction. Artificial parthenogenesis means the initiation of development on the part of the
thenogenesis means the initiation of development on the part of the
egg by chemical or physical stimulation artificially induced to take the
egg by chemical or physical stimulation artificially induced to take the
place of the type of initiation usually to be seen only when the sperm
place of the type of initiation usually to be seen only when the sperm
enters the egg. It is really a study in experimental embryology which
enters the egg. It is really a study in experimental embryology which
Line 12,832: Line 11,871:
sperm, although they usually develop after fertilization. Such cases are
sperm, although they usually develop after fertilization. Such cases are
known as facultative or optional and are of such irregular occurrence
known as facultative or optional and are of such irregular occurrence
in the series as to be of no great embryological significance. Obligatory
in the series as to be of no great embryological significance. Obligatory
parthenogenesis occurs regularly in the life cycle of organisms which
parthenogenesis occurs regularly in the life cycle of organisms which
show it as a constant feature or only at certain intervals. Its importance
show it as a constant feature or only at certain intervals. Its importance
is manifested by the fact that parthenogenetic eggs are often structur-
is manifested by the fact that parthenogenetic eggs are often structurally different from those that are to be fertilized and there are morphological differences between the animals which are produced parthenogenetically and those which are produced bisexually. For instance, the
ally different from those that are to be fertilized and there are morpho-
logical differences between the animals which are produced partheno-
genetically and those which are produced bisexually. For instance, the
eggs of daphnids which are fertilized usually develop only during the
eggs of daphnids which are fertilized usually develop only during the
colder seasons of the year; they are known as winter eggs and have
colder seasons of the year; they are known as winter eggs and have
a protective shell that is very different from the summer eggs. Often-
a protective shell that is very different from the summer eggs. Oftentimes cases of obligatory parthenogenesis show an alternation of
times cases of obligatory parthenogenesis show an alternation of
generations although not of an asexual generation with a sexual, but of
generations although not of an asexual generation with a sexual, but of
a unisexual generation or a series of them, with a bisexual generation.
a unisexual generation or a series of them, with a bisexual generation.
Where this type of development is firmly established a series of par-
Where this type of development is firmly established a series of par
 
thenogenetic generations may be developed to such an extent that it
thenogenetic generations may be developed to such an extent that it
becomes the predominant method of reproduction and sexual genera-
becomes the predominant method of reproduction and sexual genera3 24 PARTHENOGENESIS
3 24 PARTHENOGENESIS


tions appear only at infrequent intervals. Many of the more familiar
tions appear only at infrequent intervals. Many of the more familiar
cases of parthenogenesis are of this type.
cases of parthenogenesis are of this type.


Even in the extreme obligatory type it is often possible by experi-
Even in the extreme obligatory type it is often possible by experimental means to induce the sexual process, for instance, by a change
mental means to induce the sexual process, for instance, by a change
of the environmental conditions. The rotifer, Hydatina senta, as shown
of the environmental conditions. The rotifer, Hydatina senta, as shown
by Shull and by Whitney, in old culture infusions will continue partheno-
by Shull and by Whitney, in old culture infusions will continue parthenogenetically for long periods of time, but if a fresh culture fluid is used
genetically for long periods of time, but if a fresh culture fluid is used
bisexual animals soon make their appearance. Conversely, it is possible
bisexual animals soon make their appearance. Conversely, it is possible
by maintaining appropriate conditions to postpone or even entirely to
by maintaining appropriate conditions to postpone or even entirely to
suppress the sexual process, as in the case of the rose aphid when culti-
suppress the sexual process, as in the case of the rose aphid when cultivated through a series of years in a greenhouse.
vated through a series of years in a greenhouse.


In cases where structural differences are to be observed between the
In cases where structural differences are to be observed between the
parthenogenetic and the bisexually developed eggs, a functional differ-
parthenogenetic and the bisexually developed eggs, a functional difference also is frequently seen in that the eggs of certain individuals are
ence also is frequently seen in that the eggs of certain individuals are
exclusively male producing, that is arrhenotokous, and of others female
exclusively male producing, that is arrhenotokous, and of others female
producing, or thelytokous. Where both males and females are produced
producing, or thelytokous. Where both males and females are produced
Line 12,872: Line 11,901:
number of parthenogenetic generations which occurs before the sexual
number of parthenogenetic generations which occurs before the sexual
animals are produced is indefinite we say that the species has an “open
animals are produced is indefinite we say that the species has an “open
life cycle.” Such cases occur in the aphids and in some species of phyllox-
life cycle.” Such cases occur in the aphids and in some species of phylloxerans. In others the female which produces the parthenogenetic eggs and
erans. In others the female which produces the parthenogenetic eggs and
hence is known as the stem mother must develop directly from the
hence is known as the stem mother must develop directly from the
previous fertilized egg. This is the “ closed ” type, and it occurs in certain
previous fertilized egg. This is the “ closed ” type, and it occurs in certain
other phylloxerans and in the gall flies.
other phylloxerans and in the gall flies.


Considering the embryological aspects we should classify known
Considering the embryological aspects we should classify known
Line 12,889: Line 11,917:
development of the egg without fertilization always produces a male.
development of the egg without fertilization always produces a male.
(d) Partial parthenogenesis. The queen bee by the copulation on the
(d) Partial parthenogenesis. The queen bee by the copulation on the
nuptial flight receives all of the sperm which she will ever use, and
nuptial flight receives all of the sperm which she will ever use, and
afterwards she can fertilize the egg to produce a female, that is, a
afterwards she can fertilize the egg to produce a female, that is, a
worker or a queen, or leave it to develop parthenogenetically into a
worker or a queen, or leave it to develop parthenogenetically into a
Line 12,898: Line 11,926:
CYTOLOGICAL RELATIONSHIPS 325
CYTOLOGICAL RELATIONSHIPS 325


in the chapter on paedogenesis. Some larvae are produced partheno-
in the chapter on paedogenesis. Some larvae are produced parthenogenetically and inside of them others through a number of generations.
genetically and inside of them others through a number of generations.
each eating its way out and producing yet others. finally the last larvae
each eating its way out and producing yet others. Finally the last larvae
pupate, undergo metamorphosis, and develop bisexual forms. (g) Total
pupate, undergo metamorphosis, and develop bisexual forms. (g) Total


parthenogenesis. Only parthenogenetic eggs occur through many genera-
parthenogenesis. Only parthenogenetic eggs occur through many generations as is especially illustrated by the rotifers.
tions as is especially illustrated by the rotifers.


b. Cytological Relationships. A consideration of the cases of partheno-
b. Cytological Relationships. A consideration of the cases of parthenogenesis upon the basis of their cytological conditions leads to the common
genesis upon the basis of their cytological conditions leads to the common
classification of haploid and diploid parthenogenesis. By haploid parthenogenesis is meant the development without fertilization of an egg
classification of haploid and diploid parthenogenesis. By haploid par-
thenogenesis is meant the development without fertilization of an egg
which has gone through the process of chromosome reduction. Haploid
which has gone through the process of chromosome reduction. Haploid
eggs in general are sexual, and in most cases in which aspermic develop-
eggs in general are sexual, and in most cases in which aspermic development is possible the eggs are found to be capable of development either
ment is possible the eggs are found to be capable of development either
with or without fertilization. Hymenoptera, some of the Hemiptera,
with or without fertilization. Hymenoptera, some of the Hemiptera,
and the arachnids often exhibit haploid parthenogenesis. One case, the
and the arachnids often exhibit haploid parthenogenesis. One case, the
nematode Rhabdites (R. aberrans according to Kruger and R. pellio
nematode Rhabdites (R. aberrans according to Kruger and R. pellio
according to P. Hertwig), is worthy of note, however. Here the eggs
according to P. Hertwig), is worthy of note, however. Here the eggs
develop parthcnogcnetically and are of the haploid type but the pene-
develop parthcnogcnetically and are of the haploid type but the penetration of the sperm is necessary to initiate the development although
tration of the sperm is necessary to initiate the development although
it takes no further part and no true fertilization is accomplished. After
it takes no further part and no true fertilization is accomplished. After
it has penetrated the cortex of the egg, and thus set going the develop-
it has penetrated the cortex of the egg, and thus set going the developmental processes, the sperm degenerates and the further development
mental processes, the sperm degenerates and the further development
of the egg is as much parthenogenetic as if no sperm had been involved.
of the egg is as much parthenogenetic as if no sperm had been involved.


Diploid parthenogenesis is much more frequent, occurring in most
Diploid parthenogenesis is much more frequent, occurring in most
of the other groups where parthenogenesis is found at all. Copepods,
of the other groups where parthenogenesis is found at all. Copepods,
ostraeods, and the Hemiptera-Homoptera have this type character-
ostraeods, and the Hemiptera-Homoptera have this type characteristically whereas trematodes, nematodes, echinoderms, the phyllopods,
istically whereas trematodes, nematodes, echinoderms, the phyllopods,
the Orthoptera, and the Lepidoptera exhibit it in certain forms. An
the Orthoptera, and the Lepidoptera exhibit it in certain forms. An
intermediate condition is found in the rotifers, both diploid and haploid
intermediate condition is found in the rotifers, both diploid and haploid
parthenogenesis having been described for these forms. Triploid parthen-
parthenogenesis having been described for these forms. Triploid parthenogenesis is also known but is not common. The best understood case is
ogenesis is also known but is not common. The best understood case is
that of the plant genus Hieracium which has been described by Rosenberg. There are two sections of this genus which differ in their cytological
that of the plant genus Hieracium which has been described by Rosen-
berg. There are two sections of this genus which differ in their cytological
behavior. The sexual form of H. umbulatum has a diploid chromosome
behavior. The sexual form of H. umbulatum has a diploid chromosome
number of 18 whereas the variety linearifolium has a diploid number
number of 18 whereas the variety linearifolium has a diploid number
of 27. There are also some in which the diploid number is 36. The par-
of 27. There are also some in which the diploid number is 36. The parthenogenetic Archieracium, which is closely related to this species,
thenogenetic Archieracium, which is closely related to this species,
shows a chromosome number of 27. Rosenberg explains these facts
shows a chromosome number of 27. Rosenberg explains these facts
upon the basis of hybridization. The triploid races, Rosenberg main-
upon the basis of hybridization. The triploid races, Rosenberg maintains, cannot easily beproduced by the usual bisexual processes. Triploid
tains, cannot easily beproduced by the usual bisexual processes. Triploid
parthenogenesis, however, is of rare occurrence, and the triploidy in
parthenogenesis, however, is of rare occurrence, and the triploidy in
326 PARTHENOGENESIS
326 PARTHENOGENESIS
Line 12,954: Line 11,970:
single maturation division produces only one polar body and no reduc-'
single maturation division produces only one polar body and no reduc-'


tion of chromosomes can take place. There is one special case of partheno-
tion of chromosomes can take place. There is one special case of parthenogenesis to which was early ascribed theoretical significance in working
genesis to which was early ascribed theoretical significance in working
out a theory of fertilization. O. Hertwig in 1890 described a process in
out a theory of fertilization. O. Hertwig in 1890 described a process in
the maturation of the starfish Astropecten which has been many times
the maturation of the starfish Astropecten which has been many times
Line 12,962: Line 11,977:
for the egg of Thalessema in which the second polar body is not extruded,
for the egg of Thalessema in which the second polar body is not extruded,
the spindle remaining “submerged” in the cytoplasm of the egg. Upon
the spindle remaining “submerged” in the cytoplasm of the egg. Upon
the basis of these observations parthenogenesis was for a long time sup-
the basis of these observations parthenogenesis was for a long time supposed to be explained as a kind of fertilization by the polar body. It is
posed to be explained as a kind of fertilization by the polar body. It is
now known, however, that such cases seldom occur. A somewhat analogous case is that of the wasp H abrobracon in which a cytological study
now known, however, that such cases seldom occur. A somewhat anal-
ogous case is that of the wasp H abrobracon in which a cytological study
shows parthenogcnetieally produced males to be haploid on account of
shows parthenogcnetieally produced males to be haploid on account of
the fact that the first spermatocyte division is abortive while the second is
the fact that the first spermatocyte division is abortive while the second is
equational (A. Whiting, 1927). Of course cases in which only one matu-
equational (A. Whiting, 1927). Of course cases in which only one maturation division occurs are not rare.
ration division occurs are not rare.


c. Parthenogenesis and Sex. Much of the work upon parthenogenesis
c. Parthenogenesis and Sex. Much of the work upon parthenogenesis
has been due to the bearing of the problem upon sex determination.
has been due to the bearing of the problem upon sex determination.
Many experiments have been made for the purpose of discovering what
Many experiments have been made for the purpose of discovering what
factors can influence the production of males or females within the
factors can influence the production of males or females within the
parthenogenetic strains. Especially have the rotifers been used for
parthenogenetic strains. Especially have the rotifers been used for
experiments of this kind. Punnett observed various kinds of females as
experiments of this kind. Punnett observed various kinds of females as
follows: arrhenotokous females or those which produce males; thely-
follows: arrhenotokous females or those which produce males; thelytokous females (female producers) of three kinds, namely, those which
tokous females (female producers) of three kinds, namely, those which
produce, respectively, a large percentage, a small percentage, and those
produce, respectively, a large percentage, a small percentage, and those
which produce no arrhenotokous females. In the attempt to influence
which produce no arrhenotokous females. In the attempt to influence
the sex of the progeny of these forms conflicting results have been ob-
the sex of the progeny of these forms conflicting results have been obtained. The studies of rotifers have been most extensively carried on by
tained. The studies of rotifers have been most extensively carried on by
Whitney and by Shull. In general Shull’s experiments on the modification of sex have yielded positive results, for he has found a relationship
Whitney and by Shull. In general Shull’s experiments on the modifica-
tion of sex have yielded positive results, for he has found a relationship
between metabolism and sex determination. When the quantity of food
between metabolism and sex determination. When the quantity of food
given H ydatina senta is small the number of male producers is increased;
given H ydatina senta is small the number of male producers is increased;
old food reduces the number. Creatin, ammonium salts, beef extract,
old food reduces the number. Creatin, ammonium salts, beef extract,
and low temperature prevent the formation of male producers. Long-
and low temperature prevent the formation of male producers. Longcontinued parthenogenesis results in a decrease in male production.
continued parthenogenesis results in a decrease in male production.
INTERSEXES 327
INTERSEXES 327


Line 12,998: Line 12,006:
advance.
advance.


Whitney, on the other hand, has found less evidence that male pro-
Whitney, on the other hand, has found less evidence that male production is a response to external conditions, although he did find that
duction is a response to external conditions, although he did find that
crowding in H. senta permitted the development of fewer male producers in direct proportion to the degree of the crowding. He found,
crowding in H. senta permitted the development of fewer male pro-
ducers in direct proportion to the degree of the crowding. He found,
however, that neither oxygen, temperature, nor starvation is a factor.
however, that neither oxygen, temperature, nor starvation is a factor.
One of his strains when fed continuously upon a diet of Polytonia pro-
One of his strains when fed continuously upon a diet of Polytonia produced nearly all females for twenty-five generations, only three per
duced nearly all females for twenty-five generations, only three per
cent of the daughters being male producing. But a change of diet to
cent of the daughters being male producing. But a change of diet to
Dunaliella increased the percentage to 57. When they were fed again
Dunaliella increased the percentage to 57. When they were fed again
upon Polytonia, the percentage fell off. The influence of the food was
upon Polytonia, the percentage fell off. The influence of the food was
found to be upon the grandmother.
found to be upon the grandmother.


In addition to the work of Shull and of Whitney, Noyes has reported
In addition to the work of Shull and of Whitney, Noyes has reported
a series of experiments on Proales decipiens lasting through 250 genera-
a series of experiments on Proales decipiens lasting through 250 generations in which no males appeared although the animals were subjected
tions in which no males appeared although the animals were subjected
to various environmental changes including changes of chemical composition, of temperature, and of feed. More found Brachionus to give
to various environmental changes including changes of chemical com-
position, of temperature, and of feed. More found Brachionus to give
increased arrhenotekous females upon treatment with chemicals such
increased arrhenotekous females upon treatment with chemicals such
as ferric chloride (FeCl), whereas constant diet and temperature gave
as ferric chloride (FeCl), whereas constant diet and temperature gave
Line 13,033: Line 12,036:
some of the parthenogenetie strains of Cladocera. It is the condition of
some of the parthenogenetie strains of Cladocera. It is the condition of
intersexes or, as originally described by Banta, sex intergrades. The
intersexes or, as originally described by Banta, sex intergrades. The
intersex condition manifests itself through the secondary sex character-
intersex condition manifests itself through the secondary sex characteristics in that a typical female has a series of eight secondary sex characters which are identified with her sex, and similarly for a typical male.
istics in that a typical female has a series of eight secondary sex char-
acters which are identified with her sex, and similarly for a typical male.
The eight characters are as follows: (1) body size, the females are the
The eight characters are as follows: (1) body size, the females are the
larger at maturity; (2) size and position of the eye, the eyes of the
larger at maturity; (2) size and position of the eye, the eyes of the
Line 13,041: Line 12,042:


females being smaller and crowding the margin of the head less than
females being smaller and crowding the margin of the head less than
those of the males; (3) outline of the head, the angle of the antero-
those of the males; (3) outline of the head, the angle of the anteroventral margins of the head being more acute in the male; (4) absence
ventral margins of the head being more acute in the male; (4) absence
in the female of the nuchal protuberance; (5) and (6) character of first
in the female of the nuchal protuberance; (5) and (6) character of first
antennae, the males having swollen basal portions and two lateral
antennae, the males having swollen basal portions and two lateral
stylets; and (7) and (8) the outline and armature of the lateral post-
stylets; and (7) and (8) the outline and armature of the lateral postabdominal margins, these being more concave and not serrated in the
abdominal margins, these being more concave and not serrated in the
female. The intersex individuals may have the sex organs of either sex
female. The intersex individuals may have the sex organs of either sex
accompanied by from one to several of the secondary sex characters of
accompanied by from one to several of the secondary sex characters of
the other sex. There are also hermaphroditic forms with various combi-
the other sex. There are also hermaphroditic forms with various combinations of the male and female secondary characters. It is Banta’s
nations of the male and female secondary characters. It is Banta’s
opinion that these intersex conditions in Cladocera and other parthenogenetically reproducing forms are probably determined by environmental factors.
opinion that these intersex conditions in Cladocera and other partheno-
genetically reproducing forms are probably determined by environ-
mental factors.


A relation of hermaphroditism to parthenogenesis appears in certain
A relation of hermaphroditism to parthenogenesis appears in certain
Line 13,064: Line 12,060:
the females are hermaphroditic and the entrance of sperm into the egg
the females are hermaphroditic and the entrance of sperm into the egg
is necessary for the initiation of development, although it takes no
is necessary for the initiation of development, although it takes no
further part in the process and the cleavage of the egg is as truly parthen-
further part in the process and the cleavage of the egg is as truly parthenogenetie as if no sperm had penetrated into it. In addition to this
ogenetie as if no sperm had penetrated into it. In addition to this
relationship, hermaphroditism may be superimposed upon parthenogenesis at least in one family of the Phyllopoda where it appears that
relationship, hermaphroditism may be superimposed upon partheno-
Lepidurus which under favorable conditions reproduces parthenogcnetically “may become hermaphroditic when food is scarce ” (Bcrnard,1896).
genesis at least in one family of the Phyllopoda where it appears that
Lepidurus which under favorable conditions reproduces parthenogcneti-
cally “may become hermaphroditic when food is scarce ” (Bcrnard,1896).


e. Geographical Races. Another matter of interest is the occurrence
e. Geographical Races. Another matter of interest is the occurrence
Line 13,082: Line 12,075:
other a female-producing parthenogcnetic race. These occupy distinct
other a female-producing parthenogcnetic race. These occupy distinct
regions, the latter occurring in northern Europe, but at some points the
regions, the latter occurring in northern Europe, but at some points the
two may co-exist. These two races are looked upon by Vandel as in-
two may co-exist. These two races are looked upon by Vandel as incipient species. Geographical parthenogenesis has also been observed
cipient species. Geographical parthenogenesis has also been observed
CAUSES OF PARTHENOGENESIS 329
CAUSES OF PARTHENOGENESIS 329


in the moth Solenobia by Seiler. Solenobza triquetrella and S. znfleti occur
in the moth Solenobia by Seiler. Solenobza triquetrella and S. znfleti occur
in both bisexual and parthenogenetic forms, the latter being permanent
in both bisexual and parthenogenetic forms, the latter being permanent
and thelytokous. Of S. triquetrella the parthenogenetic form is widely
and thelytokous. Of S. triquetrella the parthenogenetic form is widely
Line 13,092: Line 12,084:
form has been found in a single locality only. In S. pineti the bisexual
form has been found in a single locality only. In S. pineti the bisexual
form is common but the parthenogenetic is restricted to a very few
form is common but the parthenogenetic is restricted to a very few
localities. Finally Trialeurodes vaporariorum, a white-fly has two races,
localities. finally Trialeurodes vaporariorum, a white-fly has two races,
according to Schrader, that are unlike in their parthenogenesis, in that
according to Schrader, that are unlike in their parthenogenesis, in that
the English race produces females with only three per cent males and
the English race produces females with only three per cent males and
Line 13,102: Line 12,094:
entrance of a sperm into the egg sets off the processes which are involved.
entrance of a sperm into the egg sets off the processes which are involved.
This initiatory action is capable of imitation by both chemical and
This initiatory action is capable of imitation by both chemical and
physical means as in the cases of artificial parthenogenesis. There are
physical means as in the cases of artificial parthenogenesis. There are
also conditions in which, it would appear, development may go forward
also conditions in which, it would appear, development may go forward
automatically, the participation of the sperm being entirely dispensed
automatically, the participation of the sperm being entirely dispensed
Line 13,108: Line 12,100:
for regarding the developmental processes of the egg as brought to a.
for regarding the developmental processes of the egg as brought to a.
standstill before the sperm enters. Rather they are slowed down to a
standstill before the sperm enters. Rather they are slowed down to a
speed from which they will not recover unless external influences are
speed from which they will not recover unless external influences are
operative, usually in the form of the sperm. Perhaps monogametie
operative, usually in the form of the sperm. Perhaps monogametie
development is possible only where the inhibition is less intense, thus
development is possible only where the inhibition is less intense, thus
Line 13,123: Line 12,115:
changes in the nucleo-cytoplasmic ratio. Papanicolau reached similar
changes in the nucleo-cytoplasmic ratio. Papanicolau reached similar
conclusions. Shull, however, investigated the nucleo-cytoplasmic ratios
conclusions. Shull, however, investigated the nucleo-cytoplasmic ratios
in the rotifer, H ydatina senta, without finding any correlation between
in the rotifer, H ydatina senta, without finding any correlation between
it and the mode of reproduction. Although it has been claimed that
it and the mode of reproduction. Although it has been claimed that
food, oxygen content, and other similar external factors influence the
food, oxygen content, and other similar external factors influence the
sex ratios of parthenogenetically produced animals, there is no good
sex ratios of parthenogenetically produced animals, there is no good
evidence that these factors are responsible. Banta thought the formation
evidence that these factors are responsible. Banta thought the formation
Line 13,135: Line 12,127:


Another suggestion (which is so far merely record of an observation
Another suggestion (which is so far merely record of an observation
rather than a cause) relates to the lagging chromosome of the phyllox-
rather than a cause) relates to the lagging chromosome of the phylloxerans which is observed to accompany parthenogenesis. Peacock and
erans which is observed to accompany parthenogenesis. Peacock and
Harrison working upon lepidopteran crosses reached the conclusion
Harrison working upon lepidopteran crosses reached the conclusion
that parthenogenesis is a result of hybridity and later supported this
that parthenogenesis is a result of hybridity and later supported this
conclusion by a study of the data of other crosses including Nabours’
conclusion by a study of the data of other crosses including Nabours’
experiments on parthenogencsis in Apotettix. Finally Nabours, working
experiments on parthenogencsis in Apotettix. finally Nabours, working
upon Parateltirc, studied genetically two strains one of which was highly
upon Parateltirc, studied genetically two strains one of which was highly
parthenogenetic and the other had never so reproduced. He obtained
parthenogenetic and the other had never so reproduced. He obtained
genetic evidence that parthcnogenesis is a character which segregates
genetic evidence that parthcnogenesis is a character which segregates
in a Mendelian manner and believes it due to certain genes. Robertson’s
in a Mendelian manner and believes it due to certain genes. Robertson’s
cytological studies on Nabours’ material fall into line with this hypoth-
cytological studies on Nabours’ material fall into line with this hypothesis. The entrance of the sperm is necessary for the second polocyte
esis. The entrance of the sperm is necessary for the second polocyte
division, and when it is lacking the diploid chromosome number is
division, and when it is lacking the diploid chromosome number is
retained. In this latter case if the specific genes for parthenogenesis are
retained. In this latter case if the specific genes for parthenogenesis are
present development is initiated. It is to be noted that Agar working
present development is initiated. It is to be noted that Agar working
upon Daphnia and Whiting upon Habrobracon failed to find genetic
upon Daphnia and Whiting upon Habrobracon failed to find genetic
evidence of the cause of parthenogenesis. But Punnett as long ago as
evidence of the cause of parthenogenesis. But Punnett as long ago as
1906 had suggested the probability that the question is concerned with
1906 had suggested the probability that the question is concerned with
Line 13,162: Line 12,152:
kingdom than is generally recognized, and it is not rare among the
kingdom than is generally recognized, and it is not rare among the
plants. Examples are found in the following groups of animals: rotifers,
plants. Examples are found in the following groups of animals: rotifers,
nematodes, trematodes, Dinophilus, three orders of Crustacea, myria-
nematodes, trematodes, Dinophilus, three orders of Crustacea, myriapods, arachnids, and ten orders of insects. It seems desirable to point
pods, arachnids, and ten orders of insects. It seems desirable to point
out some of the important studies in each of these groups, although no
out some of the important studies in each of these groups, although no
attempt can be made toward inclusiveness. For references and a more
attempt can be made toward inclusiveness. For references and a more
Line 13,179: Line 12,168:
b. Nematode. For the nematodes the case of Rhabdites aberrans as
b. Nematode. For the nematodes the case of Rhabdites aberrans as
described by Kriiger has already been mentioned. The trematodes are
described by Kriiger has already been mentioned. The trematodes are
commonly described as giving rise to rediae from cells which are segre-
commonly described as giving rise to rediae from cells which are segregated at one end of the body of the sporocyst and become an ovary.
gated at one end of the body of the sporocyst and become an ovary.
The new rediae arise from these so-called “ova,” which must be thought
The new rediae arise from these so-called “ova,” which must be thought
to develop parthcnogenetically if the view of their origin is maintained
to develop parthcnogenetically if the view of their origin is maintained
Line 13,188: Line 12,176:
c. Annelida. Among the annelids parthenogenesis is suspected in
c. Annelida. Among the annelids parthenogenesis is suspected in
Dinophilus conklini from the preponderance of females. In the leech
Dinophilus conklini from the preponderance of females. In the leech
Ilemiclepsis marginata the early finding of parthenogenesis has failed
Ilemiclepsis marginata the early finding of parthenogenesis has failed
of confirmation in more recent experiments (Brumpt, 1900).
of confirmation in more recent experiments (Brumpt, 1900).


d. Crustacea. Two orders of the Entomostraca exhibit partheno-
d. Crustacea. Two orders of the Entomostraca exhibit parthenogenesis and include in their number some cases that have been given a
genesis and include in their number some cases that have been given a
great amount of study, while a third offers a case which is suspected to
great amount of study, while a third offers a case which is suspected to
be parthenogenetic. Among the Phyllopoda examples may be cited
be parthenogenetic. Among the Phyllopoda examples may be cited
from both the Branchiopoda and the Cladocera. Of the former, Apus,
from both the Branchiopoda and the Cladocera. Of the former, Apus,
Lepidurus, and Artemia are well known. Reference has already been
Lepidurus, and Artemia are well known. Reference has already been
made to Lepidurus because of its hermaphroditic relationships. Thely-
made to Lepidurus because of its hermaphroditic relationships. Thelytokous parthenogenesis occurs in these forms. Artemia salina likewise
tokous parthenogenesis occurs in these forms. Artemia salina likewise
has been mentioned in connection with geographic parthenogenesis.
has been mentioned in connection with geographic parthenogenesis.
On this form the most recent studies are those of Artom (1912). Two
On this form the most recent studies are those of Artom (1912). Two
polocytes are formed in the development of the egg. Regularly a reduc-
polocytes are formed in the development of the egg. Regularly a reduction of chromosomes from 42 to 21 takes place. The parthenogenetic
tion of chromosomes from 42 to 21 takes place. The parthenogenetic
forms are tetraploid and of a type called somatic. There are therefore
forms are tetraploid and of a type called somatic. There are therefore
two strains of Artemia, one diploid and bisexual, the other tetraploid
two strains of Artemia, one diploid and bisexual, the other tetraploid
Line 13,218: Line 12,203:
Of the work on the Cladoeera, which dates from Weismann’s studies
Of the work on the Cladoeera, which dates from Weismann’s studies
in 1879, the general facts are well known. Bisexual generations are
in 1879, the general facts are well known. Bisexual generations are
followed by parthenogenetic which may continue indefinitely. The
followed by parthenogenetic which may continue indefinitely. The
various races differ greatly in the number of generations produced within
various races differ greatly in the number of generations produced within
a year and in the frequency of the bisexual forms. Apparently most if
a year and in the frequency of the bisexual forms. Apparently most if
Line 13,235: Line 12,220:


forms. There is good evidence that sex ratios and intersex conditions are
forms. There is good evidence that sex ratios and intersex conditions are
both subject to environmental influences.
both subject to environmental influences.


In the order Ostracoda, parthenogenesis was discovered in 1880 by
In the order Ostracoda, parthenogenesis was discovered in 1880 by
Line 13,258: Line 12,243:
remarked that some of the studies of ostracods have taken up the
remarked that some of the studies of ostracods have taken up the
question, raised for many Crustacea, as to the possible impairment of
question, raised for many Crustacea, as to the possible impairment of
vigor of a strain due to long-continued parthenogenesis. Here as else-
vigor of a strain due to long-continued parthenogenesis. Here as elsewhere among the members of the class the general consensus of opinion
where among the members of the class the general consensus of opinion
seems to be that no loss of vigor can be noted.
seems to be that no loss of vigor can be noted.


Mention should be made of the possibility of parthenogenesis in the
Mention should be made of the possibility of parthenogenesis in the
third order of the Entomostraca, the Rhizocephala. In the genus Sylon
third order of the Entomostraca, the Rhizocephala. In the genus Sylon
belonging to that suborder Smith reported his complete failure to find
belonging to that suborder Smith reported his complete failure to find
males and so suspected that parthenogenesis is the method of repro-
males and so suspected that parthenogenesis is the method of reproduction.
duction.


In one order of Malacostraca parthenogenesis has been reported,
In one order of Malacostraca parthenogenesis has been reported,
INSECTA 333
INSECTA 333


namely in the Isopoda. Vandel (1928) has given an account of geo-
namely in the Isopoda. Vandel (1928) has given an account of geographical parthenogenesis, already mentioned in Trichoniscus. Two
graphical parthenogenesis, already mentioned in Trichoniscus. Two
races occupying different localities were described, one bisexual, the
races occupying different localities were described, one bisexual, the
other exclusively parthenogenetic. In some places they may exist side
other exclusively parthenogenetic. In some places they may exist side
Line 13,292: Line 12,274:
for nearly a century and it may still be suspected, but Montgomery in
for nearly a century and it may still be suspected, but Montgomery in
1903 concluded that it is “very rare among spiders, and it is probable
1903 concluded that it is “very rare among spiders, and it is probable
that most species do not show it at all.” Since Montgomery’s finding, it
that most species do not show it at all.” Since Montgomery’s finding, it
does not appear that any work has been done which successfully estab-
does not appear that any work has been done which successfully establishes parthenogenesis in these animals.
lishes parthenogenesis in these animals.


Among the mites there is no doubt that parthenogenesis occurs, for
Among the mites there is no doubt that parthenogenesis occurs, for
Line 13,311: Line 12,292:
compiled in part from Winkler, summarizes the occurrence of the
compiled in part from Winkler, summarizes the occurrence of the
phenomenon. For references to most of these cases the reader is referred
phenomenon. For references to most of these cases the reader is referred
to Winkler, but a few of especial significance are mentioned following
to Winkler, but a few of especial significance are mentioned following
the table.
the table.


Line 13,328: Line 12,309:
Phasmidad
Phasmidad


Eurycnema. v. Wuelfing, 1899; three generations of parthenogenetic fe-
Eurycnema. v. Wuelfing, 1899; three generations of parthenogenetic females in Java.
males in Java.
Hanitsch, 1902; two generations of parthenogenetic females.
Hanitsch, 1902; two generations of parthenogenetic females.


Bacillus. Dominique, 1896-99; two thelytokous generations of par-
Bacillus. Dominique, 1896-99; two thelytokous generations of parthenogenesis. Males are rare.
thenogenesis. Males are rare.
Also Stadelmann, v. Bachr, Cameron, Daiber.
Also Stadelmann, v. Bachr, Cameron, Daiber.


Dixippus. Pantel and de Sinety, 1908. Parthenogenesis established.
Dixippus. Pantel and de Sinety, 1908. Parthenogenesis established.
Schmitz, 1906. Four generations of thelytokous partheno-
Schmitz, 1906. Four generations of thelytokous partheno
 
genesis.
genesis.


Hammerschmidt, 1910. Five generations of thelytokous par-
Hammerschmidt, 1910. five generations of thelytokous parthenogenesis.
thenogenesis.


Jeziorski, 1918. Four generations of thelytokous partheno-
Jeziorski, 1918. Four generations of thelytokous parthenogenesis.
genesis.


Phasma. Thurau, 1899. Only females.
Phasma. Thurau, 1899. Only females.
Line 13,361: Line 12,337:
M yrmecophila acervorum. Schimmer, 1909, suspected parthenogenesis.
M yrmecophila acervorum. Schimmer, 1909, suspected parthenogenesis.
Tettigidae
Tettigidae
fig Nabour and colleagues, 1919-1929. Thelytokous parthenogen-
fig Nabour and colleagues, 1919-1929. Thelytokous parthenogen' . B .
' . B .
Telmatemx esis est understood cases
Telmatemx esis est understood cases


Coleoptera. Parthenogenesis is of rare occurrence and most of the older ac-
Coleoptera. Parthenogenesis is of rare occurrence and most of the older accounts are not trustworthy.
counts are not trustworthy.


Tropiphorus carinatus. Calwer, 1916, reported parthenogenesis.
Tropiphorus carinatus. Calwer, 1916, reported parthenogenesis.
Line 13,386: Line 12,360:
Thysanoptera
Thysanoptera


Most species are bisexual. Many may multiply parthenogenetically. The1y-
Most species are bisexual. Many may multiply parthenogenetically. The1ytokous parthenogenesis is established for Parthenothrips, Anaphothrips, Heliothrips, Taeniothrips, and Liothrips; for a number of others it is probable.
tokous parthenogenesis is established for Parthenothrips, Anaphothrips, Helio-
Arrhenotokous parthenogenesis is experimentally shown for Antlwthrips verbasci.
thrips, Taeniothrips, and Liothrips; for a number of others it is probable.
Arrhenotokous parthenogenesis is experimentally shown for Antlwthrips ver-
basci.


Corrodentia
Corrodentia
Line 13,399: Line 12,370:
Aleurodes. Morrill and Back, 1911. Arrhenotokous parthenogenesis.
Aleurodes. Morrill and Back, 1911. Arrhenotokous parthenogenesis.


Trialeurodes. Schrader, 1920. English race thelytokous. American race ar-
Trialeurodes. Schrader, 1920. English race thelytokous. American race ar
 
rhenotokous.
rhenotokous.


Line 13,407: Line 12,377:
seasons but in south may be exclusively parthenogenetic.
seasons but in south may be exclusively parthenogenetic.


Other genera include Callipterus, Ceratophis, M acrosiphum, M yzus, Pemphi-
Other genera include Callipterus, Ceratophis, M acrosiphum, M yzus, Pemphigus, Rhopalosiphum, Schizoneura, Toxoptera; Chermcs, Pincus,Phyllozera.
gus, Rhopalosiphum, Schizoneura, Toxoptera; Chermcs, Pincus,-
Phyllozera.


Coccidae. Many genera of scale insects are described as parthenogenetic
Coccidae. Many genera of scale insects are described as parthenogenetic
although some cases are not known. Included are Aspidiotus,
although some cases are not known. Included are Aspidiotus,
Ceroplastes, Cryptococcus, Diaspis, Eriopeltis, Lecanium, Lep1.'-
Ceroplastes, Cryptococcus, Diaspis, Eriopeltis, Lecanium, Lep1.'dosaphes, Orthezia, Parthenolecanium, Pseudococcus, Pulvinaria,
dosaphes, Orthezia, Parthenolecanium, Pseudococcus, Pulvinaria,
Saissetia.
Saissetia.


Line 13,420: Line 12,387:
All proven cases belong to family Psychidae or are closely related to it.
All proven cases belong to family Psychidae or are closely related to it.
Acanthopsyche, Pachythelia, Psyche, Sterrhopteryx, Phalacropteryx, Apterona,
Acanthopsyche, Pachythelia, Psyche, Sterrhopteryx, Phalacropteryx, Apterona,
Cochlophora, and Lufia are included. The best known is Solerwbia liclwnella.
Cochlophora, and Lufia are included. The best known is Solerwbia liclwnella.
Hoffmann, 1859.
Hoffmann, 1859.


Solenobia triquetrella. Hofimann, 1859-1869. Usually bisexual. Both bisexual
Solenobia triquetrella. Hofimann, 1859-1869. Usually bisexual. Both bisexual


and parthenogenetic modes described. Geographical parthenogenesis.
and parthenogenetic modes described. Geographical parthenogenesis.
Line 13,431: Line 12,398:
Diptera. Parthenogenesis seldom found in this group.
Diptera. Parthenogenesis seldom found in this group.


Chirmwmus. Godlewski, 1914. Paedogenesis and parthenogenesis inter-
Chirmwmus. Godlewski, 1914. Paedogenesis and parthenogenesis intermingled.
mingled.
Corynoneura. Goetghebeur, 1913. Rarely parthenogenetic.
Corynoneura. Goetghebeur, 1913. Rarely parthenogenetic.
M etriocnemus. Picado, 1913. Males few in number.
M etriocnemus. Picado, 1913. Males few in number.
Line 13,527: Line 12,493:
Arrhenotokous parthenogenesis is very widespread among the ants. Many
Arrhenotokous parthenogenesis is very widespread among the ants. Many
workers are fertile and lay unfertilized eggs from which males develop.
workers are fertile and lay unfertilized eggs from which males develop.
Some hold the view that both males and females may develop from par-
Some hold the view that both males and females may develop from parthenogenetic eggs. A few cases are recorded in which thelytoky is claimed
thenogenetic eggs. A few cases are recorded in which thelytoky is claimed
to be established. Certainly it is much less common than arrhenotoky.
to be established. Certainly it is much less common than arrhenotoky.


Vespoidea
Vespoidea


Parthenogenetic eggs of queens and workers develop into males only. Ex-
Parthenogenetic eggs of queens and workers develop into males only. Examples are Polistes gallicus, v. Seibold, 1871
amples are Polistes gallicus, v. Seibold, 1871
Vespa germanica, Marchal, 1896
Vespa germanica, Marchal, 1896


Line 13,551: Line 12,515:
large extent concerned either with the general life cycle or with the
large extent concerned either with the general life cycle or with the
cytological and genetical aspects of the problem. Many studies of very
cytological and genetical aspects of the problem. Many studies of very
fine character have been made upon gametogenesis and sex determina-
fine character have been made upon gametogenesis and sex determination, and upon the factors involved in the control of sex. Of recent
tion, and upon the factors involved in the control of sex. Of recent
years the problems which are bound up with uniparental inheritance
years the problems which are bound up with uniparental inheritance
have attracted much attention. It must be admitted that much of this
have attracted much attention. It must be admitted that much of this
Line 13,565: Line 12,528:
forms of grouse locut promises much in the cytological analysis since
forms of grouse locut promises much in the cytological analysis since
grasshopper chromosomes are among the most favorable for study. The
grasshopper chromosomes are among the most favorable for study. The
saw flies have been studied especially by Doncaster and by Peacock
saw flies have been studied especially by Doncaster and by Peacock
and Harrison. Of the aphids and phylloxerans a very careful cytological
and Harrison. Of the aphids and phylloxerans a very careful cytological
study was made by Morgan. An earlier study by Tannreuther is a good
study was made by Morgan. An earlier study by Tannreuther is a good
account of the general embryology of the aphids. Parthenogenesis in
account of the general embryology of the aphids. Parthenogenesis in
the moths is most recently made known to us by the studies of Gold-
the moths is most recently made known to us by the studies of Goldschmidt and of Seiler. Of the Hymenoptera the extensive work done by
schmidt and of Seiler. Of the Hymenoptera the extensive work done by
Patterson on Paracopidosomopsis will serve to introduce the student
Patterson on Paracopidosomopsis will serve to introduce the student
to the relation of parthenogenesis and polyembryony, and the best
to the relation of parthenogenesis and polyembryony, and the best
Line 13,577: Line 12,539:
connection with other aspects of the general parthenogenesis problems.
connection with other aspects of the general parthenogenesis problems.


f. Plants. Among plants a considerable number of cases of partheno-
f. Plants. Among plants a considerable number of cases of parthenogenesis are already known and it is thought of interest to mention the
genesis are already known and it is thought of interest to mention the
conditions found there in this discussion although the problems involved
conditions found there in this discussion although the problems involved
are outside the scope of this work. It is difficult without careful study
are outside the scope of this work. It is difficult without careful study
among the plants to distinguish between cases of parthenogenesis and
among the plants to distinguish between cases of parthenogenesis and
those of the simple vegetative apogamy. Among higher plants haploid
those of the simple vegetative apogamy. Among higher plants haploid
Line 13,592: Line 12,553:


Haploid parthenogenesis: Spirogyra, Ernst, 1918; Vaucheria, von
Haploid parthenogenesis: Spirogyra, Ernst, 1918; Vaucheria, von
Wettstein, 1920; Ectocarpus, Kylin, 1918; Fucus, Overton, 1912 (prob-
Wettstein, 1920; Ectocarpus, Kylin, 1918; Fucus, Overton, 1912 (probably haploid); Gastrodia, Kusans, 1915; Oenothera, Haberlandt, 1921,
ably haploid); Gastrodia, Kusans, 1915; Oenothera, Haberlandt, 1921,
1922; Datura, Blakeslee and Belling, 1922, evidence from breeding
1922; Datura, Blakeslee and Belling, 1922, evidence from breeding
experiments; Nicotiana, Clausen and Mann, 1924.
experiments; Nicotiana, Clausen and Mann, 1924.


Diploid parthenogenesis: Chara crinita, Ernst, 1918; Athyrium fel2':c-
Diploid parthenogenesis: Chara crinita, Ernst, 1918; Athyrium fel2':cfoemina, var. clarissima, Farmer and Digby, 1907; Scolopendrium
foemina, var. clarissima, Farmer and Digby, 1907; Scolopendrium
vulgare, Farmer and Digby, 1907; Marsilia Drummondii, Strasburger,
vulgare, Farmer and Digby, 1907; Marsilia Drummondii, Strasburger,
1907 ; Allium odomm, Haberlandt, 1923 ; Atamosco texamz, Pace, 1913;
1907 ; Allium odomm, Haberlandt, 1923 ; Atamosco texamz, Pace, 1913;
Calycanthus, Schiirhofi, 1923; Alchemilla, Murbeck, 1901, Strasburger,
Calycanthus, Schiirhofi, 1923; Alchemilla, Murbeck, 1901, Strasburger,
1905, Boos, 1917; Wikstroemia, Winkler, 1906; Eupatorium glandulosum,
1905, Boos, 1917; Wikstroemia, Winkler, 1906; Eupatorium glandulosum,
Holmgren, 1919 ; Erigeron annuus, Tahara, 1921; Antennaria alpina,
Holmgren, 1919 ; Erigeron annuus, Tahara, 1921; Antennaria alpina,
Juel, 1900; Chondrilla, Rosenberg, 1912; Taraxacum, Juel, 1904, Osswa,
Juel, 1900; Chondrilla, Rosenberg, 1912; Taraxacum, Juel, 1904, Osswa,
1913, Sears, 1922; Archieracium, Rosenberg, 1917.
1913, Sears, 1922; Archieracium, Rosenberg, 1917.
ARTIFICIAL PARTHENOGENESIS 339
ARTIfiCIAL PARTHENOGENESIS 339


II. ARTIFICIAL PARTHENOGENESIS
II. ARTIfiCIAL PARTHENOGENESIS


Of great embryological significance is the phenomenon of artificial
Of great embryological significance is the phenomenon of artificial
or experimental parthenogenesis. It has been the subject of much of the
or experimental parthenogenesis. It has been the subject of much of the
work on experimental embryology of the present century and its chief
work on experimental embryology of the present century and its chief
consideration should be a matter for a treatise on experimental embry-
consideration should be a matter for a treatise on experimental embryology. However, its importance for an understanding of matters which
ology. However, its importance for an understanding of matters which
have to do with the normal embryological process is so great that a brief
have to do with the normal embryological process is so great that a brief
account should be included here. For details and bibliography the
account should be included here. For details and bibliography the
reader is referred to the extensive accounts which have been published
reader is referred to the extensive accounts which have been published
by Loeb (see his “Artificial Parthenogenesis and Fertilization”) and by
by Loeb (see his “Artificial Parthenogenesis and Fertilization”) and by
Morgan in his “Experimental Embryology.” Wilson has also critically
Morgan in his “Experimental Embryology.” Wilson has also critically
considered the cytological aspects of the problems concerned with arti-
considered the cytological aspects of the problems concerned with artificial parthenogenesis in “The Cell.”
ficial parthenogenesis in “The Cell.”


The student should be reminded of the double function which fertiliza-
The student should be reminded of the double function which fertilization serves in normal development; the one is hereditary in character
tion serves in normal development; the one is hereditary in character
in that fertilization provides the mechanism for conveying the contribution of the male to the offspring. The other is strictly developmental
in that fertilization provides the mechanism for conveying the contribu-
tion of the male to the offspring. The other is strictly developmental
in that it sets in motion those processes which have been inhibited or
in that it sets in motion those processes which have been inhibited or
are latent in the egg at the time of maturation. It is with this second
are latent in the egg at the time of maturation. It is with this second
aspect of fertilization that experimental or artificial parthenogenesis
aspect of fertilization that experimental or artificial parthenogenesis
deals. These experiments have sought to imitate and to interpret the
deals. These experiments have sought to imitate and to interpret the
normal processes of development as initiated by fertilization, and
normal processes of development as initiated by fertilization, and
Line 13,635: Line 12,590:
been reached. The experiments have shown that it is possible to cause
been reached. The experiments have shown that it is possible to cause
the unfertilized egg of a great many animals to develop into larvae
the unfertilized egg of a great many animals to develop into larvae
largely under the influence of chemical treatment, although physical
largely under the influence of chemical treatment, although physical
means have also been used to accomplish the same end less perfectly.
means have also been used to accomplish the same end less perfectly.


The work on parthenogenesis is chiefly a monument to the insight
The work on parthenogenesis is chiefly a monument to the insight
of Jacques Loeb and his analytical experiments have been of the most
of Jacques Loeb and his analytical experiments have been of the most
importance in solving the many problems involved. However, numerous
importance in solving the many problems involved. However, numerous
other students have contributed to the progress of the work both before
other students have contributed to the progress of the work both before
and since his announcement of the discovery that it was possible to
and since his announcement of the discovery that it was possible to
induce eggs to develop artificially. Among the preliminary studies
induce eggs to develop artificially. Among the preliminary studies
which antedated Loeb’s discovery in 1899 may be mentioned the paper
which antedated Loeb’s discovery in 1899 may be mentioned the paper
of Loeb himself in 1892 in which he studied the effect of addition of
of Loeb himself in 1892 in which he studied the effect of addition of
sodium chloride to the sea water in which the eggs of Arbacia developed;
sodium chloride to the sea water in which the eggs of Arbacia developed;
Richard Hertwig’s observation (1896) on the effect of treating un-
Richard Hertwig’s observation (1896) on the effect of treating unfertilized sea-urchin eggs with strychnine; a series of experiments by
fertilized sea-urchin eggs with strychnine; a series of experiments by
Morgan (1896, 1899, 1900) on the effect of salt solutions on the segmentation of eggs and the formation of artificial asters; the work of
Morgan (1896, 1899, 1900) on the effect of salt solutions on the seg-
mentation of eggs and the formation of artificial asters; the work of
Mead (1896-98) showing that unfertilized eggs of Chaetopterus will
Mead (1896-98) showing that unfertilized eggs of Chaetopterus will
340 PARTHENOGENESIS
340 PARTHENOGENESIS
Line 13,660: Line 12,613:
who in a series of papers from 1900 to 1913 added a great deal to the
who in a series of papers from 1900 to 1913 added a great deal to the
understanding of this difficult subject; he succeeded in rearing through
understanding of this difficult subject; he succeeded in rearing through
metamorphosis the larvae of both sea-urchins and starfish which had
metamorphosis the larvae of both sea-urchins and starfish which had
been induced to develop by artificial parthenogenesis. Loeb and Ban-
been induced to develop by artificial parthenogenesis. Loeb and Bancroft (1913) brought a parthenogenetic frog through metamorphosis
croft (1913) brought a parthenogenetic frog through metamorphosis
and found that its sex glands contained eggs. Shearer and Lloyd (1913)
and found that its sex glands contained eggs. Shearer and Lloyd (1913)
succeeded even better than Delage in bringing parthenogenetic larvae
succeeded even better than Delage in bringing parthenogenetic larvae
Line 13,668: Line 12,620:
brought a considerable number of parthenogenetic tadpoles to the adult
brought a considerable number of parthenogenetic tadpoles to the adult
stage. It is to be noted, however, that only in the case of frogs has it
stage. It is to be noted, however, that only in the case of frogs has it
been possible to imitate in the laboratory the conditions of nature suf-
been possible to imitate in the laboratory the conditions of nature sufficiently to bring animals developed by parthenogenesis to sexual
ficiently to bring animals developed by parthenogenesis to sexual
maturity. Since Loeb’s work, Bataillon, R. S. and F. R. Lillie, Goldschmidt, Gray, Harvey, Heilbrunn, Herbst, Herlant, and Just are
maturity. Since Loeb’s work, Bataillon, R. S. and F. R. Lillie, Gold-
among the many who have made extensive studies into the embryological phases of artificial parthenogenesis.
schmidt, Gray, Harvey, Heilbrunn, Herbst, Herlant, and Just are
among the many who have made extensive studies into the embryo-
logical phases of artificial parthenogenesis.


VVhen one begins to consider the significance of artificial partheno-
VVhen one begins to consider the significance of artificial parthenogenesis he is at once led to inquire as to how general the phenomenon
genesis he is at once led to inquire as to how general the phenomenon
is or how generally it may be expected to be possible in the animal
is or how generally it may be expected to be possible in the animal
kingdom. It may well be that eggs are so constituted as to permit their
kingdom. It may well be that eggs are so constituted as to permit their
development without fertilization, at least into the cleavage stages, and
development without fertilization, at least into the cleavage stages, and
that we are merely unable to understand the requirements in each case
that we are merely unable to understand the requirements in each case
and to devise the correct procedure. A broad generalization of this char-
and to devise the correct procedure. A broad generalization of this character is hardly safe, however, for up to the present time the only forms
acter is hardly safe, however, for up to the present time the only forms
in which it has been possible to induce experimental parthenogenesis
in which it has been possible to induce experimental parthenogenesis
are those in which the experiment is relatively easy to perform. In
are those in which the experiment is relatively easy to perform. In
every case the eggs are of the type which is shed freely into the water.
every case the eggs are of the type which is shed freely into the water.
The difficulties of the experimental work which is involved may be the
The difficulties of the experimental work which is involved may be the
reason for this limitation or it may be that a deeper limitation is oper-
reason for this limitation or it may be that a deeper limitation is operative so that eggs which are adapted for other kinds of development
ative so that eggs which are adapted for other kinds of development
may not be stimulated to cleave artificially. Thus far the following
may not be stimulated to cleave artificially. Thus far the following
groups have responded to the treatments that have been devised to
groups have responded to the treatments that have been devised to
induce parthenogenesis artificially. By far the most work has been
induce parthenogenesis artificially. By far the most work has been
done on the sea-urchins. Arbacia, Strongylocentrotus, T0:copneus'es, and
done on the sea-urchins. Arbacia, Strongylocentrotus, T0:copneus'es, and
Paracentrotus have all shown themselves excellently adapted to experi-
Paracentrotus have all shown themselves excellently adapted to experiments of this type and they have been used for much important work,
ments of this type and they have been used for much important work,
especially the first two mentioned. The sand dollar, Echinarachnius,
especially the first two mentioned. The sand dollar, Echinarachnius,
has proved adaptable for similar experiments. Among the starfishes
has proved adaptable for similar experiments. Among the starfishes
ARTIfiCIAL PARTHENOGENESIS 341
ARTIFICIAL PARTHENOGENESIS 341


the eggs of the commoner species of Asterias as well as some of the
the eggs of the commoner species of Asterias as well as some of the
more unusual starfishes, as Asterina gibbosa, have been used success-
more unusual starfishes, as Asterina gibbosa, have been used successfully. It is to be noted, however, that the methods which have proven
fully. It is to be noted, however, that the methods which have proven
most successful with the sea—urchin give but very poor results with
most successful with the sea—urchin give but very poor results with
the starfish, and conversely little success has been obtained by applying
the starfish, and conversely little success has been obtained by applying
the two best methods of inducement for the development of the starfish
the two best methods of inducement for the development of the starfish
egg, namely, carbon dioxide and mechanical shaking, to eggs of the
egg, namely, carbon dioxide and mechanical shaking, to eggs of the
Line 13,710: Line 12,654:
been again a mechanical one, namely the simple pricking of the surface
been again a mechanical one, namely the simple pricking of the surface
of the egg. Various annelids have been studied, especially Chaetopterus,
of the egg. Various annelids have been studied, especially Chaetopterus,
Amphitrite, Thalessema, but the best results in this group have unques-
Amphitrite, Thalessema, but the best results in this group have unquestionably been gotten for the eggs of Nereis. Here again the means of
tionably been gotten for the eggs of Nereis. Here again the means of
inducing parthenogenesis is physical rather than chemical, namely, the
inducing parthenogenesis is physical rather than chemical, namely, the
subjecting of the egg to heat.
subjecting of the egg to heat.


A second question arises in attempting an embryological interpreta-
A second question arises in attempting an embryological interpretation of the experiments in artificial parthenogenesis, namely, do these
tion of the experiments in artificial parthenogenesis, namely, do these
experiments produce animals that are fairly normal. As already pointed
experiments produce animals that are fairly normal. As already pointed
out Loeb’s own studies led him to the belief that “parthenogenetic
out Loeb’s own studies led him to the belief that “parthenogenetic
larvae may be normal and apparently healthy,” and indeed, he said,
larvae may be normal and apparently healthy,” and indeed, he said,
“if the raising of the larvae was not such a tedious process partheno-
“if the raising of the larvae was not such a tedious process parthenogenetic animals would exist today in large numbers.” His methods have
genetic animals would exist today in large numbers.” His methods have
certainly produced, both in his own hands and in those of other investigators as well, larvae which resemble the normal in every particular,
certainly produced, both in his own hands and in those of other investi-
gators as well, larvae which resemble the normal in every particular,
and Delage, Shearer, and also Fuchs were able to bring parthenogenetic
and Delage, Shearer, and also Fuchs were able to bring parthenogenetic
larvae to adulthood. The chromosome relations of the individuals as
larvae to adulthood. The chromosome relations of the individuals as
Line 13,737: Line 12,677:
animals.
animals.


‘Loeb developed a theory of parthenogenesis as a result of his ex-
‘Loeb developed a theory of parthenogenesis as a result of his experiments, and what he spoke of as his improved method is based upon
periments, and what he spoke of as his improved method is based upon
that theory. According to his View the formation of the egg membrane
that theory. According to his View the formation of the egg membrane
is the deciding criterion by which the initiation of development may be
is the deciding criterion by which the initiation of development may be
Line 13,746: Line 12,685:


attached much more importance to this process than had previously
attached much more importance to this process than had previously
been done. Membrane formation is the deciding condition of develop-
been done. Membrane formation is the deciding condition of development. Not all later workers have agreed with Loeb in this view, but
ment. Not all later workers have agreed with Loeb in this view, but
unquestionably his explanations have not been out of harmony with
unquestionably his explanations have not been out of harmony with
the facts which he observed.
the facts which he observed.


The so-called improved method of Loeb for inducing artificial par-
The so-called improved method of Loeb for inducing artificial parthenogenesis consists of two steps. Its details as to concentration and
thenogenesis consists of two steps. Its details as to concentration and
length of exposure must be worked out for the particular species of
length of exposure must be worked out for the particular species of
sea—urchin eggs used and indeed different individuals will respond
sea—urchin eggs used and indeed different individuals will respond
Line 13,765: Line 12,702:
acid to 50 cc. of sea water. Apparently any monobasic fatty acid would
acid to 50 cc. of sea water. Apparently any monobasic fatty acid would


serve equally well for this purpose but Loeb found butyric to be satis-
serve equally well for this purpose but Loeb found butyric to be satis
 
N
N
factory for the experiments (2.8 cc. of I5 butyric were necessary in the
factory for the experiments (2.8 cc. of I5 butyric were necessary in the


case of Strongylocentrotus purpuratus eggs). The duration of the ex-
case of Strongylocentrotus purpuratus eggs). The duration of the exposure must be brief, from 1% to 3 mintues. The eggs are then transferred to normal sea water and after 10 or 15 minutes to hypertonic
posure must be brief, from 1% to 3 mintues. The eggs are then trans-
ferred to normal sea water and after 10 or 15 minutes to hypertonic
sea water consisting of 8 cc. of 2% M NaC1 to 50 cc. of sea water. At a
sea water consisting of 8 cc. of 2% M NaC1 to 50 cc. of sea water. At a
temperature of 23° the eggs must remain in this solution from 17% to
temperature of 23° the eggs must remain in this solution from 17% to
Line 13,780: Line 12,714:
obtained from the development of fertilized eggs, go ahead with the
obtained from the development of fertilized eggs, go ahead with the
cleavage process and develop to larvae; doubtless the inability to rear
cleavage process and develop to larvae; doubtless the inability to rear
the larvae is not in any way due to the fact that they were partheno-
the larvae is not in any way due to the fact that they were parthenogenetically produced.
genetically produced.


The explanation of this double procedure has been a matter of some
The explanation of this double procedure has been a matter of some
discussion. Loeb believed that membrane formation sets going certain
discussion. Loeb believed that membrane formation sets going certain
chemical reactions upon which the future development of the egg de-
chemical reactions upon which the future development of the egg depends. These chemical reactions, however, leave the egg in a condition
pends. These chemical reactions, however, leave the egg in a condition
from which it will not itself recover, and unless a second factor is employed in the process it will disintegrate rapidly. These reactions are
from which it will not itself recover, and unless a second factor is em-
ployed in the process it will disintegrate rapidly. These reactions are
on the nature of oxidations and are at least to a certain extent cytolytic
on the nature of oxidations and are at least to a certain extent cytolytic
in nature. The second factor is therefore necessary as a corrective to
in nature. The second factor is therefore necessary as a corrective to
regulate the extensive oxidization which is produced by the exposure
regulate the extensive oxidization which is produced by the exposure
to the first solution. Loeb’s conclusion that cytolysis must take place
to the first solution. Loeb’s conclusion that cytolysis must take place
unless corrected by the hypotonic solution has been questioned by some
unless corrected by the hypotonic solution has been questioned by some
ARTIFICIAL PARTHENOGENESIS 343
ARTIfiCIAL PARTHENOGENESIS 343


later experimenters, notably by Just, who has been able to induce the
later experimenters, notably by Just, who has been able to induce the
development of normal plutei of Arbacia by the use of hypertonic solu-
development of normal plutei of Arbacia by the use of hypertonic solutions alone. The exact preparations of the salts which are used to render
tions alone. The exact preparations of the salts which are used to render
the sea water hypertonic and the durations of the exposure to this
the sea water hypertonic and the durations of the exposure to this
mixture must be regulated with a great exactness if successful results
mixture must be regulated with a great exactness if successful results
Line 13,814: Line 12,744:
which is given off by the unfertilized eggs into the sea water and which
which is given off by the unfertilized eggs into the sea water and which
has been shown to be a necessary intermediary to normal fertilization
has been shown to be a necessary intermediary to normal fertilization
with sperm. Just suggests that the activating agent which will accom-
with sperm. Just suggests that the activating agent which will accomplish experimental parthenogenesis serves to bind the fertilizin produced
plish experimental parthenogenesis serves to bind the fertilizin produced
by the egg and thus to complete the necessary cortical changes whic}
by the egg and thus to complete the necessary cortical changes whic}


must take place if development is to proceed. The full explanation or
must take place if development is to proceed. The full explanation or
the artificially induced changes has perhaps not yet been offered with
the artificially induced changes has perhaps not yet been offered with
regard to the experimental facts. However, there is no question that the
regard to the experimental facts. However, there is no question that the


entire subject has been one of the most successfully studied of all prob-
entire subject has been one of the most successfully studied of all problems of experimental embryology.
lems of experimental embryology.
CHAPTER VI
CHAPTER VI
PAEDOGENESIS AND NEOTENY
PAEDOGENESIS AND NEOTENY
Line 13,831: Line 12,759:
retain their youthful characteristics. These are to be taken up under
retain their youthful characteristics. These are to be taken up under
the general heads of paedogenesis and neoteny although not all the
the general heads of paedogenesis and neoteny although not all the
cases included come under a strict definition of either of these terms.
cases included come under a strict definition of either of these terms.
They occur in a great many widely scattered groups of the animal
They occur in a great many widely scattered groups of the animal
kingdom and present a great many variations some of them so wide
kingdom and present a great many variations some of them so wide
Line 13,838: Line 12,766:
is to be found in the literature dealing with them. Regarding the processes
is to be found in the literature dealing with them. Regarding the processes
under consideration in this chapter exactly such confusion is found,
under consideration in this chapter exactly such confusion is found,
some writers using the terms loosely and failing to classify with sharp-
some writers using the terms loosely and failing to classify with sharpness the cases cited.
ness the cases cited.


The biogenetic law comes into the discussion for the reason that one
The biogenetic law comes into the discussion for the reason that one
may regard a particular phenomenon as recapitulating past phylogenetic
may regard a particular phenomenon as recapitulating past phylogenetic
conditions, or he may look upon the animal showing it as exhibiting
conditions, or he may look upon the animal showing it as exhibiting
neoteny, at least of the characters in question, and perhaps gener-
neoteny, at least of the characters in question, and perhaps generally. Thus the familiar axolotl which is the sexually mature, unmetamorphosed Amblystoma is the usual example of neotenous development,
ally. Thus the familiar axolotl which is the sexually mature, unmeta-
morphosed Amblystoma is the usual example of neotenous development,
but it is also cited by the proponents of recapitulation as explained by
but it is also cited by the proponents of recapitulation as explained by
the general progress in development of the Proteus, Necturus, Ambly-
the general progress in development of the Proteus, Necturus, Amblystoma, Salamandra series of urodele recapitulation. Most of the cases
stoma, Salamandra series of urodele recapitulation. Most of the cases
of this kind, however, are concerned with adult conditions quite as
of this kind, however, are concerned with adult conditions quite as
much as with those of immature forms and therefore would seem to be
much as with those of immature forms and therefore would seem to be
rather outside the scope of the present discussion.
rather outside the scope of the present discussion.


The general subject of neoteny also calls up the problems of hetero-
The general subject of neoteny also calls up the problems of heterochrony, by which is meant a disturbance of the synchrony of development. That is, if one might take the normal series of developmental
chrony, by which is meant a disturbance of the synchrony of develop-
ment. That is, if one might take the normal series of developmental
time stages with each organ in its proper relation to the others as a
time stages with each organ in its proper relation to the others as a
standard, representing perhaps the phylogenetic series, then any de-
standard, representing perhaps the phylogenetic series, then any departure from this standard would be spoken of as heterochrony. (See
parture from this standard would be spoken of as heterochrony. (See
also Chapter III, Part Two, for discussion of heterochrony.) Similarly,
also Chapter III, Part Two, for discussion of heterochrony.) Similarly,
the sequence of embryonic events when disturbed, as in neotenous
the sequence of embryonic events when disturbed, as in neotenous
Line 13,870: Line 12,791:
Oppel and Keibel, although many others have contributed to it, some
Oppel and Keibel, although many others have contributed to it, some
independently and others in collaboration with Keibel in the publication
independently and others in collaboration with Keibel in the publication
of his famous “Normentafeln zur Entwickelungsgeschichte der Wir-
of his famous “Normentafeln zur Entwickelungsgeschichte der Wirbeltiere.” Oppel began this study comparing the different developmental
beltiere.” Oppel began this study comparing the different developmental
stages of different animals and arranging them in tabular form to show
stages of different animals and arranging them in tabular form to show
the comparative progress of the most important organs of vertebrates.
the comparative progress of the most important organs of vertebrates.
Line 13,883: Line 12,803:
an organ is dependent upon the time at which it will be required to
an organ is dependent upon the time at which it will be required to
function. Thus the order of appearance of organs in a developmental
function. Thus the order of appearance of organs in a developmental
series is of itself of phylogenetic significance. But Keibel did not recog-
series is of itself of phylogenetic significance. But Keibel did not recognize the biogenetic law as valid in these cases.
nize the biogenetic law as valid in these cases.


Another early student of heterochrony in vertebrates was Mehnert,
Another early student of heterochrony in vertebrates was Mehnert,
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be considered as but very indirectly concerned with a matter such as
be considered as but very indirectly concerned with a matter such as
this, but a reconsideration of the facts easily brings out a very clear
this, but a reconsideration of the facts easily brings out a very clear
relation, for we find paedogenesis to mean merely that, in an animal
relation, for we find paedogenesis to mean merely that, in an animal
exhibiting this phenomenon, the organs of the body which have to do
exhibiting this phenomenon, the organs of the body which have to do
with reproduction have been much accelerated in development, while
with reproduction have been much accelerated in development, while
Line 13,914: Line 12,833:


During the present century many investigators have contributed to
During the present century many investigators have contributed to
the knowledge.of the general subject. It will perhaps serve as an illus-
the knowledge.of the general subject. It will perhaps serve as an illustration to point out the importance of Stockard’s very extensive study
tration to point out the importance of Stockard’s very extensive study
on the development of Fundulus, particularly with regard to the effect
on the development of Fundulus, particularly with regard to the effect
of changes in the rate and to the various means by which abnormalities
of changes in the rate and to the various means by which abnormalities
Line 13,922: Line 12,840:
It is thus clear that the matters which are the subject of this chapter
It is thus clear that the matters which are the subject of this chapter
really constitute but special cases of heterochrony. In assigning to these
really constitute but special cases of heterochrony. In assigning to these
phenomena as a causal factor the disturbance of the speed of develop-
phenomena as a causal factor the disturbance of the speed of development, we bring them all into one category. It is sometimes difficult to
ment, we bring them all into one category. It is sometimes difficult to
decide whether one organ has undergone a retardation of development
decide whether one organ has undergone a retardation of development
or whether another is accelerated with respect to the normal and so it
or whether another is accelerated with respect to the normal and so it
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Disogeny is the “sexual maturity of one and the same individual in
Disogeny is the “sexual maturity of one and the same individual in
two different conditions, between which a metamorphosis with retro-
two different conditions, between which a metamorphosis with retrogression of the sex products occurs” (Chun).
gression of the sex products occurs” (Chun).


It is true that these definitions savor of dogmatism and of course
It is true that these definitions savor of dogmatism and of course
require much elaboration. It would seem, however, that neoteny and
require much elaboration. It would seem, however, that neoteny and
progenesis are not far apart and that paedogenetic animals may easily
progenesis are not far apart and that paedogenetic animals may easily
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stated, Amblystoma tigrinum occurs in two forms, the one of which is
stated, Amblystoma tigrinum occurs in two forms, the one of which is
technically immature, although it is sexually active. This paedogenic
technically immature, although it is sexually active. This paedogenic
form was first described from the lakes about Mexico City and was
form was first described from the lakes about Mexico City and was
thought to belong to the genus Siredon (S. lichenoides). The relation of
thought to belong to the genus Siredon (S. lichenoides). The relation of
this form to the well-known salamander was only discovered accidentally
this form to the well-known salamander was only discovered accidentally
Line 13,978: Line 12,894:
   
   


Fro. 218. External views of an axolotl (A) and an Amblystoma showing difierences of
Fro. 218. External views of an axolotl (A) and an Amblystoma showing difierences of
gills. body form. and leg development.
gills. body form. and leg development.


Line 13,993: Line 12,909:
The neotenous animal differs in a number of important characters
The neotenous animal differs in a number of important characters
from the type form. It has large external, red gills with gill slits, its tail
from the type form. It has large external, red gills with gill slits, its tail
is long and broad but flattened laterally so that it is adapted for swim-
is long and broad but flattened laterally so that it is adapted for swimming, and the body features are those of a water-living animal. Internal
ming, and the body features are those of a water-living animal. Internal
conditions likewise show immaturity, the skull bones, for example,
conditions likewise show immaturity, the skull bones, for example,
never becoming properly developed. With metamorphosis the animal
never becoming properly developed. With metamorphosis the animal
Line 14,004: Line 12,919:
egg laying.
egg laying.


The neotexiy of axolotl is thus facultative, for with the proper con-
The neotexiy of axolotl is thus facultative, for with the proper conditions the animal does not remain neotenous but becomes an adult
ditions the animal does not remain neotenous but becomes an adult
Amblystoma. Other urodeles, the perennibranchiates, correspond in
Amblystoma. Other urodeles, the perennibranchiates, correspond in
their adult structure very nearly to axolotl and may be looked upon as
their adult structure very nearly to axolotl and may be looked upon as
Line 14,019: Line 12,933:
evidence of reproduction by budding, gemmation, or other modes of
evidence of reproduction by budding, gemmation, or other modes of
asexual type such as are found in the Salpidae, for example, nor is any
asexual type such as are found in the Salpidae, for example, nor is any
metamorphosis known. Development is direct and the small appendicu-
metamorphosis known. Development is direct and the small appendicularia correspond in a general way to the tailed larvae of the ascidians;
laria correspond in a general way to the tailed larvae of the ascidians;
that is, they retain the tail portion of the body with its typical chordate
that is, they retain the tail portion of the body with its typical chordate
characteristics which is lost in the metamorphosis of the more familiar
characteristics which is lost in the metamorphosis of the more familiar
Line 14,039: Line 12,952:
given by Hertwig along with certain other Diptera as an example
given by Hertwig along with certain other Diptera as an example
proving his statement that paedogencsis is parthenogenesis in an
proving his statement that paedogencsis is parthenogenesis in an
immature organism. As is already seen, this statement is much too re-
immature organism. As is already seen, this statement is much too restricted, for the term paedogenesis is of equal application to cases in
stricted, for the term paedogenesis is of equal application to cases in
which inheritance is biparental.
which inheritance is biparental.


Line 14,048: Line 12,960:


student of this genus in America. No reproduction takes place during
student of this genus in America. No reproduction takes place during
the winter, and the process is interrupted in midsummer by the appear-
the winter, and the process is interrupted in midsummer by the appearance of male and female adults. The larva of Miastor possesses two
ance of male and female adults. The larva of Miastor possesses two
ovaries in the tenth and eleventh segments. In each are thirty-two
ovaries in the tenth and eleventh segments. In each are thirty-two


Line 14,056: Line 12,967:
separated off from the rest of the ovary and in a distant part of the
separated off from the rest of the ovary and in a distant part of the
body grows and develops at the expense of the tissues of the mother
body grows and develops at the expense of the tissues of the mother
larva. This process is repeated until five to seventeen separated growing
larva. This process is repeated until five to seventeen separated growing
oocytes are thus produced from one mother larva. Then one division
oocytes are thus produced from one mother larva. Then one division
takes place, the polar body which is given off divides again and both
takes place, the polar body which is given off divides again and both
Line 14,063: Line 12,974:
the germ cells, the pole plasm is segregated and the embryo gradually
the germ cells, the pole plasm is segregated and the embryo gradually
takes on its characteristic form. No oviducts are present in the mother
takes on its characteristic form. No oviducts are present in the mother
larva nor is there provision for the escape of the young thus paedogeneti-
larva nor is there provision for the escape of the young thus paedogenetically produced. They escape by rupturing the body wall of the mother
cally produced. They escape by rupturing the body wall of the mother
larva, which is left to die. After the production of a number of generations in this manner, the last larvae pupate and emerge as normal adult
larva, which is left to die. After the production of a number of genera-
tions in this manner, the last larvae pupate and emerge as normal adult
males and females.
males and females.


Line 14,072: Line 12,981:
eggs. To this form of paedogenesis in the chrysalis Packard gave the
eggs. To this form of paedogenesis in the chrysalis Packard gave the
name chrysallogenesis, although the differences from other types of
name chrysallogenesis, although the differences from other types of
paedogenesis are so slight as to make the retention of the term of doubt-
paedogenesis are so slight as to make the retention of the term of doubtful necessity. In the autumn other pupa change to flies without laying
ful necessity. In the autumn other pupa change to flies without laying
eggs and these adults are more prolific than the spring pupae were.
eggs and these adults are more prolific than the spring pupae were.
The process was described as a seasonal phenomenon depending upon
The process was described as a seasonal phenomenon depending upon
temperature.
temperature.


Pacdogenetic reproduction has also been reported for the Tenthre-
Pacdogenetic reproduction has also been reported for the Tenthredinidae, the saw flies, thus extending this phenomenon to a second order
dinidae, the saw flies, thus extending this phenomenon to a second order
of the insects, the Hymenoptera. '
of the insects, the Hymenoptera. '


The molluscs show one case of neoteny in the shell-less snail, Stame-
The molluscs show one case of neoteny in the shell-less snail, Stamedorsia verrucosa, which according to Cuénot reproduces long before true
dorsia verrucosa, which according to Cuénot reproduces long before true
adulthood is reached.
adulthood is reached.


Line 14,098: Line 13,004:
one within the other.
one within the other.


The second case of this group is that of Polystoma integerrimum orig-
The second case of this group is that of Polystoma integerrimum originally described by Zeller in 1872. The embryo hatches in the water
inally described by Zeller in 1872. The embryo hatches in the water
and swims Freely. It seeks for a young frog tadpole which it must find
and swims Freely. It seeks for a young frog tadpole which it must find
within twenty-four hours or die. If one is found it creeps over the surface
within twenty-four hours or die. If one is found it creeps over the surface
until it finds the branchial opening, which it quickly enters; it undergoes
until it finds the branchial opening, which it quickly enters; it undergoes
metamorphosis, and passes down the alimentary canal to the rectum
metamorphosis, and passes down the alimentary canal to the rectum
and thence to the urinary bladder. Here it remains for three years to
and thence to the urinary bladder. Here it remains for three years to
Line 14,108: Line 13,013:
has attacked a very young tadpole which still has external gills. In this
has attacked a very young tadpole which still has external gills. In this
case it remains in the gill chamber where nutriment is abundant, grows
case it remains in the gill chamber where nutriment is abundant, grows
rapidly, and becomes sexually mature in the short space of five weeks.
rapidly, and becomes sexually mature in the short space of five weeks.
It does not then pass further along the alimentary tract but dies before
It does not then pass further along the alimentary tract but dies before
the metamorphosis of its host. It differs in its structure as well as its
the metamorphosis of its host. It differs in its structure as well as its
Line 14,117: Line 13,022:
to the paedogenetic P. integerrimum.
to the paedogenetic P. integerrimum.


Among the digenetic trematodes the life cycle of the liver-flukes in-
Among the digenetic trematodes the life cycle of the liver-flukes involves questions which are of interest in this connection. The main facts
volves questions which are of interest in this connection. The main facts
are well known and are referred to in several chapters of this work. In
are well known and are referred to in several chapters of this work. In
both rediae and cercariae reproduction may take place and daughter
both rediae and cercariae reproduction may take place and daughter
rediae, and daughter cercariae may be produced. If it can be shown
rediae, and daughter cercariae may be produced. If it can be shown
that these daughter forms are produced from eggs, either partheno-
that these daughter forms are produced from eggs, either parthenogenetically or bisexually, then this is a case of paedogenesis. However,
genetically or bisexually, then this is a case of paedogenesis. However,
it has lately been shown for some flukes that the germ balls from which
it has lately been shown for some flukes that the germ balls from which
the daughter larvae develop are budded off asexually and never undergo
the daughter larvae develop are budded off asexually and never undergo
any chromosome reduction (F. G. Brooks), so that for these forms at
any chromosome reduction (F. G. Brooks), so that for these forms at
least it cannot be said that paedogenesis occurs in the flukes. It has been
least it cannot be said that paedogenesis occurs in the flukes. It has been
the usual view, however, that there is here the production of partheno-
the usual view, however, that there is here the production of parthenogenetic ova, and hence paedogenesis.
genetic ova, and hence paedogenesis.


Of the examples usually recognized, the final one is that of the lobate
Of the examples usually recognized, the final one is that of the lobate
ctenophore, Bolina hydatina. Here the cydippid larvae become sexually
ctenophore, Bolina hydatina. Here the cydippid larvae become sexually
mature, producing eggs and sperm. Fertilization follows and the eggs
mature, producing eggs and sperm. Fertilization follows and the eggs
develop in the regular manner. The larval gonads subsequently degen-
develop in the regular manner. The larval gonads subsequently degenerate, metamorphosis takes place, a new set of gonads appear, the
erate, metamorphosis takes place, a new set of gonads appear, the
animals again attain sexual maturity, producing eggs and sperm, this
animals again attain sexual maturity, producing eggs and sperm, this
time as adults.
time as adults.
Line 14,145: Line 13,046:
In addition to these, experimentally produced delay or acceleration
In addition to these, experimentally produced delay or acceleration
of development are well known. Frogs transferred as larvae to alpine
of development are well known. Frogs transferred as larvae to alpine
heights where the winters come early have remained in the larval con-
heights where the winters come early have remained in the larval condition over the winter. High temperatures hasten sexual maturity.
dition over the winter. High temperatures hasten sexual maturity.
Brackish water or fresh water will often hasten the maturity of oceanic
Brackish water or fresh water will often hasten the maturity of oceanic
forms. Hunger in some forms and overfeeding in others result in hetero-
forms. Hunger in some forms and overfeeding in others result in heterochronic growth. Termites which are fed in a certain manner mature
chronic growth. Termites which are fed in a certain manner mature
very early while the wings are still undeveloped and eyes have not yet
very early while the wings are still undeveloped and eyes have not yet
appeared (Grassi). Parasitism may be looked upon as a strong factor
appeared (Grassi). Parasitism may be looked upon as a strong factor
Line 14,156: Line 13,055:
It may be observed that there have been omitted many cases of
It may be observed that there have been omitted many cases of
larval budding and other forms of asexual reproduction such as may be
larval budding and other forms of asexual reproduction such as may be
so commonly found, for example, among jellyfishcs, liver—flukes, bryozoa,
so commonly found, for example, among jellyfishcs, liver—flukes, bryozoa,
and tunicates. These cases, though not a far step from the types dis-
and tunicates. These cases, though not a far step from the types discussed in this chapter, are not properly considered here, for paedogenesis
cussed in this chapter, are not properly considered here, for paedogenesis
and neoteny are matters of sexual reproduction. It is admitted that in
and neoteny are matters of sexual reproduction. It is admitted that in
some cases, as already shown for the 1iver—flukes, the distinctions are
some cases, as already shown for the 1iver—flukes, the distinctions are
hard to draw, but for the sake of clarity it is usually thought wiser to
hard to draw, but for the sake of clarity it is usually thought wiser to
adhere to the definitions given.
adhere to the definitions given.
Line 14,174: Line 13,072:
somatic stages the organs in question have fallen behind the others, in
somatic stages the organs in question have fallen behind the others, in
short they have become distinctly heterochronic. Bolk has discussed
short they have become distinctly heterochronic. Bolk has discussed
the features of man which resemble the structure of embryos of anthro-
the features of man which resemble the structure of embryos of anthropoid apes, assuming that the latter‘are nearer the ancestral forms of
poid apes, assuming that the latter‘are nearer the ancestral forms of
structure. Among the features of man which show resemblance to the
structure. Among the features of man which show resemblance to the
embryonic structures of the ancestral types, for which he uses the term
embryonic structures of the ancestral types, for which he uses the term
foetalization, are the relatively high weight of the brain, the retention
foetalization, are the relatively high weight of the brain, the retention
of the embryonic cranial flexure with the resulting erect posture as Bolk
of the embryonic cranial flexure with the resulting erect posture as Bolk
thinks to have demonstrated, the position of the foramen magnum, the
thinks to have demonstrated, the position of the foramen magnum, the
late closure of the skull sutures, the flatness of the face, lack of hair on
late closure of the skull sutures, the flatness of the face, lack of hair on
the body, and others. Bolk’s study of cranial flexure and human posture
the body, and others. Bolk’s study of cranial flexure and human posture
comparing both adult and ancestral conditions is particularly interest-
comparing both adult and ancestral conditions is particularly interesting. He finds as a result that the flat face as compared with the elongated
ing. He finds as a result that the flat face as compared with the elongated
muzzle of other mammals is largely responsible for the trend of human
muzzle of other mammals is largely responsible for the trend of human
evolution with regard to vision and other special senses, the character
evolution with regard to vision and other special senses, the character
Line 14,194: Line 13,090:


One other illustration, from those given by De Beer, may be cited to
One other illustration, from those given by De Beer, may be cited to
show the part that neoteny may have played in evolution. It is a com-
show the part that neoteny may have played in evolution. It is a comparison between the important structural characteristics of adult insects
parison between the important structural characteristics of adult insects
and larval myriapods. The larva of Iulus has a head composed of six or
and larval myriapods. The larva of Iulus has a head composed of six or
seven segments, an elongated segmented body, the first three metameres
seven segments, an elongated segmented body, the first three metameres
of which bear pairs of legs whereas posterior segments bear only rudi-
of which bear pairs of legs whereas posterior segments bear only rudimentary legs at the time of hatching or shortly thereafter (Metchnikoff).
mentary legs at the time of hatching or shortly thereafter (Metchnikoff).
These features are quite insect like, in that the insect head has six or
These features are quite insect like, in that the insect head has six or
seven segments, the thorax three, each bearing a pair of legs, and the
seven segments, the thorax three, each bearing a pair of legs, and the
Line 14,211: Line 13,105:


From these cases it would appear that the study of neoteny from the
From these cases it would appear that the study of neoteny from the
standpoint of embryology offers a productive field of quite a new order
standpoint of embryology offers a productive field of quite a new order
for investigations and that the conclusions reached from researches of
for investigations and that the conclusions reached from researches of
this kind may profoundly affect our ideas of phylogeny.
this kind may profoundly affect our ideas of phylogeny.
Line 14,218: Line 13,112:


By polyembryony is meant among zoologists the production of
By polyembryony is meant among zoologists the production of
multiple embryos from a single egg. (This definition does not apply to
multiple embryos from a single egg. (This definition does not apply to
botanical nomenclature.) The number of individuals produced from a
botanical nomenclature.) The number of individuals produced from a
single egg ranges from hundreds as in the parasitic Hymenoptera down
single egg ranges from hundreds as in the parasitic Hymenoptera down
to two, although in the latter case the condition is usually known as
to two, although in the latter case the condition is usually known as
twinning, and not all types of twins are properly thought of as poly-
twinning, and not all types of twins are properly thought of as polyembryonic.- Polyembryony occurs very widely distributed through the
embryonic.- Polyembryony occurs very widely distributed through the
animal kingdom in groups which are totally unrelated to each other.
animal kingdom in groups which are totally unrelated to each other.
Because of this wide distribution the literature to which reference can
Because of this wide distribution the literature to which reference can
be made in this connection is really very extensive and the significance
be made in this connection is really very extensive and the significance
of some of the cases extends beyond the realm of embryology. Of the
of some of the cases extends beyond the realm of embryology. Of the
numerous investigators who have studied the question only a few need
numerous investigators who have studied the question only a few need
Line 14,233: Line 13,126:
not included in this discussion. Patterson has summarized the knowledge
not included in this discussion. Patterson has summarized the knowledge
of polyembryony in a paper in Volume II of the Quarterly Review of
of polyembryony in a paper in Volume II of the Quarterly Review of
Biology and it is suggested that the student consult this paper in be-
Biology and it is suggested that the student consult this paper in beginning a more extensive study of these problems.
ginning a more extensive study of these problems.


Patterson recognized three types of polyembryony: “ (1) experimental
Patterson recognized three types of polyembryony: “ (1) experimental
polyembryony, or the production of multiple embryos by artificial
polyembryony, or the production of multiple embryos by artificial
means; (2) accidental or sporadic polyembryony, or the occasional pro-
means; (2) accidental or sporadic polyembryony, or the occasional production of multiple embryos in the species which is typically monembryonic; (3) specific polyembryony, or the habitual production of
duction of multiple embryos in the species which is typically mon-
multiple embryos in a given species.” The general student of comparative embryology is interested in the last type much more than in
embryonic; (3) specific polyembryony, or the habitual production of
multiple embryos in a given species.” The general student of com-
parative embryology is interested in the last type much more than in
the first two, although cases of the first two throw much light upon
the first two, although cases of the first two throw much light upon
many fundamental problems of organization of the egg and embryo
many fundamental problems of organization of the egg and embryo
and offer a very stimulating field for the experimental embryologist.
and offer a very stimulating field for the experimental embryologist.
Many types of eggs whose normal development includes no hint of
Many types of eggs whose normal development includes no hint of
polyembryony can be induced to produce double monsters and even
polyembryony can be induced to produce double monsters and even
complete embryos by experimental means.
complete embryos by experimental means.


Cases of occasional or sporadic polyembryony are recorded for coel-
Cases of occasional or sporadic polyembryony are recorded for coelenterates, cestodes, annelids, echinoderms, arthropods, and vertebrates. Perhaps because the latter group is so much more studied, there
enterates, cestodes, annelids, echinoderms, arthropods, and verte-
brates. Perhaps because the latter group is so much more studied, there


353
353
Line 14,259: Line 13,146:
have been more cases reported for the vertebrates than for the others
have been more cases reported for the vertebrates than for the others
and, as Patterson points out, it is here that the occasional identical
and, as Patterson points out, it is here that the occasional identical
twins of the human species should be classified.
twins of the human species should be classified.


Specific polyembryony, to which our attention is drawn as the
Specific polyembryony, to which our attention is drawn as the
special problem of the comparative embryologist, is found in the follow-
special problem of the comparative embryologist, is found in the following groups of animals: flatworms, bryozoa belonging to the Cyclostomata, earthworms, parasitic Hymenoptera, and the mammals, especially
ing groups of animals: flatworms, bryozoa belonging to the Cyclostom-
ata, earthworms, parasitic Hymenoptera, and the mammals, especially
as illustrated by the armadillo. It is of more widespread distribution,
as illustrated by the armadillo. It is of more widespread distribution,
however, than is indicated by these groups, but here are included the
however, than is indicated by these groups, but here are included the
Line 14,270: Line 13,155:


An inspection of this list is sufficient to show that polyembryony has
An inspection of this list is sufficient to show that polyembryony has
no phylogenetic or taxonomic significance, for the groups are too widely
no phylogenetic or taxonomic significance, for the groups are too widely
separated and too diverse in structure to admit of an interpretation of
separated and too diverse in structure to admit of an interpretation of
this kind. Moreover, the structural differences both of adults and
this kind. Moreover, the structural differences both of adults and
embryos in these various groups are so great that it is not possible to
embryos in these various groups are so great that it is not possible to
look for the causes of the phenomena in any simple embryological
look for the causes of the phenomena in any simple embryological
process common to all. Doubtless in the final analysis all these processes
process common to all. Doubtless in the final analysis all these processes
have a common underlying causal factor which is bound up with the
have a common underlying causal factor which is bound up with the
innate protoplasmic organization of the egg substance.
innate protoplasmic organization of the egg substance.
Line 14,284: Line 13,169:
qualities of the living substance which make possible its reproduction
qualities of the living substance which make possible its reproduction
are basic to the one case no more than to the other. We must recognize
are basic to the one case no more than to the other. We must recognize
that specific polyembryony is as much a characteristic of certain animals
that specific polyembryony is as much a characteristic of certain animals
as is the formation of a coelome. At a certain stage in development there
as is the formation of a coelome. At a certain stage in development there
occurs a series of events which lead perhaps to two buds, or more, from
occurs a series of events which lead perhaps to two buds, or more, from
Line 14,302: Line 13,187:
that the blastomeres in the 2-cell stage become separated and each
that the blastomeres in the 2-cell stage become separated and each
gives rise to an embryo. This is a view with few observational data to
gives rise to an embryo. This is a view with few observational data to
support it, but it may be presumed to find considerable support in the
support it, but it may be presumed to find considerable support in the
THE CAUSES OF POLYEMBRYONY 355
THE CAUSES OF POLYEMBRYONY 355


Line 14,313: Line 13,198:
do not cohere to one another. In some of these experiments the isolated
do not cohere to one another. In some of these experiments the isolated
blastomeres have lived and developed for a time; in others they have
blastomeres have lived and developed for a time; in others they have
produced partial larvae (ascidians etc.); and in others they have de-
produced partial larvae (ascidians etc.); and in others they have developed into whole larvae (amphioxus, Cerebratulus). But in forms
veloped into whole larvae (amphioxus, Cerebratulus). But in forms
where direct evidence for blastotomy is possible none has been found
where direct evidence for blastotomy is possible none has been found
which forces one to this view for cases of polyembryony. As will be
which forces one to this view for cases of polyembryony. As will be
Line 14,338: Line 13,222:
harmonize well with this explanation.
harmonize well with this explanation.


This ‘theory of budding has been criticized rather severely, particu-
This ‘theory of budding has been criticized rather severely, particularly by Assheton, on the grounds that budding cannot take place unless
larly by Assheton, on the grounds that budding cannot take place unless
there is a stock from which the buds may arise and the presence of a
there is a stock from which the buds may arise and the presence of a
stock Assheton claims was not demonstrated in the cases to which the
stock Assheton claims was not demonstrated in the cases to which the
theory was applied. Rather he interprets the described facts as cases of
theory was applied. Rather he interprets the described facts as cases of
fission. The blastocyst of several mammals, for he was particularly con-
fission. The blastocyst of several mammals, for he was particularly considering the theory as applied to the armadillo, he described as undergoing direct fission into two embryonic rudiments. As a matter of fact
sidering the theory as applied to the armadillo, he described as under-
going direct fission into two embryonic rudiments. As a matter of fact
the fission hypothesis does not differ from the idea of budding in relation
the fission hypothesis does not differ from the idea of budding in relation
to the facts as described, but is primarily a redefinition of them, for in
to the facts as described, but is primarily a redefinition of them, for in
both cases the embryonic vesicle is regarded as divided into several
both cases the embryonic vesicle is regarded as divided into several
primordia, each of which is the beginning of a distinct formative area
primordia, each of which is the beginning of a distinct formative area
Line 14,355: Line 13,236:
emphasis is placed upon the embryonic mass which is thought to bud
emphasis is placed upon the embryonic mass which is thought to bud
or upon the separate areas which arise from it as would be the case
or upon the separate areas which arise from it as would be the case
in fission does not seem to involve any particular difference in the result
in fission does not seem to involve any particular difference in the result
nor to carry the explanation of the environmental processes much
nor to carry the explanation of the environmental processes much
further toward a final analysis.
further toward a final analysis.


As an explanation of the process a physiological interpretation must
As an explanation of the process a physiological interpretation must
be called on. Stockard has pointed out that if a developmental pause
be called on. Stockard has pointed out that if a developmental pause
occurs at the critical moment in the formative stages of an embryo, a
occurs at the critical moment in the formative stages of an embryo, a
series of consequences ranging from simple malformation up to the pro-
series of consequences ranging from simple malformation up to the production of double monsters or even two individuals may result. He
duction of double monsters or even two individuals may result. He
applies this conception to the explanation of polyembryony, supposing
applies this conception to the explanation of polyembryony, supposing
that the reason for the loss of dominance of the first formative region
that the reason for the loss of dominance of the first formative region
of the embryo and the subsequent ascendency of the primary and
of the embryo and the subsequent ascendency of the primary and
secondary buds is connected in some way with the developmental pause.
secondary buds is connected in some way with the developmental pause.
Line 14,374: Line 13,254:
and from these formative areas the multiple embryos are produced.
and from these formative areas the multiple embryos are produced.


An obvious connection exists between the phenomenon of poly-
An obvious connection exists between the phenomenon of polyembryony and that of metagenesis which involves at least the alternation
embryony and that of metagenesis which involves at least the alternation
of one sexually produced generation with an asexually produced one. It
of one sexually produced generation with an asexually produced one. It
is usually the practice to limit alternation of generations to the lower
is usually the practice to limit alternation of generations to the lower
Line 14,383: Line 13,262:
of cells may be looked upon as one generation, namely the one produced
of cells may be looked upon as one generation, namely the one produced
from the fertilized egg, and that it is completed when it becomes a
from the fertilized egg, and that it is completed when it becomes a
stock from which other buds, that is growing points, begin their de-
stock from which other buds, that is growing points, begin their development. This point of view has its application even to mammals
velopment. This point of view has its application even to mammals
whether only a single organism results or several as in the case of the
whether only a single organism results or several as in the case of the
armadillo. Here the blastocyst would be regarded as the sexually pro-
armadillo. Here the blastocyst would be regarded as the sexually produced individual and the buds which give rise to the four young as
duced individual and the buds which give rise to the four young as
those asexually produced from it.
those asexually produced from it.


Line 14,403: Line 13,280:
the animal kingdom.”
the animal kingdom.”


If the blastocyst is to be looked upon as a sexually produced in-
If the blastocyst is to be looked upon as a sexually produced individual from which arises asexually another or several others of a
dividual from which arises asexually another or several others of a
second generation, it is suggested that in this fact lies the explanation
second generation, it is suggested that in this fact lies the explanation


FIG. 219. The development of the ovicell in Crista remosa. (From Patteron, after
fiG. 219. The development of the ovicell in Crista remosa. (From Patteron, after
Harmer.)
Harmer.)


Line 14,413: Line 13,289:
from polypide-bud; ov., ovary; ovi., oviccll.
from polypide-bud; ov., ovary; ovi., oviccll.


of the difliculties that have met every attempt to homologize the early
of the difliculties that have met every attempt to homologize the early
development of the mammals with that of the lower vertebrate classes.
development of the mammals with that of the lower vertebrate classes.
These differences have been discussed in Chapter X on the formation
These differences have been discussed in Chapter X on the formation
of the mammalian embryo; they constitute a problem of major im-
of the mammalian embryo; they constitute a problem of major importance to the comparative embryologist.
portance to the comparative embryologist.


B. Onsnnvnn CASES or POLYEMBRYONY
B. Onsnnvnn CASES or POLYEMBRYONY


We may now devote ourselves to the consideration of the groups of
We may now devote ourselves to the consideration of the groups of
organisms in which specific polyembryony has already been noted to
organisms in which specific polyembryony has already been noted to
358 POLYEM BRYON Y
358 POLYEM BRYON Y


Line 14,429: Line 13,304:
suggested explanations.
suggested explanations.


Flatworms. Among the flatworms are many cases which depart from
flatworms. Among the flatworms are many cases which depart from
the usual methods of reproduction. Of these some which do not fully
the usual methods of reproduction. Of these some which do not fully
fit into the classification have been described
fit into the classification have been described
from time to time as polyembryony. There
from time to time as polyembryony. There
is one flatworm in which polyembryony un-
is one flatworm in which polyembryony undoubtedly occurs, however; it is the cestode
doubtedly occurs, however; it is the cestode
Taema echmococcus, or Echmococcus coenurus
Taema echmococcus, or Echmococcus coenurus
as it is sometimes known. This small tape-
as it is sometimes known. This small tapeworm produces eggs which develop into
worm produces eggs which develop into
the usual hooked embryo, the onchosphere,
the usual hooked embryo, the onchosphere,
and these in their turn produce a cyst which
and these in their turn produce a cyst which
Line 14,452: Line 13,325:
secondary bladders which produce multiple
secondary bladders which produce multiple
scolices in their turn are described. Thus
scolices in their turn are described. Thus
the encysted worm may grow to an enor-
the encysted worm may grow to an enormous size to endanger the life of the host and
mous size to endanger the life of the host and
oftentimes bring about its death.
oftentimes bring about its death.


Line 14,461: Line 13,333:
animals live in colonies made up of zooecia
animals live in colonies made up of zooecia


FIG 220- Section through which are in general tubular with densely
fiG 220- Section through which are in general tubular with densely


a follicle of Cnaza remosa show- - -
a follicle of Cnaza remosa show- - mg primary embryo (1) which calcareous walls. The circular orifices of the
mg primary embryo (1) which calcareous walls. The circular orifices of the


§>ré>dt:)c1I(IiL(zisecorZ<I‘i‘ary erlgnbgnis zooecia give the group their name. At the time
§>ré>dt:)c1I(IiL(zisecorZ<I‘i‘ary erlgnbgnis zooecia give the group their name. At the time
son, Xftei’ H$fi;e,_,r°m 3 e ' of the breeding season a curious specialized
son, Xftei’ H$fi;e,_,r°m 3 e ' of the breeding season a curious specialized
zooecium develops which is called the oecium
zooecium develops which is called the oecium


Line 14,480: Line 13,351:
is capable of forming a new colony upon escape from the oecium.
is capable of forming a new colony upon escape from the oecium.
Earthworm. In the earthworm of the species Lumbricus trapczoides
Earthworm. In the earthworm of the species Lumbricus trapczoides
(Helodrilus caliginosus trapezoides) polyembryony results in the pro-
(Helodrilus caliginosus trapezoides) polyembryony results in the production of twins, a process which by Kleinenberg was regarded as
duction of twins, a process which by Kleinenberg was regarded as
universal for the species, but by Vejdovsky was held to be abnormal.
universal for the species, but by Vejdovsky was held to be abnormal.
It is due to a process of fission of the embryo. The cleavage of the egg
It is due to a process of fission of the embryo. The cleavage of the egg


   
   
Line 14,490: Line 13,360:
C D
C D


FIG. 221. Twinning in the earthworm, Lumbncus trapezoides. (From Patterson, A, B, C.
fiG. 221. Twinning in the earthworm, Lumbncus trapezoides. (From Patterson, A, B, C.
after Kleinenberg.)
after Kleinenberg.)


Line 14,497: Line 13,367:
formed when embryos fail to separate.
formed when embryos fail to separate.


is much modified from the typical spiral form of the annelids and indeed
is much modified from the typical spiral form of the annelids and indeed
is variable. A blastula is formed, the endoderm and mesoblast cells pass
is variable. A blastula is formed, the endoderm and mesoblast cells pass
into the cavity and the entire mass begins to elongate. Across the
into the cavity and the entire mass begins to elongate. Across the
Line 14,512: Line 13,382:
earthworms are produced.
earthworms are produced.


In two other genera of oligochaetes double monsters have been de-
In two other genera of oligochaetes double monsters have been described, and one infers that the twinning phenomena, though rare, may
scribed, and one infers that the twinning phenomena, though rare, may
occur in a number of families. These cases were Tubifea: tubifex, found
occur in a number of families. These cases were Tubifea: tubifex, found
by Welch, Tubzfex rivulorum by Penner, and Sparganophilus eiseni by
by Welch, Tubzfex rivulorum by Penner, and Sparganophilus eiseni by
Line 14,520: Line 13,389:
Parasitic Hymenoptera. In the parasitic wasps we find some of the
Parasitic Hymenoptera. In the parasitic wasps we find some of the
most important and complex cases of polyembryony in the entire
most important and complex cases of polyembryony in the entire
animal kingdom, and certainly here the results of the process are ex-
animal kingdom, and certainly here the results of the process are exemplified in the most striking manner. In a single brood hatching from
emplified in the most striking manner. In a single brood hatching from
one parasitized caterpillar hundreds of individuals may be seen to
one parasitized caterpillar hundreds of individuals may be seen to
issue all developed from one egg. Our knowledge of polyembryony in
issue all developed from one egg. Our knowledge of polyembryony in
Line 14,530: Line 13,398:
1921, 1927), Hill (1922, 1923), and Leiby and Hill (1923, 1924), as well
1921, 1927), Hill (1922, 1923), and Leiby and Hill (1923, 1924), as well
as others. The important genera studied include Litomastix truncatellus,
as others. The important genera studied include Litomastix truncatellus,
Ageniaspis fuscicollis, several species of Copidosoma, Paracopz'doso-
Ageniaspis fuscicollis, several species of Copidosoma, Paracopz'dosomopsis floridanus, and three species of Platygaster. The most recent study
mopsis floridanus, and three species of Platygaster. The most recent study
is that of Parker (1931) upon the braconid, M acrocentrus. Undoubtedly
is that of Parker (1931) upon the braconid, M acrocentrus. Undoubtedly
many other forms of insects show polyembryony, but the ones mentioned
many other forms of insects show polyembryony, but the ones mentioned
Line 14,539: Line 13,406:
these forms is perhaps best understood by beginning as Patterson has
these forms is perhaps best understood by beginning as Patterson has
done in the paper earlier referred to with a description of Platygaster
done in the paper earlier referred to with a description of Platygaster
hiemalis, a parasite of the Hessian fly, which usually produces two in-
hiemalis, a parasite of the Hessian fly, which usually produces two individuals from one egg. From this comparatively simple case we have
dividuals from one egg. From this comparatively simple case we have
a gradual increase in complexity which at the end of the series is only
a gradual increase in complexity which at the end of the series is only
incompletely understood, but the simpler cases at least are suggestive
incompletely understood, but the simpler cases at least are suggestive
Line 14,554: Line 13,420:
cytoplasm surrounding it become cut off from the remainder and
cytoplasm surrounding it become cut off from the remainder and
constitute the embryonic region, for only from it comes the material
constitute the embryonic region, for only from it comes the material
which will go into the formation of the developing embryos. The re-
which will go into the formation of the developing embryos. The rePARASITIC HYMENOPTERA 36 I
PARASITIC HYMENOPTERA 36 I


mainder of the egg containing the paranucleus and its own cytoplasm
mainder of the egg containing the paranucleus and its own cytoplasm
entirely surrounding the embryonic region functions to absorb and
entirely surrounding the embryonic region functions to absorb and


FIG 222. Polyembryonie development of Platyoaster hwmalw (From Patterson, after
fiG 222. Polyembryonie development of Platyoaster hwmalw (From Patterson, after
Leiby and Hill )
Leiby and Hill )


A. Egg of four hours, showing sperm head and first maturation division B, Egg show-
A. Egg of four hours, showing sperm head and first maturation division B, Egg showing two polocytes. and both pronuclei C, Egg with pronuclei in comunction and polar
ing two polocytes. and both pronuclei C, Egg with pronuclei in comunction and polar
nucleus D. Embryo, two polar nuclei and a. parasitic body showing four nuclei E, Enclosed within a cyst formed from tissue of the host are two embryonic bodies each surrounded by trophamnion F. A later stage in the development of two embryos G, A
nucleus D. Embryo, two polar nuclei and a. parasitic body showing four nuclei E, En-
closed within a cyst formed from tissue of the host are two embryonic bodies each sur-
rounded by trophamnion F. A later stage in the development of two embryos G, A
thirteen-day-old polygerm in section, showing several embryos.
thirteen-day-old polygerm in section, showing several embryos.


Line 14,579: Line 13,441:


The paranucleus as development proceeds divides amitotically twice
The paranucleus as development proceeds divides amitotically twice
and the daughters distribute themselves in the trophamnion surround-
and the daughters distribute themselves in the trophamnion surrounding the embryonic region. The zygotic nucleus of the embryonic region
ing the embryonic region. The zygotic nucleus of the embryonic region
divides first into two, then four, embryonic nuclei. Thereupon, the
divides first into two, then four, embryonic nuclei. Thereupon, the
embryonic region becomes constricted and presently separated into
embryonic region becomes constricted and presently separated into
two regions, each provided with two nuclei, and the trophamnion with
two regions, each provided with two nuclei, and the trophamnion with
Line 14,595: Line 13,456:
the next year.
the next year.


In another species of this genus, P. vernalis, eight embryos are regu-
In another species of this genus, P. vernalis, eight embryos are regularly developed. Here the process has a fundamental similarity to that
larly developed. Here the process has a fundamental similarity to that
just described, but the details of development differ. The parasitic body
just described, but the details of development differ. The parasitic body
develops a number of embryonic nuclei surrounded by an appropriate
develops a number of embryonic nuclei surrounded by an appropriate
Line 14,614: Line 13,474:
the larval differentiation begins.
the larval differentiation begins.


Armadillo. The final case of polyembryony to be discussed is perhaps
Armadillo. The final case of polyembryony to be discussed is perhaps
the one in which the greatest interest lies. The Texas nine-banded
the one in which the greatest interest lies. The Texas nine-banded
armadillo Dasypus (Tatusia) novemcinctus normally produces four
armadillo Dasypus (Tatusia) novemcinctus normally produces four
Line 14,646: Line 13,506:
the ectodermal cells takes place, resulting in the formation of the em~
the ectodermal cells takes place, resulting in the formation of the em~
bryonic shield with its thick ectoderm and the true amnion above it.
bryonic shield with its thick ectoderm and the true amnion above it.
In this stage the first sign of polyembryony makes its appearance, for
In this stage the first sign of polyembryony makes its appearance, for
from opposite sides of the ectodermal vesicle thus formed blunt pro-
from opposite sides of the ectodermal vesicle thus formed blunt projections extend laterally. Patterson called these primary buds. By this
jections extend laterally. Patterson called these primary buds. By this
time that portion of the trophoblast which has not become involved
time that portion of the trophoblast which has not become involved
in the attachment to the uterine wall disappears and the yolk sac
in the attachment to the uterine wall disappears and the yolk sac
Line 14,658: Line 13,517:
positions that are about equally spaced from each other.
positions that are about equally spaced from each other.


Meanwhile the vesicle grows, and the endoderm of the yolk sac, in-
Meanwhile the vesicle grows, and the endoderm of the yolk sac, including those portions with which the embryonic ectoderm of each bud
cluding those portions with which the embryonic ectoderm of each bud
is in contact and which will form the gut endoderm of the embryo,
is in contact and which will form the gut endoderm of the embryo,
faces the uterine cavity. The anterior ends of all the embryos point
faces the uterine cavity. The anterior ends of all the embryos point
Line 14,665: Line 13,523:
original amniotic cavity, and the entire vesicle may now be spoken of
original amniotic cavity, and the entire vesicle may now be spoken of
as the common amniotic vesicle. The entire structure now grows very
as the common amniotic vesicle. The entire structure now grows very
rapidly, especially that portion of it which originated from the tropho-
rapidly, especially that portion of it which originated from the trophoblastic knob or the Trdger. This growth finally comes to occupy most
blastic knob or the Trdger. This growth finally comes to occupy most
364 POLYEMBRYONY
364 POLYEMBRYONY


of the space in the fundus of the uterus. The further history is especially
of the space in the fundus of the uterus. The further history is especially
concerned with the embryonic buds. Their posterior ends lengthen out
concerned with the embryonic buds. Their posterior ends lengthen out
with the growth of the vesicle and finally unite at a point opposite the
with the growth of the vesicle and finally unite at a point opposite the
original attachment and from their point of union the umbilicus later
original attachment and from their point of union the umbilicus later
arises. The common amniotic vesicle by this growth procedure is left
arises. The common amniotic vesicle by this growth procedure is left


FIG. 223. The development of the blastocyst of the armadillo. (After Patterson.)
fiG. 223. The development of the blastocyst of the armadillo. (After Patterson.)
ec., ectoderm; en., endoderm; icm., inner cell mass; mes.. mesoderm; tr., trager; tro.,
ec., ectoderm; en., endoderm; icm., inner cell mass; mes.. mesoderm; tr., trager; tro.,
trophoblast; u.. uterus.
trophoblast; u.. uterus.
Line 14,682: Line 13,539:
most of the remaining portion of the cyst mass with its developing
most of the remaining portion of the cyst mass with its developing
embryos is derived from the growth of the Trdger. The buds meanwhile
embryos is derived from the growth of the Trdger. The buds meanwhile
continue their growth, each forming a primitive streak, which is a sub-
continue their growth, each forming a primitive streak, which is a substitution for the embryonic shield as described for other mammals.
stitution for the embryonic shield as described for other mammals.
The further development of the embryos and the subsequent changes
The further development of the embryos and the subsequent changes
which lead to the production of the four foetuses need not be traced
which lead to the production of the four foetuses need not be traced
Line 14,691: Line 13,547:
following. The relations which are necessary for the understanding of
following. The relations which are necessary for the understanding of


FIG. 224. A, The uterus and entire blastocyst of the armadillo showing paired origin
fiG. 224. A, The uterus and entire blastocyst of the armadillo showing paired origin
01' embryos. B, Half-grown foetuses spread out from uterus wall. (After Patterson.)
01' embryos. B, Half-grown foetuses spread out from uterus wall. (After Patterson.)


Line 14,711: Line 13,567:
development.
development.


Among the trematodes the egg of Fasciola hepatica, the sheep fluke,
Among the trematodes the egg of Fasciola hepatica, the sheep fluke,
is fertilized in the body of the adult fluke, makes its way down the bile
is fertilized in the body of the adult fluke, makes its way down the bile
duct and out of the intestine of the sheep and hatches when it rains
duct and out of the intestine of the sheep and hatches when it rains
as a tiny ciliated larva, a miricidium. Entering the intermediate host,
as a tiny ciliated larva, a miricidium. Entering the intermediate host,
the snail, the miricidium becomes a sporocyst and within it partheno-
the snail, the miricidium becomes a sporocyst and within it parthenogenetic ova appear which develop into rediae, the next larval form.
genetic ova appear which develop into rediae, the next larval form.
Within the body of the rediae the process may be repeated but at length
Within the body of the rediae the process may be repeated but at length
cercariae are developed which escape from the snail and bring about
cercariae are developed which escape from the snail and bring about
the reinfestation of the adult host. This case has been called poly-
the reinfestation of the adult host. This case has been called polyembryony by some, but by others it is regarded as paedogenesis, for
embryony by some, but by others it is regarded as paedogenesis, for
here the new larvae are said to be produced not asexually but from
here the new larvae are said to be produced not asexually but from
parthenogenetic ova, a difierence in method which, if true, would
parthenogenetic ova, a difierence in method which, if true, would
seem to be fundamental. However, the reservation must be made that
seem to be fundamental. However, the reservation must be made that
if the germ masses from which the new larvae arise are not ova, but are
if the germ masses from which the new larvae arise are not ova, but are
produced asexually (as F. G. Brooks believes, having found no matura-
produced asexually (as F. G. Brooks believes, having found no maturation phenomena or other egg—like behavior), then we have to do here
tion phenomena or other egg—like behavior), then we have to do here
merely with asexual reproduction, and not even paedogenesis,
merely with asexual reproduction, and not even paedogenesis,


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Salpa it has long been known that two forms of individuals are to be
Salpa it has long been known that two forms of individuals are to be
expected, one a solitary form and the other a colony which is usually
expected, one a solitary form and the other a colony which is usually
found as a chain of individuals. The first of these develops asexually,
found as a chain of individuals. The first of these develops asexually,
although produced from a fertilized egg. The second is known to be
although produced from a fertilized egg. The second is known to be
budded ofi’ from a stolon which grows out from the asexual individual,
budded ofi’ from a stolon which grows out from the asexual individual,
and among the colonial forms some at least are sexual, producing the
and among the colonial forms some at least are sexual, producing the
eggs and sperm which in their turn start the cycle over again. The genus
eggs and sperm which in their turn start the cycle over again. The genus
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In Doliolum an oozoid is developed from the fertilized egg and it
In Doliolum an oozoid is developed from the fertilized egg and it
reproduces asexually. By some it is regarded as a larval zooid, and
reproduces asexually. By some it is regarded as a larval zooid, and
certainly it has not yet reached its final character. If it is correct to
certainly it has not yet reached its final character. If it is correct to
EXAMPLES OF DOUBTFUL POLYE-MBRYON Y 367
EXAMPLES OF DOUBTFUL POLYE-MBRYON Y 367


regard the oozoid as a larval form, this case is very closely akin to
regard the oozoid as a larval form, this case is very closely akin to
polyembryony. From the ventral posterior part of the oozoid a pro-
polyembryony. From the ventral posterior part of the oozoid a proliferating stolon is formed as a protrusion of the ectoderm into which
liferating stolon is formed as a protrusion of the ectoderm into which
the mesoderm penetrates. From the stolon buds arise which break loose
the mesoderm penetrates. From the stolon buds arise which break loose
in a very immature condition and Worm their way upward and dorsally
in a very immature condition and Worm their way upward and dorsally
Line 14,762: Line 13,614:
trophozooids or gasterozooids and their only function is to nourish the
trophozooids or gasterozooids and their only function is to nourish the
colony. The dorsal row of buds undergoes metamorphosis into several
colony. The dorsal row of buds undergoes metamorphosis into several
kinds of zooids. Some become phorozooids or nurse zooids, and accord-
kinds of zooids. Some become phorozooids or nurse zooids, and according to some investigators they produce from a ventral stalk buds which
ing to some investigators they produce from a ventral stalk buds which
are protogonozooids or primary sex buds. These latter either by budding
are protogonozooids or primary sex buds. These latter either by budding
or fission produce the sexual animals, the gonozooids or blastozooids, in
or fission produce the sexual animals, the gonozooids or blastozooids, in
which with further development sex organs are formed and the cycle is
which with further development sex organs are formed and the cycle is
completed. Here an alternation of generations occurs in which there are
completed. Here an alternation of generations occurs in which there are
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A problem which has run through the entire history of embryology
A problem which has run through the entire history of embryology
and is yet a live question at the present time concerns the extent to
and is yet a live question at the present time concerns the extent to
which the egg represents a fixed and definite system whose course is
which the egg represents a fixed and definite system whose course is
set when its development has begun. This is the determination problem.
set when its development has begun. This is the determination problem.
It first became a live issue during the controversy between the preforma-
It first became a live issue during the controversy between the preformationists and the epigenesists of the seventeenth and eighteenth centuries
tionists and the epigenesists of the seventeenth and eighteenth centuries
and was even in that crude form an attempt to solve the question of the
and was even in that crude form an attempt to solve the question of the
organization of the egg. The one school held that development was
organization of the egg. The one school held that development was
Line 14,799: Line 13,649:
the literature is voluminous. It is not even possible to summarize in a
the literature is voluminous. It is not even possible to summarize in a
short discussion the work which has been done. All that can be attempted
short discussion the work which has been done. All that can be attempted
is to bring together briefly the lines of work which have been responsible
is to bring together briefly the lines of work which have been responsible
for the present conceptions in regard to determination.
for the present conceptions in regard to determination.


Two sets of facts confront the student who would consider the de-
Two sets of facts confront the student who would consider the determination problem. Neither bears directly upon the question at issue,
termination problem. Neither bears directly upon the question at issue,
but both serve to limit it. In the first place an egg goes through certain
but both serve to limit it. In the first place an egg goes through certain
steps with surprising uniformity and produces an individual which is
steps with surprising uniformity and produces an individual which is
structurally very complex and very much differentiated. It is organized
structurally very complex and very much differentiated. It is organized
Line 14,810: Line 13,659:
has shown that the egg to begin with possesses in the mechanism by
has shown that the egg to begin with possesses in the mechanism by
which the genes are controlled and distributed a type of organization
which the genes are controlled and distributed a type of organization
likewise complex in the extreme; and there is no doubt that this mechan-
likewise complex in the extreme; and there is no doubt that this mechanism operates to produce the conditions found in later ontogeny. Yet
ism operates to produce the conditions found in later ontogeny. Yet
differentiation is a matter of the cytoplasm of the cells. The repeated
differentiation is a matter of the cytoplasm of the cells. The repeated


Line 14,836: Line 13,684:
last century.
last century.


These two questions are really two aspects of the problem of organiza-
These two questions are really two aspects of the problem of organization, for differentiation is the manifestation of the operative mechanism
tion, for differentiation is the manifestation of the operative mechanism
of the egg as modified by extrinsic factors. To discover the extreme to
of the egg as modified by extrinsic factors. To discover the extreme to
which this operative mechanism is already present in the early stages
which this operative mechanism is already present in the early stages
and to which it gives a definite “set” to the differentiating embryo is
and to which it gives a definite “set” to the differentiating embryo is
the aim of the work on determination. If differentiations become visible
the aim of the work on determination. If differentiations become visible
early and are little modified by extrinsic factors with the result that
early and are little modified by extrinsic factors with the result that
the course of development is orderly in a high degree, we say that the
the course of development is orderly in a high degree, we say that the
egg is strongly determinative. But if the egg retains its embryonic
egg is strongly determinative. But if the egg retains its embryonic
plasticity and easily adapts itself to environmental disturbances, that
plasticity and easily adapts itself to environmental disturbances, that
is, is easily modified by extrinsic factors, it is said to be indeterminative
is, is easily modified by extrinsic factors, it is said to be indeterminative
or of the regulatory type. If differentiations manifest themselves early,
or of the regulatory type. If differentiations manifest themselves early,
little regulatory capacity is retained by the egg. In other words, the
little regulatory capacity is retained by the egg. In other words, the
Line 14,852: Line 13,699:
progress of differentiation.
progress of differentiation.


It must be borne in mind also in considering the problem of differenti-
It must be borne in mind also in considering the problem of differentiation (and hence of determination) that the chemico-physical organization of the cell limits the conclusions which may be reached. Differentiation manifests itself through colloidal materials. The chemistry of the
ation (and hence of determination) that the chemico-physical organiza-
tion of the cell limits the conclusions which may be reached. Differentia-
tion manifests itself through colloidal materials. The chemistry of the
protoplasmic system is so imperfectly known that whatever conclusions
protoplasmic system is so imperfectly known that whatever conclusions
are reached regarding these problems must be subject to revision when
are reached regarding these problems must be subject to revision when
Line 14,865: Line 13,709:
Conklin and of others that the position and size of the spindle are
Conklin and of others that the position and size of the spindle are
matters of great importance in differentiation. Yet the physico-chemical
matters of great importance in differentiation. Yet the physico-chemical
factors which are involved in spindle behavior have not yet been ade-
factors which are involved in spindle behavior have not yet been adequately analyzed. Other problems of physico-chemical nature similarly
quately analyzed. Other problems of physico-chemical nature similarly
affect our"conclusions. It is not too much to say that in spite of the vast
affect our"conclusions. It is not too much to say that in spite of the vast
amount of embryological research differentiation and its mechanism is
amount of embryological research differentiation and its mechanism is
one of the least understood fields of biology.
one of the least understood fields of biology.


It has been pointed out that the function of cleavage is to sort out
It has been pointed out that the function of cleavage is to sort out
Line 14,879: Line 13,722:
other. It does not follow, however, that this sorting-out process of
other. It does not follow, however, that this sorting-out process of
cleavage is the cause of the subsequent development. Rather there must
cleavage is the cause of the subsequent development. Rather there must
be a fundamental underlying mechanism of organization, the mani-
be a fundamental underlying mechanism of organization, the manifestations of which are the cleavage phenomena. Primarily determination
festations of which are the cleavage phenomena. Primarily determination
concerns itself with the manifestations of these underlying methods of
concerns itself with the manifestations of these underlying methods of
organization. It seeks for evidence of pre—1ocalization of areas or sub-
organization. It seeks for evidence of pre—1ocalization of areas or substances within the egg or even of an early promorphology which gives
stances within the egg or even of an early promorphology which gives
visible expression to the underlying mechanism. Some of the questions
visible expression to the underlying mechanism. Some of the questions
involved may perhaps be formulated in the following manner: Are there
involved may perhaps be formulated in the following manner: Are there
Line 14,889: Line 13,730:
at the very beginning of development and which are independent of
at the very beginning of development and which are independent of
each other and of other parts of the egg? If so, how are they formed?
each other and of other parts of the egg? If so, how are they formed?
Must all appear at the same time, or may some appear later on? Con-
Must all appear at the same time, or may some appear later on? Conversely, are the definite structures of the embryo never independent of
versely, are the definite structures of the embryo never independent of
each other? Are the parts always influenced by the whole of which they
each other? Are the parts always influenced by the whole of which they
are constituents? Or finally, are there some eggs which are determinative
are constituents? Or finally, are there some eggs which are determinative
in their character and others which are not, or are some parts of the
in their character and others which are not, or are some parts of the
individual embryo determinative and other parts not? Perhaps all these
individual embryo determinative and other parts not? Perhaps all these
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CLASSICAL THEORIES OF THE NATURE OF DEVELOPMENT 371
CLASSICAL THEORIES OF THE NATURE OF DEVELOPMENT 371


Wilhelm His (1874). This is the doctrine that definitely localized areas
Wilhelm His (1874). This is the doctrine that definitely localized areas
perhaps even in the unsegmented egg are the forerunners of the'organs
perhaps even in the unsegmented egg are the forerunners of the'organs
and parts of the embryo, that “the germinal disc [of the chick] contains
and parts of the embryo, that “the germinal disc [of the chick] contains
the preformed germs of the organs spread out over a flat surface, and
the preformed germs of the organs spread out over a flat surface, and
conversely . . . every point of the germinal disc is found again in a
conversely . . . every point of the germinal disc is found again in a
later organ.” Ray Lankester supported His in his views, saying that
later organ.” Ray Lankester supported His in his views, saying that
it was quite possible for the cell to “contain already formed and indi-
it was quite possible for the cell to “contain already formed and individualized, various kinds of physiological molecules. The visible process
vidualized, various kinds of physiological molecules. The visible process
of segregation is only the sequel of a differentiation already established
of segregation is only the sequel of a differentiation already established
and not visible.” Whitman as a result of his work on Clepsine concluded
and not visible.” Whitman as a result of his work on Clepsine concluded
Line 14,935: Line 13,774:
within the egg rather than the areas which they occupy receive the
within the egg rather than the areas which they occupy receive the
chief attention. Here again it is obvious that not all materials within
chief attention. Here again it is obvious that not all materials within
the egg, even though they be definitely localized, are formative. Yolk,
the egg, even though they be definitely localized, are formative. Yolk,
pigment, oil globules, and other inclusions in the cytoplasm are definitely
pigment, oil globules, and other inclusions in the cytoplasm are definitely
located in many eggs, yet clearly are not formative. In some instances
located in many eggs, yet clearly are not formative. In some instances
visibly differentiated substances within the unsegmented egg have been
visibly differentiated substances within the unsegmented egg have been
shown to have no formative function. At least they have been displaced
shown to have no formative function. At least they have been displaced
by pressure or by centrifugal force, and normal embryos have neverthe-
by pressure or by centrifugal force, and normal embryos have nevertheless resulted. Yet in other forms the materials of the egg have been
less resulted. Yet in other forms the materials of the egg have been
traced in a precise manner to the organs of the embryo. Surely a principle
traced in a precise manner to the organs of the embryo. Surely a principle
of determination is here involved which is too important to deny be-
of determination is here involved which is too important to deny because of a particular formulation of a doctrine. Perhaps the importance
cause of a particular formulation of a doctrine. Perhaps the importance
of the visible organ-forming substances has been overemphasized and
of the visible organ-forming substances has been overemphasized and
these are but manifestations of a more fundamental mechanism. Yet
these are but manifestations of a more fundamental mechanism. Yet
in very many eggs the mechanism undoubtedly exists, and later re-
in very many eggs the mechanism undoubtedly exists, and later researches have certainly demonstrated the essential correctness of the
searches have certainly demonstrated the essential correctness of the
principle involved in the conception that the egg is not without an
principle involved in the conception that the egg is not without an
organization before cleavage begins which conditions the future course
organization before cleavage begins which conditions the future course
Line 14,956: Line 13,792:
As a result of the early work on cell lineage by Whitman, Rabl, van
As a result of the early work on cell lineage by Whitman, Rabl, van
Beneden and others the former view that blastomeres were indifferent
Beneden and others the former view that blastomeres were indifferent
both in position and significance was gradually replaced by another
both in position and significance was gradually replaced by another
to the effect that the cleavage pattern was in the nature of a mosaic,
to the effect that the cleavage pattern was in the nature of a mosaic,
and that a blastomere occupied its particular place because of the
and that a blastomere occupied its particular place because of the
Line 14,968: Line 13,804:
certainly expresses one of the underlying truths of embryology. One
certainly expresses one of the underlying truths of embryology. One
may, however, raise the question of the manner and the time of origin
may, however, raise the question of the manner and the time of origin
of the mosaic work and also whether it is so fixed that it is not subject
of the mosaic work and also whether it is so fixed that it is not subject
to the regulatory processes of which the organism is capable.
to the regulatory processes of which the organism is capable.


The question of regulation brings up yet another theory of historical
The question of regulation brings up yet another theory of historical
significance which We owe to Driesch. His terms prospective significance,
significance which We owe to Driesch. His terms prospective significance,
prospective potency, his equipotential system, are all well known to
prospective potency, his equipotential system, are all well known to
those who are familiar with the history of the determination problem.
those who are familiar with the history of the determination problem.
By prospective significance of a cell he meant the actual destiny in the
By prospective significance of a cell he meant the actual destiny in the
developmental process. By prospective potency he meant the possible
developmental process. By prospective potency he meant the possible
fate which the cell might attain. Prospective potency includes the sum
fate which the cell might attain. Prospective potency includes the sum
Line 14,984: Line 13,820:
material and might be interchanged like balls in a pile without affecting
material and might be interchanged like balls in a pile without affecting
the result in the development of the embryo; in other words that the
the result in the development of the embryo; in other words that the
fate, the prospective significance, of a particular blastomere is a “func-
fate, the prospective significance, of a particular blastomere is a “function of its position.” Driesch’s theory was in opposition to the mosaic
tion of its position.” Driesch’s theory was in opposition to the mosaic
theory of development according to which the fate of the blastomeres
theory of development according to which the fate of the blastomeres
did not depend upon their position alone but upon their organization.
did not depend upon their position alone but upon their organization.
It was based upon the conception current at the time when work on
It was based upon the conception current at the time when work on
cell lineage first rose to an important place. Pfliiger had held that the
cell lineage first rose to an important place. Pfliiger had held that the
egg and its blastomeres were homogeneous throughout and that cleavage
egg and its blastomeres were homogeneous throughout and that cleavage
simply multiplied the units out of which diiferentiations were later to
simply multiplied the units out of which diiferentiations were later to
arise. This view was also favored by Oscar Hertwig. Driesch, who
arise. This view was also favored by Oscar Hertwig. Driesch, who
although chiefly interested in philosophy, set himself to carry out
although chiefly interested in philosophy, set himself to carry out
experiments in development upon which certain philosophical de-
experiments in development upon which certain philosophical decisions might be based, made this conception the starting point of his
cisions might be based, made this conception the starting point of his
theory of development.
theory of development.


Line 15,003: Line 13,837:
extent the theory of Driesch may be based, while there is also evidence
extent the theory of Driesch may be based, while there is also evidence
upon which the mosaic conception may rest. On the one hand certain
upon which the mosaic conception may rest. On the one hand certain
eggs possess a high degree of regulatory capacity and are hence in-
eggs possess a high degree of regulatory capacity and are hence indeterminative in their cleavage. On the other hand certain other eggs
determinative in their cleavage. On the other hand certain other eggs
show the marks of differentiation appearing at a very early stage in the
show the marks of differentiation appearing at a very early stage in the


Line 15,042: Line 13,875:
within the germ cells. Although we do not by any means identify these
within the germ cells. Although we do not by any means identify these
units with visible structures in the egg cell nor do we know how they
units with visible structures in the egg cell nor do we know how they
express their influence upon the developing organism, yet any theory
express their influence upon the developing organism, yet any theory
of particulate inheritance (that is inheritance based upon the presence
of particulate inheritance (that is inheritance based upon the presence
of organized particles within the germ cell) is, in so far as it is justified,
of organized particles within the germ cell) is, in so far as it is justified,
evidence in favor of a morphological basis of determinate development.
evidence in favor of a morphological basis of determinate development.
This evidence bears out the conclusion stated above that, although
This evidence bears out the conclusion stated above that, although
Line 15,052: Line 13,885:
are none which are purely regulatory.
are none which are purely regulatory.


The first signs of differentiation in the developing egg have to do with
The first signs of differentiation in the developing egg have to do with
the general features of polarity, symmetry, and pattern of the egg.
the general features of polarity, symmetry, and pattern of the egg.
From these’ general features more detailed diiferentiations with respect
From these’ general features more detailed diiferentiations with respect
Line 15,058: Line 13,891:
and parts of the embryo arise and later the differentiations of tissues
and parts of the embryo arise and later the differentiations of tissues
and the beginning of organs. Development is thus progressive, and
and the beginning of organs. Development is thus progressive, and
differentiation, at first relating only to the most general features, gradu-
differentiation, at first relating only to the most general features, gradually passes to specialized details. Since polarity, symmetry, and cleavage
ally passes to specialized details. Since polarity, symmetry, and cleavage
pattern are general in character their importance is sometimes overlocked by the student, yet very little thought is required to convince
pattern are general in character their importance is sometimes over-
locked by the student, yet very little thought is required to convince
one that they are really basic. Our morphological knowledge with regard
one that they are really basic. Our morphological knowledge with regard
to the development of polarity and symmetry has been discussed in the
to the development of polarity and symmetry has been discussed in the
Line 15,067: Line 13,898:
reference should be made to those chapters. These observations have
reference should be made to those chapters. These observations have
been checked by many experiments of the greatest importance and it
been checked by many experiments of the greatest importance and it
will perhaps suflice to refer to these experiments under the second line
will perhaps suflice to refer to these experiments under the second line
of evidence as listed here.
of evidence as listed here.


Line 15,074: Line 13,905:
in the studies at the hands of the students of cell lineage. It early became
in the studies at the hands of the students of cell lineage. It early became
clear that certain types of cleavage were predominately determinative.
clear that certain types of cleavage were predominately determinative.
Some eggs with bilateral cleavage, certain types of eggs with superficial
Some eggs with bilateral cleavage, certain types of eggs with superficial
cleavage, those with spiral cleavage, with disymmetrical, and even an
cleavage, those with spiral cleavage, with disymmetrical, and even an
occasional form having radial cleavage, such as Strongylocentrotus, were
occasional form having radial cleavage, such as Strongylocentrotus, were
Line 15,085: Line 13,916:
2. Experimental Evidence
2. Experimental Evidence


The second line of evidence which bears upon the problem of deter-
The second line of evidence which bears upon the problem of determination is perhaps no more important than the morphological evidence
mination is perhaps no more important than the morphological evidence
but is certainly not less so and is much more recent. It is obtained from
but is certainly not less so and is much more recent. It is obtained from
those special experiments* which have to do with this problem.
those special experiments* which have to do with this problem.
Line 15,098: Line 13,928:
EXPERIMENTAL EVIDENCE 375
EXPERIMENTAL EVIDENCE 375


The first series of experiments of significance for study of determina-
The first series of experiments of significance for study of determination is concerned with the localization of the median plama. Here as with
tion is concerned with the localization of the median plama. Here as with
the other experiments to be summarized the student is referred to
the other experiments to be summarized the student is referred to
Morgan’s critical discussion as well as to the original papers which
Morgan’s critical discussion as well as to the original papers which
describe them. It would be impossible in a work of this size to give
describe them. It would be impossible in a work of this size to give
even a brief account of the experiments themselves. Reference can only
even a brief account of the experiments themselves. Reference can only
be made to those which seem most significant.
be made to those which seem most significant.


The matter of the localization of the median plane is of importance
The matter of the localization of the median plane is of importance
Line 15,110: Line 13,939:
on the part of the egg. According to some the polarity of the egg may
on the part of the egg. According to some the polarity of the egg may
be traced back even into an ovarian condition, and some believe that
be traced back even into an ovarian condition, and some believe that
the type of symmetry is determined in the egg cytoplasm before ferti-
the type of symmetry is determined in the egg cytoplasm before fertilization. Although the evidence of these relationships seems good in
lization. Although the evidence of these relationships seems good in
some cases it has not been made clear how much the appearance of
some cases it has not been made clear how much the appearance of
symmetry_in these early stages is related to the cleavage plane or the
symmetry_in these early stages is related to the cleavage plane or the
Line 15,117: Line 13,945:


Experimental embryology has seemed to cover a wide range of topics and the results
Experimental embryology has seemed to cover a wide range of topics and the results
of the investigations in this field are scattered throughout many journals. There
of the investigations in this field are scattered throughout many journals. There
have been but few attempts to bring this material into the scope of a single volume.
have been but few attempts to bring this material into the scope of a single volume.
The first section of Korschelt and Heider’s “Lehrbuch der vergleichenden Entwick-
The first section of Korschelt and Heider’s “Lehrbuch der vergleichenden Entwicklungsgeschichte der wirbcllosen Thiere” deals with the experimental results obtained
lungsgeschichte der wirbcllosen Thiere” deals with the experimental results obtained
up to that time (1902). In 1909 Jenkinson published his book entitled “Experimental Embryology” and summarized much of the work available at that time.
up to that time (1902). In 1909 Jenkinson published his book entitled “Experi-
mental Embryology” and summarized much of the work available at that time.
The contribution to experimental embryology most important now, however, is the
The contribution to experimental embryology most important now, however, is the
volume by Morgan entitled “Experimental Embryology” and published in 1927.
volume by Morgan entitled “Experimental Embryology” and published in 1927.
Morgan has promised a further volume which will deal with such topics as growth,
Morgan has promised a further volume which will deal with such topics as growth,
reflex reactions, tropisms of the larvae, the influence of environment upon the embryos,
reflex reactions, tropisms of the larvae, the influence of environment upon the embryos,
the source of energy of development, etc. It is to be hoped that this volume will
the source of energy of development, etc. It is to be hoped that this volume will
appear at no distant date.
appear at no distant date.


In spite of the diversity of topics which have engaged the attention of experi-
In spite of the diversity of topics which have engaged the attention of experimental embryologists it is possible to classify them into a few divisions. (1) The early
mental embryologists it is possible to classify them into a few divisions. (1) The early
students of this field were specially interested in the discovery of the effect that
students of this field were specially interested in the discovery of the effect that
external factors have upon the developing embryo. Among these factors are gravitation, mechanical agitation, electricity, light, heat, atmospheric pressure, osmotic
external factors have upon the developing embryo. Among these factors are gravi-
tation, mechanical agitation, electricity, light, heat, atmospheric pressure, osmotic
pressure, and the chemical composition of. the medium in which development takes
pressure, and the chemical composition of. the medium in which development takes
place. (2) In addition to this the growth problem, the problems centering around
place. (2) In addition to this the growth problem, the problems centering around
fertilization, have occupied much attention during the present century. Something
fertilization, have occupied much attention during the present century. Something
of the nature of these problems is suggested in the section of this book which has
of the nature of these problems is suggested in the section of this book which has
to do with artificial parthenogenesis, although this is but one of the many topics
to do with artificial parthenogenesis, although this is but one of the many topics
that have been studied. (3) Finally a great deal of attention has been given by
that have been studied. (3) finally a great deal of attention has been given by
experimental embryologists to those problems which are concerned with the forrna—
experimental embryologists to those problems which are concerned with the forrna—
tive changes of the egg. These factors are internal in their nature and seem to take
tive changes of the egg. These factors are internal in their nature and seem to take
Line 15,146: Line 13,970:
of the organism than do the other problems enumerated. The experiments which
of the organism than do the other problems enumerated. The experiments which
bear on the problem of determination come under this head. Those experiments
bear on the problem of determination come under this head. Those experiments
which have sought light on this problem fall chiefly within a few animal groups,
which have sought light on this problem fall chiefly within a few animal groups,
namely: the ctenophores, some hydromedusae, the nematodes, annelids and molluscs,
namely: the ctenophores, some hydromedusae, the nematodes, annelids and molluscs,
echinodcrms, ascidians. It may be remarked that not only are these the forms which
echinodcrms, ascidians. It may be remarked that not only are these the forms which
Line 15,156: Line 13,980:
first cleavage plane and the planes of symmetry of the later embryo
first cleavage plane and the planes of symmetry of the later embryo
have been made out it is thought that the point of entrance of the
have been made out it is thought that the point of entrance of the
spermatozoon and the path traveled by the sperm pronucleus in ap-
spermatozoon and the path traveled by the sperm pronucleus in approaching the egg pronucleus determine the position of the plane.
proaching the egg pronucleus determine the position of the plane.
Suggestions have also been made that the pressure of the enveloping
Suggestions have also been made that the pressure of the enveloping
membrane of the egg or pressure from the oviduct or other external
membrane of the egg or pressure from the oviduct or other external
Line 15,164: Line 13,987:
however, that so long as the possibility remains of a relationship for
however, that so long as the possibility remains of a relationship for
example at the point of entrance of the spermatozoon it is necessary
example at the point of entrance of the spermatozoon it is necessary
to assume that the symmetry of the embryo goes back to a predeter-
to assume that the symmetry of the embryo goes back to a predetermined symmetry of the egg.
mined symmetry of the egg.


The question of a relationship of the median plane and the first
The question of a relationship of the median plane and the first
cleavage plane arises in the history of embryology in relation to the
cleavage plane arises in the history of embryology in relation to the
frog egg. As long ago as 1851 Newport had reported that the two co-
frog egg. As long ago as 1851 Newport had reported that the two coincide, and from that time the question has been often discussed. In
incide, and from that time the question has been often discussed. In
the frog egg at the time of cleavage there is already present a bilaterality
the frog egg at the time of cleavage there is already present a bilaterality
as shown by the presence of the gray crescent. The real question involved
as shown by the presence of the gray crescent. The real question involved
in determining the symmetry relationships is: what in the uncleaved
in determining the symmetry relationships is: what in the uncleaved
egg causes the material to take the position of the gray crescent, and
egg causes the material to take the position of the gray crescent, and
why does the first cleavage plane cut through the middle of it? Experi-
why does the first cleavage plane cut through the middle of it? Experiments have shown that its position is determined after fertilization and
ments have shown that its position is determined after fertilization and
that any meridian of the unfertilized egg may become the median plane.
that any meridian of the unfertilized egg may become the median plane.
After fertilization the meridians are not equivalent in this respect,
After fertilization the meridians are not equivalent in this respect,
however, for usually the crescent forms opposite the point of entrance
however, for usually the crescent forms opposite the point of entrance
of the sperm. A long series of experiments can be cited to show that in
of the sperm. A long series of experiments can be cited to show that in
nearly two-thirds of the cases the first cleavage plane does coincide
nearly two-thirds of the cases the first cleavage plane does coincide
with the middle of the gray crescent. It is clear, however, that if 30 per
with the middle of the gray crescent. It is clear, however, that if 30 per
cent or more of the eggs fail to show this relationship the mechanism of
cent or more of the eggs fail to show this relationship the mechanism of
determination is by no means a fixed one. In other amphibia the experi-
determination is by no means a fixed one. In other amphibia the experiments of Jordan indicate that the first cleavage plane is at right angles
ments of Jordan indicate that the first cleavage plane is at right angles
to the axis of the egg of Diemyctylus, and Spemann has found for Triton
to the axis of the egg of Diemyctylus, and Spemann has found for Triton
that the second cleavage plane coincides with the median plane of the
that the second cleavage plane coincides with the median plane of the
embryo. Of course it is immaterial from the standpoint of determination
embryo. Of course it is immaterial from the standpoint of determination
as to whether it is the first or second plane which shows the relationship.
as to whether it is the first or second plane which shows the relationship.
In the teleost fishes according to the work of Morgan and of Clapp no
In the teleost fishes according to the work of Morgan and of Clapp no
definite relation between the second plane and the median plane of the
definite relation between the second plane and the median plane of the
body can be made out. For the sea-urchin a considerable amount of
body can be made out. For the sea-urchin a considerable amount of
evidence is available. In Toxopneustes, Wilson and Mathews related the
evidence is available. In Toxopneustes, Wilson and Mathews related the
appearance of the first cleavage plane to the entrance of the sperma-
appearance of the first cleavage plane to the entrance of the spermatozoon, and Boveri held that it coincided with the median plane of the
tozoon, and Boveri held that it coincided with the median plane of the
EXPERIMENTAL EVIDENCE 377
EXPERIMENTAL EVIDENCE 377


embryo. In the eggs of Echinus, Driesch found the second plane to
embryo. In the eggs of Echinus, Driesch found the second plane to
correspond to the median plane and Runnstrém assumed that the first
correspond to the median plane and Runnstrém assumed that the first
cleavage coincides with the median plane. Recently Von Ubisch has
cleavage coincides with the median plane. Recently Von Ubisch has
performed a very ingenious experiment by which certain portions of
performed a very ingenious experiment by which certain portions of
the egg were stained with intra vitam stains; in three species of sea-
the egg were stained with intra vitam stains; in three species of seaurchins he obtained results which are in agreement. He was able to
urchins he obtained results which are in agreement. He was able to
demonstrate no fixed relation between the planes of symmetry and
demonstrate no fixed relation between the planes of symmetry and
planes of cleavage, but found some evidence that the first cleavage
planes of cleavage, but found some evidence that the first cleavage
plane more nearly coincides with the median plane. On the whole for
plane more nearly coincides with the median plane. On the whole for
the sea-urchins perhaps this is the most acceptable conclusion. In his
the sea-urchins perhaps this is the most acceptable conclusion. In his
study of ascidian embryology Conklin determined that the first cleavage
study of ascidian embryology Conklin determined that the first cleavage
plane is the median plane of the embryo, and that in Cynthia its position
plane is the median plane of the embryo, and that in Cynthia its position
is indicated before the pronuclei meet. In the nematodes, according to
is indicated before the pronuclei meet. In the nematodes, according to
Line 15,214: Line 14,031:
the median plane of the embryo. In Nereis, Just has found that the
the median plane of the embryo. In Nereis, Just has found that the
second cleavage plane usually corresponds to the median plane of the
second cleavage plane usually corresponds to the median plane of the
embryo but the first cleavage plane is determined by the position of
embryo but the first cleavage plane is determined by the position of
the entering spermatozoon. Insect eggs are distinctly bilateral so far as
the entering spermatozoon. Insect eggs are distinctly bilateral so far as
their orientation is concerned, the position of the egg as laid correspond-
their orientation is concerned, the position of the egg as laid corresponding to the symmetry of the mother’s body and definitely indicating the
ing to the symmetry of the mother’s body and definitely indicating the
position of the embryo in the egg. For the chick and pigeon Bartelmez
position of the embryo in the egg. For the chick and pigeon Bartelmez
has held that bilaterality is present even in the small ovarian eggs.
has held that bilaterality is present even in the small ovarian eggs.
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A second series of experiments related to the problem of determination
A second series of experiments related to the problem of determination
has sought to discover to what extent localization of germinal areas is
has sought to discover to what extent localization of germinal areas is
present before cleavage, using as a method the development of egg frag-
present before cleavage, using as a method the development of egg fragments. Eggs of Cerebratulus were out along definite planes by Wilson,
ments. Eggs of Cerebratulus were out along definite planes by Wilson,
Zeleny, and Yatsu. Cuts were made both before and after fertilization
Zeleny, and Yatsu. Cuts were made both before and after fertilization
and development followed without difficulty. The cleavage of the frag-
and development followed without difficulty. The cleavage of the fragments in general corresponded to the type of cleavage of the whole egg
ments in general corresponded to the type of cleavage of the whole egg
but upon a much reduced scale. It was not found to make a difference
but upon a much reduced scale. It was not found to make a difference
from which part of the egg the fragment was taken. The experiments
from which part of the egg the fragment was taken. The experiments
show that either factors which determined cleavage were not yet
show that either factors which determined cleavage were not yet
definitely localized at the time of maturation or the egg is capable of
definitely localized at the time of maturation or the egg is capable of
very extensive regulation. According to Yatsu if the operation occurred
very extensive regulation. According to Yatsu if the operation occurred
between the formation of the first and second polar bodies the cleavage
between the formation of the first and second polar bodies the cleavage
was entirely regular but if it was after the second division irregularities
was entirely regular but if it was after the second division irregularities
developed in some of the cases. Wilson experimented with fragments
developed in some of the cases. Wilson experimented with fragments
Line 15,244: Line 14,058:
into fragments in the unsegmented condition produces in some cases
into fragments in the unsegmented condition produces in some cases
partial embryos and in others whole ones depending on whether the cut
partial embryos and in others whole ones depending on whether the cut
is symmetrical or oblique. Driesch, Morgan, Yatsu, and Fischel have
is symmetrical or oblique. Driesch, Morgan, Yatsu, and fischel have
experimented with this form. With sea-urchin eggs conflicting results
experimented with this form. With sea-urchin eggs conflicting results
have been obtained from experiments with the development of frag-
have been obtained from experiments with the development of fragments. Taylor and Tennant using accurate methods of cutting with a
ments. Taylor and Tennant using accurate methods of cutting with a
micro-dissecting machine obtained small pluteae from the developing
micro-dissecting machine obtained small pluteae from the developing
fragments which were like the normal ones. But Harnley obtained
fragments which were like the normal ones. But Harnley obtained
evidence that the materials of the egg were qualitatively different.
evidence that the materials of the egg were qualitatively different.
Finally experiments on the development of parts of Triton eggs have
finally experiments on the development of parts of Triton eggs have
been performed by Spemann and Baltzer. Non-nucleated fragments,
been performed by Spemann and Baltzer. Non-nucleated fragments,
obtained by separating the egg by means of a hair tied around it, de-
obtained by separating the egg by means of a hair tied around it, developed but rarely and the nucleated fragments produced dwarf larvae
veloped but rarely and the nucleated fragments produced dwarf larvae
which did not live long enough to undergo metamorphosis although
which did not live long enough to undergo metamorphosis although
normal in most particulars.
normal in most particulars.
Line 15,266: Line 14,078:
is accomplished by the entrance of the spermatozoon. The cleavage of
is accomplished by the entrance of the spermatozoon. The cleavage of
egg fragments demonstrates that for many types of eggs the pattern
egg fragments demonstrates that for many types of eggs the pattern
develops along with the mitotic figure.
develops along with the mitotic figure.


Another series of experiments has sought to discover to what extent
Another series of experiments has sought to discover to what extent
it is possible for a whole embryo to develop from an isolated blastomere.
it is possible for a whole embryo to develop from an isolated blastomere.
In some few eggs it is possible to cut the blastomeres apart at the time
In some few eggs it is possible to cut the blastomeres apart at the time
when they are most widely separated from each other as the first cleav-
when they are most widely separated from each other as the first cleavage is closing. In others it has been found possible to separate them by
age is closing. In others it has been found possible to separate them by
shaking them in a tube of water, or by squirting them from a pipette.
shaking them in a tube of water, or by squirting them from a pipette.
Again eggs of echinoderms permit the easy separation of the blastomeres
Again eggs of echinoderms permit the easy separation of the blastomeres
if they are kept in calcium-free sea water while the first cleavage is
if they are kept in calcium-free sea water while the first cleavage is
taking place. Isolation experiments have been performed on sea-urchins,
taking place. Isolation experiments have been performed on sea-urchins,
the hydroid Clytia flavidula, Cerebratulus, amphioxus, teleost fishes,
the hydroid Clytia flavidula, Cerebratulus, amphioxus, teleost fishes,
Triton, and the frog, and in all these cases whole embryos were obtained
Triton, and the frog, and in all these cases whole embryos were obtained
from the isolated blastomere. On the other hand blastomeres of cteno-
from the isolated blastomere. On the other hand blastomeres of ctenophores, molluscs, and ascidians when isolated give rise to half embryos
phores, molluscs, and ascidians when isolated give rise to half embryos
only. It would seem that this emphasizes again the distinction between
only. It would seem that this emphasizes again the distinction between
determinative and regulatory eggs.
determinative and regulatory eggs.
Line 15,295: Line 14,105:
the missing portion of the embryo was restored. This conclusion seems
the missing portion of the embryo was restored. This conclusion seems
doubtful as there is now good evidence that the resulting embryo is more
doubtful as there is now good evidence that the resulting embryo is more
nearly one-half than a whole. Later studies have shown that, in experi-
nearly one-half than a whole. Later studies have shown that, in experiments of this kind, if the plane of the first cleavage goes through the
ments of this kind, if the plane of the first cleavage goes through the
middle of the gray crescent a half embryo results. If the plane is parallel
middle of the gray crescent a half embryo results. If the plane is parallel
to the gray crescent and the injured blastomere is the one which con-
to the gray crescent and the injured blastomere is the one which contains it, nothing recognizable is produced from the opposite one. But
tains it, nothing recognizable is produced from the opposite one. But
if the opposite blastomere is injured the one containing the gray crescent
if the opposite blastomere is injured the one containing the gray crescent
will produce the anterior end of the embryo. Even if the cleavage plane
will produce the anterior end of the embryo. Even if the cleavage plane
Line 15,319: Line 14,127:
partial embryo. In this same connection the experiments of a number
partial embryo. In this same connection the experiments of a number
of investigators, of whom Hegner and Reith are typical, on the effect
of investigators, of whom Hegner and Reith are typical, on the effect
of injury to the eggs of insects should be mentioned. Insect eggs appar-
of injury to the eggs of insects should be mentioned. Insect eggs apparently may be among the most determinative with which we have to deal,
ently may be among the most determinative with which we have to deal,
for these experiments indicate that different cytoplasmic areas on the
for these experiments indicate that different cytoplasmic areas on the
surface of the egg are fixed in their prospective significance even before
surface of the egg are fixed in their prospective significance even before
the cleaving nuclei with their surrounding cytoplasmic islands migrate
the cleaving nuclei with their surrounding cytoplasmic islands migrate
to the surface and they have no great powers of readjustment. There is
to the surface and they have no great powers of readjustment. There is
Line 15,330: Line 14,137:
dependence upon the injured portion, but will produce only that part of
dependence upon the injured portion, but will produce only that part of
the embryo which was to be expected. Reith found that, if the posterior
the embryo which was to be expected. Reith found that, if the posterior
end of the egg of the house fly is injured, the parts normally resulting
end of the egg of the house fly is injured, the parts normally resulting
from the anterior end will develop. If the anterior end is the location of
from the anterior end will develop. If the anterior end is the location of
the injury, a larva without a head end develops, and in some cases in-
the injury, a larva without a head end develops, and in some cases injury to the middle portion of the egg was not so severe but that both
jury to the middle portion of the egg was not so severe but that both
anterior and posterior organs developed.
anterior and posterior organs developed.


Hegner’s experiments on the eggs of the chrysomelid beetles Calli-
Hegner’s experiments on the eggs of the chrysomelid beetles Calligrapha multipunctata and Leptinotarsa decemlineata are Well known.
grapha multipunctata and Leptinotarsa decemlineata are Well known.
Here the posterior end of the egg is the location of the pole plasm which
Here the posterior end of the egg is the location of the pole plasm which
Hegner found to pass into the germ cells in development. By injuring
Hegner found to pass into the germ cells in development. By injuring
this region with a hot needle he was able to secure embryos without
this region with a hot needle he was able to secure embryos without
germ cells. Evidently the cytoplasmic regions in the eggs of these insects
germ cells. Evidently the cytoplasmic regions in the eggs of these insects
are very early set aside to produce definite parts of the embryo. Yet it
are very early set aside to produce definite parts of the embryo. Yet it
must not be inferred that the regions in question retain no powers of
must not be inferred that the regions in question retain no powers of
adjustment. As cleavage progresses the possibilities of readjustment
adjustment. As cleavage progresses the possibilities of readjustment
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A very important series of experiments carried out in the laboratory
A very important series of experiments carried out in the laboratory
of Spemann on the embryos of Triton have shown that the future of
of Spemann on the embryos of Triton have shown that the future of
certain ectodermal areas in the gastrula are much modified by their
certain ectodermal areas in the gastrula are much modified by their
position. The method by which these experiments were carried out was
position. The method by which these experiments were carried out was
that of transplanting a portion of the ectoderm by means of a micro-pipette
that of transplanting a portion of the ectoderm by means of a micro-pipette
Line 15,362: Line 14,167:
become notochord, mesoblastic somites, pronephros, or perhaps other
become notochord, mesoblastic somites, pronephros, or perhaps other
organs. Ectoderm taken from a slightly later stage, that is, after the
organs. Ectoderm taken from a slightly later stage, that is, after the
closure of the blastopore, if carried into the mesoderm becomes meso-
closure of the blastopore, if carried into the mesoderm becomes mesodermal somites; if carried into the endoderm goes to the formation of
dermal somites; if carried into the endoderm goes to the formation of
the archenteron. It should be pointed out that particular organs which
the archenteron. It should be pointed out that particular organs which
differentiate from given substances may through the process of re-
differentiate from given substances may through the process of rearrangement be induced in an entirely different direction from that
arrangement be induced in an entirely different direction from that
which their normal determination indicated. Throughout the animal
which their normal determination indicated. Throughout the animal
kingdom there are many cases which serve to emphasize the difference
kingdom there are many cases which serve to emphasize the difference
between the determination of an organ and the actual differentiation
between the determination of an organ and the actual differentiation
which sometimes results from the modification of normal processes.
which sometimes results from the modification of normal processes.
What is shown by such cases, however, is not that the unusual condition
What is shown by such cases, however, is not that the unusual condition
is one of indetermination but that the organism has responded to modi—
is one of indetermination but that the organism has responded to modi—
Line 15,379: Line 14,182:
A problem which has given rise to a great deal of experimentation in
A problem which has given rise to a great deal of experimentation in
relation to the question of determination is the influence of pressure
relation to the question of determination is the influence of pressure
upon cleaving eggs. The work began with the experiments of Pflfiger
upon cleaving eggs. The work began with the experiments of Pflfiger
in 1884 in compressing the eggs of frogs between two glass plates. The
in 1884 in compressing the eggs of frogs between two glass plates. The
direction of the first three cleavage planes was found to be at right
direction of the first three cleavage planes was found to be at right
angles to the plane of compression. When the compression was released,
angles to the plane of compression. When the compression was released,
normal embryos developed. Similar experiments have been performed
normal embryos developed. Similar experiments have been performed
Line 15,387: Line 14,190:
found to follow the release of pressure on eggs of hydroids, sea-urchins,
found to follow the release of pressure on eggs of hydroids, sea-urchins,
frogs, and Cerebralulus. In eggs of N ereis, Ciona, and molluscs, abnormal
frogs, and Cerebralulus. In eggs of N ereis, Ciona, and molluscs, abnormal
development follows compression. In the first group of eggs it is to be
development follows compression. In the first group of eggs it is to be
noted that differentiation does not begin until there is relatively a
noted that differentiation does not begin until there is relatively a
large number of cells present. In the second group signs of differentia-
large number of cells present. In the second group signs of differentiation are to be noted very early. This series of experiments was used by
tion are to be noted very early. This series of experiments was used by
0. Hertwig and by Driesch in support of their opposition to the mosaic
0. Hertwig and by Driesch in support of their opposition to the mosaic
theory of development. Perhaps the experiments are less crucial than
theory of development. Perhaps the experiments are less crucial than
Line 15,397: Line 14,199:
capacities for regulation as distinguished from determination.
capacities for regulation as distinguished from determination.


Finally the literature of experimental embryology contains many
finally the literature of experimental embryology contains many
records of attempts to bring about the redistribution by centrifuging
records of attempts to bring about the redistribution by centrifuging
of egg substances, particularly those which are visibly different. These
of egg substances, particularly those which are visibly different. These
materials as well as the formed materials of the egg yolk, pigment, fat,
materials as well as the formed materials of the egg yolk, pigment, fat,
and other inclusions are often of different specific gravity and hence
and other inclusions are often of different specific gravity and hence
respond to centrifuging by redistributing themselves in different zones
respond to centrifuging by redistributing themselves in different zones
or strata. This transfer of materials throughout the egg takes place as
or strata. This transfer of materials throughout the egg takes place as
Line 15,410: Line 14,212:
embryology both because of the introduction of a new method and
embryology both because of the introduction of a new method and
because of his discovery that the redistribution of the egg constituents
because of his discovery that the redistribution of the egg constituents
does not afiect the development of the eggs from the standpoint of
does not afiect the development of the eggs from the standpoint of
determination. Many other investigators have used this method for
determination. Many other investigators have used this method for
the study of eggs through a wide range of animal forms. The results of
the study of eggs through a wide range of animal forms. The results of
Line 15,416: Line 14,218:
that the visibly stratified substances in the egg are not determinative in
that the visibly stratified substances in the egg are not determinative in
the sense that they are organ forming. It would seem that the method,
the sense that they are organ forming. It would seem that the method,
though productive of results which have great value from other stand-
though productive of results which have great value from other standpoints, has failed to give critical evidence as to the determinative character of development in the eggs to which it has been applied.
points, has failed to give critical evidence as to the determinative char-
acter of development in the eggs to which it has been applied.


As a conclusion to this long catalogue of evidences, the position
As a conclusion to this long catalogue of evidences, the position
Line 15,426: Line 14,226:
N 0 eggs are known which are purely regulatory or purely determinative,
N 0 eggs are known which are purely regulatory or purely determinative,
but at one end of the series differentiation sets in very late and the
but at one end of the series differentiation sets in very late and the
regulatory capacity is high. At the other end the marks of difierentiation
regulatory capacity is high. At the other end the marks of difierentiation
begin even before cleavage and the powers of regulation are correspond-
begin even before cleavage and the powers of regulation are correspondingly lessened.
ingly lessened.




==CHAPTER IX ECOLOGICAL CONTROL OF INVERTEBRATE LARVAL TYPES==
==CHAPTER IX ECOLOGICAL CONTROL OF INVERTEBRATE LARVAL TYPES==


Throughout the animal kingdom many diverse environmental rela-
Throughout the animal kingdom many diverse environmental relations surround the eggs and young so that many responses might be
tions surround the eggs and young so that many responses might be
catalogued. Environmental influences find expression in the places
catalogued. Environmental influences find expression in the places
where the eggs are laid, in the amount and kind of food provided for the
where the eggs are laid, in the amount and kind of food provided for the
young during the early development, in the different devices for their
young during the early development, in the different devices for their
protection, in specialized modifications for accomplishing locomotion
protection, in specialized modifications for accomplishing locomotion
and other vital activities, and in many cases in the production of forms
and other vital activities, and in many cases in the production of forms
of larvae ‘which are totally different from the adult organisms. These
of larvae ‘which are totally different from the adult organisms. These
Line 15,456: Line 14,254:
has presented many difficulties to the developing young and as a result
has presented many difficulties to the developing young and as a result
those animals which live in fresh water or are terrestrial are more often
those animals which live in fresh water or are terrestrial are more often
characterized by direct development than are the salt-water forms.-
characterized by direct development than are the salt-water forms.
 
It may be regarded as an axiom of development that sessile adults
It may be regarded as an axiom of development that sessile adults
have active young. This activity has two obvious results; first, the
have active young. This activity has two obvious results; first, the
species secures its dispersal through the migration of the young, and
species secures its dispersal through the migration of the young, and
econd, it extends the range. The migration is commonly passive but
econd, it extends the range. The migration is commonly passive but
over a period of time serves to extend the range of the species as success-
over a period of time serves to extend the range of the species as successfully as if the adults themselves were able to move. To insure dispersal,
fully as if the adults themselves were able to move. To insure dispersal,
vast numbers of gametes must be produced, for the chance method of
vast numbers of gametes must be produced, for the chance method of
fertilization that usually accompanies such cases results in a failure of
fertilization that usually accompanies such cases results in a failure of
Line 15,469: Line 14,265:
eggs which are fertilized only a few can come to maturity. The larval mortality is very high indeed, for these young are the food of many
eggs which are fertilized only a few can come to maturity. The larval mortality is very high indeed, for these young are the food of many
species as well as the victims of physical forces and of their own inability
species as well as the victims of physical forces and of their own inability
to find continuously satisfactory conditions for growth. The vast number
to find continuously satisfactory conditions for growth. The vast number
of eggs produced may be realized by reference to the turbot which pro-
of eggs produced may be realized by reference to the turbot which produces 9,000,000 in a single season, the cod with 5,000,000, and to the
duces 9,000,000 in a single season, the cod with 5,000,000, and to the
flounder with 1,000,000. In higher animals the reproductive energy
flounder with 1,000,000. In higher animals the reproductive energy
is conserved by various means for caring for the young during early life,
is conserved by various means for caring for the young during early life,
but in marine forms this is usually not the case. The second consequence
but in marine forms this is usually not the case. The second consequence
of larval activity is to bring the growing forms into an entirely difierent
of larval activity is to bring the growing forms into an entirely difierent
range. This is illustrated in the case of the lobster, which is a bottom
range. This is illustrated in the case of the lobster, which is a bottom
feeder, lurking in the crevices between stones and elsewhere to capture
feeder, lurking in the crevices between stones and elsewhere to capture
Line 15,492: Line 14,287:
then goes to the bottom. Herrick makes note of several changes in
then goes to the bottom. Herrick makes note of several changes in
structure and instincts which take place at the beginning of the fourth
structure and instincts which take place at the beginning of the fourth
stage, which marks the most surprising leap in the whole history of de-
stage, which marks the most surprising leap in the whole history of development. Among these are the following: the primitive swimming
velopment. Among these are the following: the primitive swimming
branches of the thoracic appendages are lost; the cuticle becomes shell—
branches of the thoracic appendages are lost; the cuticle becomes shell—
like, containing more lime; the pigments are denser, the colors brilliant,
like, containing more lime; the pigments are denser, the colors brilliant,
Line 15,500: Line 14,294:
at least a part of this stage, moves toward the light and swims steadily
at least a part of this stage, moves toward the light and swims steadily
at the surface with the great claws directed forward and held close
at the surface with the great claws directed forward and held close
together; the preying instinct is more marked; the fighting instinct,
together; the preying instinct is more marked; the fighting instinct,
the instinct of fear, “feigning,” and hiding are all developed by the
the instinct of fear, “feigning,” and hiding are all developed by the
close of the fourth stage or in the fifth, when the animal goes to the
close of the fourth stage or in the fifth, when the animal goes to the
bottom to stay. In many other animals similar gain is accomplished
bottom to stay. In many other animals similar gain is accomplished
by a specialized form of larval structure. The larva finds itself adapted
by a specialized form of larval structure. The larva finds itself adapted
to-securing food which is suitable for it, and structures which have
to-securing food which is suitable for it, and structures which have
only temporary employment are present and useful. It follows, however,
only temporary employment are present and useful. It follows, however,
that the gain to the larva would become a loss if the subsequent stages
that the gain to the larva would become a loss if the subsequent stages
in the life cycle were not radically changed in such a way as to enable
in the life cycle were not radically changed in such a way as to enable
the organism to undertake a new mode of life. In other words, meta-
the organism to undertake a new mode of life. In other words, metamorphosis in such cases is a necessity for bringing about those adaptations which fit the organism to live in its permanent environment and
morphosis in such cases is a necessity for bringing about those adapta-
tions which fit the organism to live in its permanent environment and


there to undergo those further changes which look toward the produc-
there to undergo those further changes which look toward the production of new germ cells.
tion of new germ cells.


It is not usual to find metamorphosis in animals which live in fresh
It is not usual to find metamorphosis in animals which live in fresh
water, although there are some outstanding cases in which larvae
water, although there are some outstanding cases in which larvae
totally unlike the adult are developed in species inhabiting fresh water.
totally unlike the adult are developed in species inhabiting fresh water.
It may, however, be taken as a general rule that development in fresh-
It may, however, be taken as a general rule that development in freshwater forms with the exception of certain few highly specialized cases
water forms with the exception of certain few highly specialized cases
is direct. Fresh water presents a great lack of constancy in living conditions as compared with those of the sea. With but few exceptions the
is direct. Fresh water presents a great lack of constancy in living con-
bodies of fresh water lack sufficient depth and area to maintain even a
ditions as compared with those of the sea. With but few exceptions the
bodies of fresh water lack sufficient depth and area to maintain even a
low degree of constancy. Fresh water becomes heated much more easily
low degree of constancy. Fresh water becomes heated much more easily
than the sea, it freezes comparatively quickly, its streams are subjected
than the sea, it freezes comparatively quickly, its streams are subjected
to periods of flood during which the water runs rapidly and scours out
to periods of flood during which the water runs rapidly and scours out
the beds or overflows, and when it recedes leaves innumerable forms of
the beds or overflows, and when it recedes leaves innumerable forms of
life stranded to perish. Every stream has narrows and depths where it
life stranded to perish. Every stream has narrows and depths where it
runs rapidly and flats where its current is slow, an environment in
runs rapidly and flats where its current is slow, an environment in
which the fragile larvae would scarcely be able to maintain themselves,
which the fragile larvae would scarcely be able to maintain themselves,
and there are but few animals which go through an independent larval
and there are but few animals which go through an independent larval
Line 15,536: Line 14,325:
animals have not been able to gain a foothold in fresh water. A very few
animals have not been able to gain a foothold in fresh water. A very few
sponges, almost no coelenterates, occur in this environment, and many
sponges, almost no coelenterates, occur in this environment, and many
groups of marine fish and ascidians, cephalopods, king crabs, and some
groups of marine fish and ascidians, cephalopods, king crabs, and some
of the worm groups have not a single representative in fresh water.
of the worm groups have not a single representative in fresh water.
Animals that cannot produce eggs which develop into young like the
Animals that cannot produce eggs which develop into young like the
adult are prevented from gaining ‘a. foothold by such a changeable
adult are prevented from gaining ‘a. foothold by such a changeable
medium as fresh water. In addition to the difficulties of fresh-water life
medium as fresh water. In addition to the difficulties of fresh-water life
already noted, a zone of brackish water between the fresh water and
already noted, a zone of brackish water between the fresh water and
the sea is itself an almost impassable barrier to the entrance of marine
the sea is itself an almost impassable barrier to the entrance of marine
Line 15,555: Line 14,344:


environment are the following: temperature undergoes a wide range
environment are the following: temperature undergoes a wide range
of variation, often passing quickly between the extremes. This con-
of variation, often passing quickly between the extremes. This condition is quite unknown in the ocean and is much less in fresh water.
dition is quite unknown in the ocean and is much less in fresh water.
The very changeableness as well as the extremes of heat and cold are
The very changeableness as well as the extremes of heat and cold are
hardships for the developing larvae. The weight of the body is no
hardships for the developing larvae. The weight of the body is no
Line 15,566: Line 14,354:
more restricted as to kind, and presents an increased toughness since
more restricted as to kind, and presents an increased toughness since
in the composition of land forms the percentage of water is much less,
in the composition of land forms the percentage of water is much less,
and the food is necessarily more difficult to find. The glare of daylight
and the food is necessarily more difficult to find. The glare of daylight
and the consequent difficulty of avoiding enemies puts the terrestrial
and the consequent difficulty of avoiding enemies puts the terrestrial
larvae to a disadvantage which forms living in the subdued shadows of
larvae to a disadvantage which forms living in the subdued shadows of
the water do not share. Finally the rapid evaporation to which terres-
the water do not share. finally the rapid evaporation to which terrestrial forms are subjected requires special devices for protecting the soft
trial forms are subjected requires special devices for protecting the soft
exterior of the organism. A heavy shell, mucous glands, and other
exterior of the organism. A heavy shell, mucous glands, and other
similar devices show what a serious drain upon the organism require-
similar devices show what a serious drain upon the organism requirements of this kind cause.
ments of this kind cause.


These considerations account in a large measure for the lack of
These considerations account in a large measure for the lack of
uniformity in the occurrence of larval types throughout the different
uniformity in the occurrence of larval types throughout the different
groups of the animal kingdom. The particular forms of larvae within a
groups of the animal kingdom. The particular forms of larvae within a
group are of adaptive rather than taxonomic significance.
group are of adaptive rather than taxonomic significance.


The general subject of the care of young animals was briefly but
The general subject of the care of young animals was briefly but
instructively discussed by Gamble in “The Animal World” (Holt and
instructively discussed by Gamble in “The Animal World” (Holt and
Company). Some of the ideas mentioned on the three preceding pages
Company). Some of the ideas mentioned on the three preceding pages
are suggested by his discussion. Gamble sums up the responses of
are suggested by his discussion. Gamble sums up the responses of
animals to different environmental conditions in which the young must
animals to different environmental conditions in which the young must
be produced as follows:* “We find isolated examples of the retention of
be produced as follows:* “We find isolated examples of the retention of
the young by diminution in the size of the family. Speaking generally,
the young by diminution in the size of the family. Speaking generally,
marine animals pour their eggs broadcast, and leave their minute larvae
marine animals pour their eggs broadcast, and leave their minute larvae
Line 15,602: Line 14,388:
which go through their larval life in fresh water. But the protection
which go through their larval life in fresh water. But the protection


is usually of the simplest kind and is confined to the earlier stages of
is usually of the simplest kind and is confined to the earlier stages of
development.
development.


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Richards A Outline of Comparative Embryology. (1931)
1931 Richards: Part One General Embryology 1 Historical Development of Embryology | 2 The Germ-Cell Cycle | 3 Egg and Cleavage Types | 4 Holoblastic Types of Cleavage | 5 Meroblastic Types of Cleavage | 6 Types of Blastulae | 7 Endoderm Formation | 8 Mesoderm Formation | 9 Types of Invertebrate Larvae | 10 Formation of the Mammalian Embryo | 11 Egg and Embryonic Membranes | Part Two Embryological Problems 1 The Origin And Development Of Germ Cells | 2 Germ-Layer Theory | 3 The Recapitulation Theory | 4 Asexual Reproduction | 5 Parthenogenesis | 6 Paedogenesis And Neoteny | 7 Polyembryony | 8 The Determination Problem | 9 Ecological Control Of Invertebrate Larval Types

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Outline of Comparative Embryology

By

Aute Richards

Profaso 0 7,00/ugy Univrr.r1' 0 0/c/ahomc:

NEW York JOHN WILEY 8: SONS, INC. LONDON: CH/APMAN 8: HALL, LIMITED ’ 1931 (,'um1uL.u'1', 1951


Preface

As the result of a number of years of experience in introducing students to the subject of embryology, the writer has found it desirable to ‘depart from the common practice of studying chiefly the special embryology of the chick, pig, and perhaps of amphioxus and the frog, and to devote much attention to the principles of general embryology. This procedure is based upon the assumption that a broad background of general knowledge forms a desirable starting point for the study of special embryology to be taken up later. As comparative anatomy has proven to be the best basis for the later study of anatomy, so comparative embryology forms a proper basis for a study of special embryology. Unfortunately there has been no book in our language which brings together in a small compass the principles of general comparative embryology.

In this book it is the aim to set up the general principles of development so that the student may see how his special case—chick, starfish, or other form—is merely one of several types and what its relation to the other types may be. The writer holds that the most effective presentation of the subject matter of embryology is the laboratory study of desirable types, supported by text-book and “quiz” work on these forms and accompanied by the consideration from a comparative standpoint of the broad principles of the subject, such as types of egg structure, of cleavage, of gastrulation, and the critical consideration of classical embryological doctrines, etc. To present the material in brief form for this general part of a course in Comparative Embryology this volume is designed. '

In Part One are taken up those phases of development which are passed through in the embryology of most higher forms of animals. A comparative study of these phases no doubt forms the basis of ninetenths of the courses in this subject. Of the vast amount of material from which choice must be made, the decision as to whether any certain topic should be discussed has been based always upon a single criterion. It is sought to show only how the single-celled fertilized egg arrives at the multicellular condition characteristic of the fully formed, but undifferentiated, young organism in which the organ systems are established. In an outline of comparative embryology it is not possible to follow through all the details nor to repeat descriptions whose general features apply to more than one kind of animal. Nor is it possible to follow through for these forms the later stages in their development and differentiation. If completeness were the goal, it would be necessary to include the special embryology of the many forms about which investigators would desire information, an obviously impossible task. It is hoped, however, that a basis is here laid for understanding the detailed embryology of any of the types and for working out later stages in whatever group the student’s interest may lie.


Part Two considers numerous miscellaneous problems that have arisen in connection with the history of embryology. Here the choice of topics has been governed largely by questions asked by students both beginning and more advanced. No attempt is made to cover all the classical topics of embryology, nor to arrange the ones chosen in an order to develop any particular thesis. It is simply thought to satisfy in some measure student interest in them and to make them easily available. Discussions of many of them are not available in brief form in any English text, although they concern matters about which students of zoology should be informed, for they are chiefly problems of normal development.


The embryology of the present day is experimental embryology. Its aim is to secure an insight into the real nature of those steps by which a single-celled egg becomes a completed adult. An understanding of development in its true sense is its goal. Many aids to experiment used only by chemists or physicists in years gone by are now every-day tools of the embryologists, for descriptive embryology alone is inadequate to give a complete understanding of development. Yet experimental embryology runs the danger of considering only processes and those out of relation to structures. It is in structures that functions are inherent, for one cannot understand the workings of a machine with which he is unfamiliar. Morphology in its descriptive phases is therefore basic to a proper attempt to work out functional relations. Our admiration for the attempts to secure an intelligent conception of the mystery which underlies the pageant of development must not allow us to disregard the importance of a foundation of knowledge of descriptive embryology. Perhaps the errors which may be avoided by the study of descriptive embryology in its comparative phases may serve to recompense the student for the time lost from experimental embryology.


Undoubtedly numerous errors are to be found in this volume. Much that is discussed has been the subject of life-long study by many investigators and has concerned material collected from all over the world. To understand all adequately so that each may be mentioned correctly and weighted properly in a brief outline, is a task hardly to be accomplished, and many inconsistencies of treatment must be apparent to the reader. It must be borne in mind, however, that not an extended treatise but an outline of principles is the intent of the book, and the intent places many limitations upon what can be undertaken.


Acknowledgments are due for assistance in almost every section. The material treated in a work of this kind is by no means new, and it would be impossible to present any one phase of it without finding parallel treatment in some source of information available to students of embryology of this day. There is no claim to originality in the book, not even in the treatment of many chapters. The book will have served its purpose, however, if it appears to have sufficient pedagogical background and if it presents in sufficiently compact form these principles, many of which I think are not briefly summarized elsewhere in the English language, and which are needed to give students a basis for work in special embryology,-either medicalor experimental.


Korschelt and Heider’s “Lehrbuch der vergleiehenden Entwicklungs— geschichte” is a great treasure house of embryological learning to which constant reference has been made. In many places (particularly in Chapters VII and VIII, Part One) even their arrangement has been so much the best that only minor departures from it are to be found here. In others an entirely different organization of the same material is here adopted. But the debt to Korschelt and Heider is a very great one. I appreciate very mucl_1-the gracious verbal permission to use their material freely which was given me by both Doctors Korschelt and Heider. .”_


Drawings to illustrate ,the text are from many sources and not many are new. The writer is not impressed with the desirability of replacing pictures made by investigators on specialforms with new ones when the former are well known and of proven value. The drawings in every case are accompanied by a legend giving the name of the investigators to whom indebtedness is due.


Permission has been granted by the following publishers to make use of the figures indicated either as modified, or in the case of numbers 1, 2, 3, 135, 136, 142, 153, 1-81 of the figures themselves. By Henry Holt & Co. permission has been given to use from Loey’s “Biology and Its Makers,” our figures 1, 2, and 3; to use from Kellicott’s “General Embryology” our figure 5; from Kellicott’s “Chordate Development” our figures 135, 136, 142, 144, and 181; and from Lillie’s “Embryology of the Chick” our figures 151, 152. By P. Blakiston’s Son & Co., Inc., permission has been given to use from Folsom’s “Entomology with Special Reference to Its Ecological Aspects,” 3rd edition, our figures 117, 161, and 162; and from Patten’s “Embryology of the Pig,” figure 7. The Oxford University Press has permitted the use from Jenkinson’s “Vertebrate Embryology” of our figures 81 and 173. The Princeton University Press has granted permission to use from Conklin’s “ Heredity and Environment” our figures 7 and 8. The U. S. Bureau of fisheries has given permission to use from Herrick’s “American Lobster” figures 113, and 1973.. And William Wood & Co. have permitted the modification of figures from Bailey and Miller’s “Textbook of Embryology” represented in figures 140 and 141. Macmillan & Co., Ltd., has sold us permission to make use of our figures 103, 109, 110 from McBride’s “Textbook of Embryology, Vol. I, Invertebrate Embryology,” and of our figures 167, 168, and 170 from Graham Kerr’s “Textbook of Embryology, Vol. II, Vertebrate Embryology.” The graciousness of the various publishing companies in thus facilitating our work is deeply appreciated.


Especial acknowledgment for help in many ways including aid with the materials used and the reading of parts of the text is due to 1ny wife, Mrs. Mildred Hoge Richards. My colleagues of the Department of Zoology of the University of Oklahoma, Doctor A. O. Weese and Doctor A. I. Ortenburger have assisted with advice and have read portions of the text. Professor J. F. Paxton of the Department of Greek has aided me with questions of terminology. And finally my assistants Mrs. Celeste Whaley Taft and Miss Kara J. Fullerton have given the most painstaking attention to a multitude of details. To all of these I am deeply grateful.

A. R.

Part One General Embryology

Chapter I Historical Development of Embryology

The science of embryology is scarcely a century old, dating from the work of Pander (1817) and von Baer (1827) whose investigations into developmental phenomena were more accurate than those of the earlier students and who were the first to give systematic form to the subject; but interest in and curiosity as to the events of the pre—natal period in animals or of the life and growth of an embryo, especially of the chick before hatching, goes back to the ancients, as evidenced by the contributions by Aristotle and Galen among the Greeks. Aristotle was the author of three works of great zoological importance, in one of which, “De Generatione Animalium,” are given the results of his observations on the reproduction of various forms of animals as well as a description of the progressive stages in the development of an incubated egg. These observations were made directly upon the egg without the aid of lenses, and of course were very incomplete. The advance of embryological knowledge waited for the application of the lens to the study of life forms and processes which began seine four hundred years ago. With the invention of the microscope the subject wen fresh impetus until it became one of the major biological sciences when supported by exact cell studies in the last century.

Following Loey,* we may divide the progress during this time into periods as follows: (1) the period of Harvey and Malpighi; (2) the period of Wolff; (3) the period of von Baer; (4) the period from von Baer to Balfour; (5) the period of Balfour and comparative embryology; (6) the period of experimental embryology.

1. Harvey published in 1651 a treatise on embryology (“Exercitationes de Generatione Animalium”) in which are recorded observations on the development of the chick and some facts of mammalian embryology. He also discussed the nature of development and deduced from observations the important principles that all animals come from ova and that the development is a new formation, not more growth or enlargement. His study was made with simple lenses which did not enable him to trace the genesis of the embryo from its earliest stages. Malpighi, who was more of a microscopist than Harvey, outranks him as an

  • Only the first five periods are recognized by Locy.

1 2 HISTORICAL DE\'l*lL()l’.\Il£.\'l‘ OI" la'.\lBl{\ ()L()GY

embryologist. His work on the development of the chick, published in 1672, shows Harvey’s influence, but by means of excellent descriptions

and many sketches carries the account of the development back to the close of the first day of incubation.

2. A century later than Harvey came the work of Caspar Friedrich Wolff, whose “Theoria Generationis” was first published in 1759. At

that time embryology was dominated by the conception of pref0rma Fur. 1. William Harvey. (From Loey.)

tion which had gradually grown up around the observations of Malpighi, Leeuwenhoek, Boerhaave, and oth.'-rs. Although the point of view maintained by Wolff, that of epigenesis, had also been that of Harvey and Aristotle, he is to be regarded as the first active proponent of that doctrine. He was opposed by the great physiologist, Haller, and by Bonnet, a very prolific writer on the subject. Led by these men, the 1)1-eforination-epigenesis controversy held the attention of embryologists to the close of the eighteenth century. lll.\"l‘()l{lCAL DEVlCL()I’ME‘.\"l‘ <)[*‘ l".I\Il1l{\'0I.0GY 3

3. The pmiml of von Baer really begins with the ()l).\‘C1'V2l,tl()I1S of his friend, Pander, first published in 1817. Pander established the presence

of three layers in the early embryo from which the later organs are developed. Obviously this is a conclusive argument against the old preformation views. Von Bacr, however, is responsible for the germ fiG. 2. K.ul Ernst um Bu-1 (Fmm Lot-\.l

layer doctrine as a ;1(*m‘l.lllA2l,tl()n, and fun the (‘\])()~itiOn of the manner in which the layers give rise to the later organs of the embryo. He also discovered the egg in the ovary of mammals and of man and pointed out the similarity in the mode of origin of these animals to those lower in the scale. He was the first to recognize the notochord as occurring in all vertebrate animals and to point out the value of comparative embryology for anatomy and zoology. With von Baer the modern pmiml of 4 llIS'l‘Ol{l(‘\l. l)|l\ l,l.()l’.\IlCN'l‘ OI" EMl§RY()l.0GY

(‘l!1l)I‘}’()l()gy really begins. Von Baer is often spoken of as the originator of the 1'(‘e:t1,)lt1llatl0I1 doctrine, and he did hint at it, but the formulation is due to Fritz Miillcr in 1863. Von Baer called attention to the greater similarity that exists between embryos of related groups than between adults. The younger the embryos the more alike are they. The recapitulation theory will be considered on a later page.

4. The period following von Baer is one of rich biological achievement. The discovery of the cell, nuclei, mitosis, the publication of the evolution doctrine, the birth of histology and pathology, all wrought changes in the aspects of biology that necessarily had their influence on embry


fi(. C l \l llillnm (l“minl,m\)

ology. The facts of development were harmonized by the conception of evolution, and both comparative anatomy and paleontology threw light on the reasons for some of the ()bs(‘u1'0 embryological phenomena discovered. This period saw established the relation of cells, tissues, and organs in the embryo, recognition of egg and sperm as cells, the process of fertilization, many details in the development of both vertebrates and invertebrates, and the beginnings of the doctrine of germinal continuity.

5. The period of Balfour was one of exact morphological research. Balfour was a young English embryologist (1851-1882) whose “Monograph on the Development of Elasmobranch fishes” (1878), and whose “'l‘r<-alise on (‘mnp:11'ati\<- l3lml)ryology” (1880-1881), Won the highest EVENTS OF IMPORTANCE IN THE HISTORY OF EMBRYOLOGY 5

recognition. With improved microscopes and technique vast numbers of investigations have been undertaken since his time and the literature of the science greatly enriched. The newer science of cytology is a direct offshoot of the embryology of this period due to the pushing farther and farther back of the questions on the origin of germ cells and the fertilization and early development of the egg. One of the most notable advances of this period lay in the field of cell lineage. The investigations of the eighties and nineties established for the eggs of many animals a complete history from the one-celled egg to the larval form with definite fundaments of organs which later by specialization and elaboration make up the body of the adult. Thus is the organized character of the young embryo made clear even before the germ-layer stage. Thus also we know that in the organization of the egg there is a predetennination of the adult characters, a point of view which corresponds closely to neither of the old ideas of preformation and epigenesis.

6. While much of a morphological character remains to be learned by embryologists of the future, it is not to be supposed that the nature of the organic mechanism could be investigated only from that standpoint. With the increase of exact knowledge of the structure of the organism, we demand information as to its method of operation. To the developing animal must be applied not only the laws of physiology, with a correspondingly better understanding of the origin and development of these functions, but also the laws of physics and chemistry, and particularly physical chemistry must be appealed to. The study of development in the light of these laws is the dominant note of the embryology of the present day, and as an experimental science it is making remarkable strides forward. The present is the period of experimental embryology, although of course there are many problems of morphological character which are still to be solved.

EVENTS OF IMPORTANCE IN THE HISTORY OF EMBRYOLOGY

AN('1aN'r 'l‘IMEs. Much information and many observations known to have been accumulated, but not recorded as a body of knowledge. Systems of medicine were developed both in Greece and in Egypt in PreAristotelean times.

4-TH CENTURY, B.C. Aristotle (384—322 B.C.) made first system of classification of animals and plants, published first accounts which are extant of natural history, anatomy, and embryology. Wrote “De Generatione Animalium.”

Dissection of human body legalized in Alexandria.

2ND CENTURY, A.D. Galen compiled and brought up to date knowledge of anatomy and physiology, but without aid of human dissection.

16TH CENTURY. Vesalius (1514-1564) reformed teaching of anatomy. intro-6 HISTORICAL DEVELOPMENT OF EMBRYOLOGY

.ducing dissection and replacing appeal to ancient authorities. “Structure of Human Body” published 1543. V _ 1625. K Fabricius’ (1537-1619) treatise on development of chick published. ‘1,7'1jH'C1:N'rURY. Harvey (1578-1667) instituted experimental study of living animals. Announced discovery of circulation of blood in 1616; published .“De ’Motu Cordis et Sanguinis” in 1628. Published in 1651 “De Generations Animalium,” an embryological treatise. Invention of compound microscope had occurred by early years of seven! teenth century and it was applied to biological uses by middle of '- century. 16-15. Severinus (1580-1656) published “Zootomia Democritae” giving anatomical descriptions of comparative type of some vertebrates, and some developmental stages.

1665. Hooke (1635-1703) published “Microgr:iphia.”

16,66. Redi experimentally disproved spontaneous generation of life among insects.

1669., Malpighi (1628-1694) published “Anatomy of Silkworm.”

_l672. Malpighi published two works on embryology: “De Formatione Pulli in Qvo,” and “De Uvo Incubate.”

Swaiiiinerdam (1637-1680) studied development of butterfly and by analogy to pupa thought earlier organs were preformed in egg (not published until 1737).

1675. Leeuwenhoek discovered spermatozoa (also attributed to Hamm,

' a medical student). Leeuwenhoek accordingly became a strong preforlniationist, adhering to the school of the “spermists.” 18TH CENTURY. 1713. Leeuwenhoek discovered parthenogenesis in plants. ' 1735. ‘Linnaeus (1707-1778) published first edition of “Systcma Naturae.” ' In 1753 he introduced the binomial system of nomenclature in “Species

‘ Plantarum,” and in 10th edition of “Systema Naturae” in 1758.

1759. Wolff (1733-1794) published “Theoria Gcnerationis” in defence of position of epigenesis.

1768. He published “De Formatione Intcstinorum,” the greatest master‘piece of embryology before V011 Bacr.

1799. Cuvier (1769-1832) founded comparative anatomy.

19TH CENTURY. 1800. Bichat (1771—1801) founded histology. ’ ' 1812. Cuvier founded vertebrate paleontology.

1817. Pander (1794-1865) recognized three primary body layers in chick.

18:24. ' Prevost and Dumas saw segmentation in animal egg.

1828. "Von Baer (1792-1876) published “Entwicklungsgesehichte der "1‘iere.” Founded embryology as a science. Established the doctrine of germ layers. Made embryology comparative. Proposed a theory of recapitulation.

1831., Robert Brown (1773-1858) discovered the nucleus.

1835. Dujardin (1801-1862) discovered living matter, sareode, in lower animals. EVENTS OF IMPORTANCE IN THE HISTORY OF EMBRYOLOGY 7

1838. Schwann (1810-1882) with Schleiden (1804-1881) founded cell theory.

1841. Remak (1815-1865) figured cell division (amitosis). His work and that of Kiilliker laid foundations for a theory of cell division.

1846. Von Mohl (1805-1872) observed protoplasm in plants and named it.

1851. Newport observed entrance of sperm of frog into egg.

1856. Von Siebold (1804-1885) described parthenogcnesis.

1858. Virchow (1821-1903) published “Cellular Pathology.” Omnis cellula e cellula.

1859. Darwin (1809-1882) published “Origin of Species.”

1861. Kolliker (1817-1905) published general treatise on embryology. Studied segmentation of egg.

1861. Max Schultze (1825-1874) formulated protoplasin doctrine.

1863. Muller (1821-1897) propoundcd rccapitulation doctrine.

1865. Sperms recognized as cells.

1866. Mendel (1822-1884) published studies on inheritance.

1866. Kowalcvsky (1840-1901) showed that all animals pass through gastrula stage.

1862-1869. Pasteur (1822-1805) and Tyndall (1820-1893) disproved spontaneous generation.

1868. Use of stains in study of cells and protoplasm introduced.

1870. His (1831-1904) introduced use of microtome.

1873. Anton Dohrn (1840-1909) founded the Naples Zoological Station.

1874. Haeckel (1834-1919) proposed gastrea theory.

1874. Balfour and Foster published “Elements of limbryology.”

1875. fleininiiig (1843-1905) discovered centrosome.

1875. Strasburger (1844-1912) first figured adequatel_v chromosomes and cell division.

1878. Whitman (1842-1910) published “l7.mbryology of Clepsine,” which with Ma1'k’s (1847— ) paper on “Maturation, Fecundation, and Segmentation of Limax” began the studies which became known as cell lineage in the next two decades.

1879. flemming distinguished between direct and indirect types of cell division. ‘

188()—1881. Balfour (1851-1882) published “Comparative Embryology.”

1882. flemming discovered longitudinal split of chromosomes.

1883. Roux (1850-1924) began studies of experimental embryology using frog’s egg.

1891. Weismann (1834-1914) published theory of germ plasm.

Since 1890 the advances of embryology have been so numerous and so many investigators have been concerned that it is impossible now to choose between them as to historical significance.

Bibliographic Note

Among the more important accounts of the subjects contained in this chapter are the following: Locy, Osborne, Foster, Wilson, Gerould, Hertwig, and Nordenskiold. These works are cited in full in the bibliography on page 406.

Chapter II The Germ-Cell Cycle

The ontogeny of an organism includes its entire cycle of development from its earliest beginnings to old age and death. Embryology includes the first part of this cycle. Broadly considered, it may be held to include the development of the germ cells (gametogenesis) in their preparation for fertilization and cleavage, and most text-books treat of these matters. It is our purpose, however, in the present study to give but brief treatment to this phase of the subject, for general introductory courses in zoology commonly include a brief outline of gametogenesis, and a more thorough study deserves more treatment than can be given in a course in embryology.

Embryonic development in its narrower sense may be said to begin with fertilization of the egg and to consist of four periods. These are: first, cleavage; second, formation of germ layers; third, period of organ development; fourth, period of histological differentiation. It is to be noted that in many animals these four periods are not sharply separated from each other. The principles which are of importance from a comparative standpoint are chiefly illustrated by the first three of these periods.

The beginning of the life cycle of every organism is very closely related to the development of the parent, in that the cells from which the new organism comes are early set aside and from then on are to be distinguished from the other cells and organs of the body. Strictly speaking, the embryology of an animal would require us to trace the germ cells from their very first appearance on up through the stages of their development and to trace the formation of the matured sperm and ovum as well as the fertilization, cleavage, germ-layer formation and the subsequent stages, if we were to give a complete account of development. But it has come to be the practice to begin the embryologieal account with fertilization and cleavage, and we shall therefore deal with the germ-cell history only briefly, leaving the cytological details for other more exhaustive treatments.

Our knowledge of this development is a matter of the last half century, and so voluminous has the accumulated information become on

the problems connected with the cell that it now constitutes an entirely 8 THE GERM-CELL CYCLE 9

separate division 0" zoological science, namely cytology. The foundations of this science were laid in the last two decades of the nineteenth century by investigators who sought information concerning earlier and earlier stages of germ-cell development. These studies received a great impetus from the conception of the germ plasm which was published during the early part of the period by Weismann. The organism was thought of as consisting of two more or less opposing portions, a germ plasm (which functions as a hereditary vehicle and is passed on to the next generation as it gives rise to the new individual) and soma or somatoplasm (which is the remainder of the organism’s body and is concerned with its individual well-being). It was thought by the earlier students that certain cells were thus the germ plasm, that is, the germ cells as contrasted with the body cells, while others had no part in the reproductive activities of the organism except in so far as they were necessary for nourishment and support.

This conception has been largely responsible for the attempts, now of many years’ standing, to trace the origin of the germ cells back to the early blastomeres, that is, earlier than the period in which they can be recognized as part of the reproductive organ, the gonad. These attempts were productive of successful results in quite a number of cases in both vertebrates and invertebrates where it was found that the antecedents of the primordial germ cells could be recognized even in early cleavage divisions. In other cases, however, it has not been found possible to trace the history of the primordial germ cells back of their first appearance in the gonads. The origin of the primordial germ cells is an embryological problem of considerable importance in itself aside from its relation to the germ-plasm doctrine, and as such it is discussed in detail in a later chapter in this book. (See Part Two, (‘hapter II.)

Partly as a result of the inconclusive data from the study of the origin of the primordial germ cells in‘ the animal kingdom as a whole, but more especially as a result of the work of recent years on heredity in which the importance of the chromosome has been made manifest, a new conception of the germ plasm has now showed itself to be more acceptable to many students of these problems than that of Weismann. According to this new view, each cell contains material which corresponds to both the germ plasm and soma, the chromatin representing the former and the cytoplasm the latter. This interpretation explains many facts which had previously proven difficult to understand and enables us to regard the origin of germ cells as a problem of embryology rather than as one whose chief interest is in relation to the transmission of a “germ plasm.” 10 THE GERM-CELL CYCLE

1. Cell Division in Gametogenesis

Regardless of their source or of the time of their first appearance, there are present in a developing gonad certain cells which are known as primordial germ cells. They remain in a quiescent stage during the early development of the organism, beginning their active development only when the somatic structures are well on the way to their adult condition. Somatic structures are produced by the differentiation of the cytoplasmic portions of the cells (giving rise to the familiar histological distinctions between tissues), and must obviously precede those activities which have for their end the reproduction of the organism. On the other hand, specialization of the nuclear structures involved in the function of mitotic cell division is responsible for reproduction and must wait until the proper development of the somatic structure has been attained.

a. Multiplication Period. At length the primordial germ cells begin a period of proliferation known as the multiplication period. This period varies in different forms, both as to its beginning and its duration, for it does not necessarily begin at the same stage in the life cycle, nor does it consist of the same number of cell divisions. It is said that in the grasshopper there are eight divisions in this period; thus each primordial germ cell would produce as a result 256 descendants. The cells undergoing the various divisions of the multiplication period are knovsn as gonia; the male cells are sperrnatogonia and the female oiigonia, alike in every fundamental respect.

b. Growth Period. At the end of the multiplication peziod, that is, with the formation of the primary oiigonia or spermatogonia, the active proliferation of cells ceases and there follows a growth period. During this period without further division the cells increase in size and store up nutrient material, deutoplasm, to furnish them with energy for the further activities they are to undergo. In the case of the oogonia this material is the yolk, often present in large amount to furnish food for the embryo until it has become at least in part able to obtain sustenance from its surroundings. The amount and distribution of this yolk material is a very important factor in determining the type of cleavage and future development of the embryo, for cell division becomes increasingly difiicult with the accumulation of inert yolk material. (This point should be kept in mind, for frequent use must be made of it in the study of cleavage types.) These cells are new primary spermatocytes or ooeytes.

c. Maturation Period. Two maturation divisions now succeed each other, usually with some degree of rapidity. They constitute the matuMATURATION PERIOD 11

ration period during which nuclear events of the utmost importance from the standpoint of the future organism occur. In oogenesis as well

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fiG. 4. Diagram to illustrate the processes of gametogenesia.

as spermatogenesis there are two divisions which are similar in all respects except one. In the maturation of male germ cells, the first 12 THE GERM~CELL CYCLE

division results in two second spermatocytes which promptly divide again producing four spermatids from each primary spermatogonium. (In the grasshopper obviously there would be now 1024 descendants from each primordial germ cell.) These cells do not again divide but go through a seriés of changes (spermiogenesis) by which they become metamorphosed into functional spermatozoa with the characteristic structure of spermatozoa; these changes are cytoplasmic in character. In the developing female germ cells, however, maturation results in the production of one functional egg and three non-functional cells which are its equivalents from the standpoint of nuclear content and which are known as polocytes or polar bodies. This is accomplished as an immediate result of the fact that the first maturation spindle is short and occupies a position near the surface of the large oocyte. Since the division plane cuts through the center of the spindle, a very small cell, the polocyte, is cut off from the larger “egg cell” which is now the second oécyte. In the second maturation division both cells divide, the “egg cell” again unequally producing a matured egg and another polocyte, and the first polocyte two other polocytes. This size dil’ferentiation of the four cells which are descendants of the primary oiigonia allows the normal nuclear events of maturation to go on unmodified, but concentrates the ooplasmie materials, which are necessary to the nourishment of the embryo, in one functional cell.

Gametogenesis is now completed. Sperm and egg are ready for the next step toward the production of a new organism, namely fertilization. By fertilization is meant the entrance of the sperm into the egg, but the process is very complicated and is completed only with the union of egg and sperm nuclei into a fusion or cleavage nucleus. Fertilization has two functions which are distinctly different: the initiation of cleavage or the development of the zygote, and the restoration of the chromatin material equivalent to that lost in reduction. This complicated process has been the subject of much study during the last two decades, especially from the viewpoint of experimental or physiological embryology, and many fundamental conceptions have resulted from this fascinating phase of embryologieal research.

2. Nuclear Events in Gametogenesis

The nuclear events during gametogenesis must also be understood, at least in outline. Their study has been the especial problem of cytology during the last quarter of a century.

a. Reduction. It may be stated as a general law that every species of organism is characterized by a definite number of chromosomes, and, REDUCTION 13

with a few exceptions which are not in contradiction to a full and adequate statement of the law, this number occurs in all the cells throughout the bodies of all the members of a particular species. This characteristic number is spoken of as the somatic or diploid number. In the history of the germ cells all the divisions of the multiplication period are found to have this characteristic number. During the maturation divisions, however, this number is halved, that is, reduction occurs, and the matured gametes have only half the number characteristic of the species. The union of the male and female gametes in fertilization effects a return to the somatic number. The process of reduction is often called meiosis and the divisions meiotic divisions. Commonly, although not at all of necessity, the first division is the reductional or heterotypic as distinguished from the somatic or homcotypic divisions. If the first is hcterotypic the second is homcotypic, and conversely.

In those cases in which the (lijfcrences between reductional and somatic mitoses are most clearly recognizable (that is, in those cases in which tctrads are formed), we may say that the explanation lies in two outstanding facts, namely, the peculiar prophase of the first division with its synaptic pairing of homologous chromosomes, and the entire absence of a prophase to the second division. The case of Ascaris, the roundworm, is one of the best known, and it may serve as an illustration of these processes. The somatic number of chromosomes in the common Ascaris is four. These are not looked upon as four separate and unrelated individual chromosomes, however, but as two pairs, for it has been shown in some animals that one member of each pair came from the male parent and one from the female in the preceding fertilization, and it is very probable that this is always the case. The members of a pair are spoken of as homologous chromosomes. Thus each individual derived from a fertilized egg contains in each of its cells two full sets of homologous chromosomes. This fact is to be contrasted with the well-substantiated observation that the germ eells contain but a single set of chromosomes owing to the process of reduction. It will be recalled that a typical mitotic division, whether in a germ cell or a somatic cell, involves in the prophase a condition which is really the climax of the entire set of mitotic events, namely the splitting of the spireme thread which is to condense to form the metaphase chromosomes. For this reason the metaphase chromosome may be looked upon as consisting of two halves, or chromatids, even if this condition sometimes is not easily seen under the microscope. That is to say, the ordinary chromosome is a. bivalent one, a dyad. With these facts in mind we are now ready to inquire into the nature of synapsis. fiG. 5. Fertilization and cleavage of Ascaris. (Redrawn from Kellicott after Bovcri.)

A, epermntozoon entering the egg as the second maturation division is taking plan-. B. pronuclei going into prophnso and division of sphere and centrosome beginning; C, I), showing further advance toward E, the first cleavage division. SYN APSIS 15

b. Synopsis. By synapsis is meant the union in the first maturation prophase of the two homologous members of each chromosome pair to form 3* Smgle chromosome; although one which has a valence of four, as

h‘ h’ h‘ h‘ fiG. 6. Diagram of tctr-ad formation and subsequent ro(lu('lion. (Suggested by diagrams from Sharp.)

a. chromosome conditions in spernmtogoniu and at beginning: of first maturation prophuse; I). synopsis in prophnse of first maturation prophnsc (first spernw.tot_vte), 0, tctrad-5 ready for the division; d. metaphnse of first niaturmitm division; 0. unaphuse of d; f. second spcrmntocytes produced by the division of e; g, division of second spermutocytes; h. resulting distribution of chromosomes as they go into the four spermatozoa.

contrasted with the preceding bivalent condition. Since two somatic chromosomes, each consisting of two chromatids, are involved in the formation of this new chromosome, it is called it tetrml. It is evident 16 THE GERM-CELL CYCLE

that by synapsis a reduction in the number of chromosomes, but not in the amount of chromatin, has been effected. It is the function of the two maturation divisions to complete this reduction in amount by distributing the four component parts of each tetrad to the four different spermatozoa,or, in the case of oogenesis, to the egg and the three polar bodies.

As a result of synapsis it appears that there are in each first spermatocyte or oocyte the reduced number of chromosomes in the form of tetrads, or quadrivalent chromosomes. Each tetrad consists of four chromatids, aa/bb’, two from each of the homologous mates, A and B. If, in the succeeding metaphases and anaphases, the bivalent chromosomes (dyads) which are the result of the division of the tetrad are each composed of two chromatids derived from the same one of the constituent synaptic mates, that is, a and a’ in one chromosome and b and b’ in the other, the division is said to be rcductional or heterotypic. In other words, in a reducing division whole chromosomes are separated. In this case the second division would be an equational division for the equivalent half chromosomes would necessarily be separated as in any ordinary mitosis. That is, the bivalent aa’ is now divided into a and a’ and bb’ into b and b’, and the maturation with the consequent distribution of the four parts of the tetrad to the four germ cells is completed. If, on the other hand, the bivalent chromosomes resulting from the division of the tetrads consist of half of each synaptic mate, that is a and b in one and a’ and b’ (or of course a and b’ or a’ and b may be linked together), then the first division is equational. The second division would then be reductional and as in the previous case would result in the distribution of the four component parts of the tetrad to the four matured germ cells.

In these cases in which tetrads are formed there is no resting stage preceding the second maturation division, but the dyads without a reorganization arrange themselves on the second spindle. There is a large number of cases, however, in which actual tetrads are not formed owing to the failure of the usual split of the spireme to appear during the early stages of the first division. In this case the first division is always reductional; there is a pause between the first and second divisions during which the chromosomes undergo seine reorganization; and the splitting which was delayed takes place. It is evident, therefore, that precisely the same result is achieved in the two cases, whether or not tetrad formation occurs. That is, there are formed from each spermatocyte or ooeyte of the first order four cells, each with half the number of chromosomes characteristic of the species. These four cells are mature spermatozoa or one functional egg and three polocytes or polar bodies. FERTILIZATION 17

3. Fertilization

It has already been pointed out that there are two totally different functions served by fertilization, namely, the one concerned with the hereditary mechanism in which the diploid number of chromosomes is restored, and the other which sets into operation those processes leading to cleavage and the further development of the embryo. The first of these functions is accomplished in the conjoining of the male and female pronuclei. The sperm with its reduced number of chromosomes enteis the egg, and its subsequent union with the female pronucleus which also contained the reduced number produces in the zygotic nucleus so formed the full number of chromosomes. The second function is accomplished in a very complicated series of processes of physico—(-hemical nature. Much of the research in experimental embryology of the last two (i(‘('£l.(l(‘s has dealt with the physico-chemical aspects of the activation of the egg,


he 7 Entrance of speimatozoon into egg of the starfish Astcruza glaL1u.[7..s. (Redraun from (‘onkhn after Fol )

and results have been obtained which have given real insight into the fundamental nature of the living organism.

The morphological aspect of fertilization is well known from the studies of Lillie on Nerezs, of Wilson on Toxopneustcs, of Kostaneeki and of Wierzejski on Physa, of Boveri on Ascarzs, and of many others. In most animals the entire sperm enters the egg, but there are many others, as in the sea—urchin and the staifish, in which the tail or at least most of it remains outside. The important elements of the sperm that enter the egg and have a function in fertilization are the head which is equivalent to the nucleus, the central body or the structures derived from it, the acrosome which is derived from the Golgi apparatus of the spermatid, and some chondriosome material. Of course the most important of these is the nucleus, but historically the central body also has been the subject of much discussion in connection with fertilization. The sperm enters rather largely through the activity of the cortical layer of the egg and by a. fairly definite path makes its way toward the egg pronucleus. Immediately upon entrance, however, it rotates so that the middle piece 18 THE GERM-CELL CYCLE

precedes in the advance to the female pronuc‘eus. The sperm aster appears from this region, and it is the usual condition that it should become the aster of the cleaving egg. It divides and forms the spindle

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a, mature spermatozooii, iii. traiisforination of speimatozooii into male pronucleus, {, female pronucleus

between the two approaching pronuclei. It is not the rule that the egg aster contributes to the formation of a cleavage spindle.

The entrance of the sperm occurs at different times with respect to the extrusion of the polar bodies in different eggs. At one extreme is the condition as found in the sea-urchin and in the coelenterates in which both maturation divisions are completed before the sperm can FERTI LIZATION 1 9

enter. At the other extreme is the Ascaris type in which the sperm enters the egg before either polar body has been extruded; in some cases it may be before the germinal vesicle has been broken down, in others while the first maturation mitosis is in the metaphase stage. Nematodes, fiatworms, molluscs, some annelids and crustaceans belong to the Ascaris type. There are of course intermediate stages between these two extremes.

The series of processes involved in fertilization may be said to be completed when the two pronuclei have closely approached each other and a cleavage spindle is formed between them. There is seldom an actual fusion of the pronuclei as such; rather they lie side by side upon the developing first cleavage spindle, and at the end of this first division the chromosomes of the components are intermingled and are no longer to be distinguished as from the two parents.

We are thus back at the stage from which we started and cleavage is the next step in ontogeny.

Brsuoonspnxc News

Among the more important accounts of the subjects contained in this chapter are the following: Wilson, Sharp, Kellicott, Cowdry. These works are cited in full in the bibliography on page 406.


Chapter III Egg and Cleavage Types

Of the four stages of embryonic development, cleavage, germ-layer formation, period of development of organs, and of histological differentiation, the period of cleavage is the most constantly recognizable and the most distinct. It consists of a succession of cell divisions taking place in a very regular manner and having for their purpose the distribution of the egg protoplasm into a great many single cells. Every organism above the protozoa consists of many cells, and every one starts as a single-celled egg. The first problem of development for the fertilized egg, therefore, is that of the regular distribution of its substance in such a manner that the organs of the later stages may normally arise from the appropriate material. Since divisions follow one another with considerable rapidity during cleavage the daughter cells never have time to grow to the size of the mother cell. The cleavage cells or blastomeres normally divide into two cells each, thus setting up a normal rhythm of 2, 4, 8, 16, 32 cells, etc. Even in the simplest cases, however, this rhythm cannot long persist, for with the beginning of differentiation processes certain cells lag behind in the divisions and irregularities thus come in.

Cleavage usually results in spherical blastomeres which are in contact only at the point where the cytoplasmic division last cut through. ()wing to the tension and other physical factors, this condition at once passes and the blastomeres come to lie closely pressed together with only a furrow remaining to show where the separation really is. The furrow naturally falls perpendicular to the spindle axis of the last division. Often the plane of the first furrow corresponds to the median plane of the future embryo.

This last fact, along with others which indicate that there are, at least on many eggs, structural features that link up the uncleaved egg with the future organs developing from its various special regions, raises the question of the promorphology of the ovum. This matter is correlated with the preformation discussion to which reference is made elsewhere. It is often possible to trace the origin of organs or cell groups to very early blastomeres or even to the single-cell stage, a study which is known as cell lineage, and there are often in the egg marks of structural

20 EGG AND CLEAVAGE TYPES 21

differences by which regional differentiation is indicated. The presence, for example, of yolk at the vegetative pole of the egg distinguishes the ectodermic and the endodermic portions at once. In ascidian eggs there are differences in the consistency of the protoplasm and in the pigments

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Fro. 9. The progress of the first cleavages of the snail, Planorbis, showing the manner in which the furrows out through forming two spherical blastomcres. which then draw together, substituting :1. plane of contact for the point of contact.

present, so that with the entrance of the sperm there can be distinguished four regions, namely, a clear protoplasmic cap at the animal pole, a darker area at the vegetative, and in between two crescents, one yellow and one light gray. There are thus localized certain organ-forming sub22 EGG AND CLEAVAGE TYPES

stances in four different regions, and these will give rise to very different parts of the embryo. For these reasons we say that there exists in the eggs of many species a predelineation of the structures which are to be developed. This is of course contrary to the assertion sometimes made that the blastornere is similar to the entire egg, is a small picture of the whole. This statement is true only in the sense that the egg commonly shows little evidence of histological differentiation, and the same is at least superficially true of the early blastomercs. That the resemblance is only superficial, however, is also borne out by the nuclei of certain forms. In Ascaris one of the two nuclei of the 2—cell stage undergoes a process known as chromatin diminution, becomes smaller, and stains more lightly than the other; this is indicative of the separation of the germ line from the soma.

As cleavage progresses the tension which keeps the entire protoplasmic mass nearly spherical imparts to the individual cells a tendency to approach each other and press together. Largely owing to this tendency the blastomeres arrange themselves at the periphery of the mass and leave a cavity at the center, known variously as a cleavage cavity, segmentation cavity, blastocoele, or primary body cavity. It is filled with fluid or with a gelatinous secretion. In eggs containing large amounts of yolk, however, the cavity is crowded out of the center and often greatly restricted by this deutoplasmic accumulation. The cellular surface of the embryo at this stage is known as a blastoderm, whether it involves the entire surface or is limited to a small area of it.

Cleavage may be said to begin with the formation of the first segmentation spindle. This is a more accurate statement than that it follows fertilization, for in the case of eggs which develop parthenogenetically there is of course no fertilization. It is more difficult to say when it closes, for any limit which we may set has only relative value. Although some cases do not conform, it may be said that the end of cleavage is reached with the establishment of a definite size relation between nucleus and cytoplasm (the nucleo-cytoplasmic ratio), the particular ratio being that which is normal for that particular stage of that particular species. It is of course to be noted that where differentiations due to yolk, etc., are present there cannot be a single nucleo—cytoplasmic ratio for an entire embryo. It is perhaps better to say that cleavage is ended when a typical blastula is formed consisting of the first primary genn layer with the cells arranged in an epithelial layer.

It must be borne in mind by the analytical student of developmental phenomena. that three distinct kinds of processes are involved in the transformation of the egg into a larva. These are cell division, growth, and difi‘erentia.tion—processes which are not only distinct, but to a certain extent antagonistic, the last two never taking place at the same CLASSIfiCATION OF EGG TYPES 23

time with the first, and only to a minor extent together. (Differentiation is here used in the sense of histological differentiation, for of course in another sense its processes take place by means of cell divisions.) We may regard the actual growth processes, that is, increase in bulk, as anabolic, and obviously cell division is largely katabolic, from which it follows that the two cannot take place as dominant factors in the same cell at one time. Their independence in this relation does not mean, however, that they are not dependent on each other, for if they do not maintain their proper balance further development on the part of the organism as a whole cannot occur.

Before discussing the types of cleavage it should be pointed out that development is possible in some cases without regular cleavage. This really amounts to a delay in cell division as contrasted with nuclear division. Several nuclear divisions take place in succession without the cleavage of the cell body; at a later stage the cell areas are cut off around the nuclei all at one time. Examples of such development are found in the alcyonarian Clavularia (Kowalevsky and Marion), Ii’em'lla (Wilson), Alcyonium (Hickson), Tealia (Appellof), and Cucumaria glacialis (Mortensen).

It should also be made clear that a classification of cleavage types has nothing of the evolutionary significance which the systematic grouping of animals has, nor can it be made a basis for systematic classification. Although cleavage types are in general stable and are coextensive with certain animal groups, yet there are very notable departures in this regard. It will be seen by an inspection of the table below that the cephalopods have a different type of cleavage from other molluscs, that the scorpions cleave differently from others of their class, and that many other exceptions also exist. Indeed, there are instances in which nearly related species have different methods of cleavage, and the extreme modification of this sort is perhaps seen where two types of cleavage occur in the very same species. An example of this last case is seen in Polyphemus oculus, whose summer eggs undergo regular holoblastie cleavage, whereas in the winter eggs a type of Ineroblastic cleavage occurs which strongly suggests conditions found in the superficial cleavage of some insect eggs. These are, of course, extreme cases which merely serve to show how variable cleavage forms may be, doubtless as adaptive responses to the conditions of development, without having any special phylogenetic or taxonomic significance.

1. Classification of Egg Types

On the basis of their structure, particularly as modified by the amount of yolk present, Balfour divided eggs into three groups, alecithal, telolecithal, and centrolecithal. 24 EGG AND CLEAVAGE TYPES

Alecithal, or better homolecithal, eggs (also called isolecithal) are those in which there is relatively a small amount of deutoplasmic material uniformly distributed throughout the egg. Such eggs cleave regularly into equal-sized blastomeres. Echinoderm eggs are examples.

Telolecz'thal’eggs have a clear axial structure, the protoplasm at the animal pole containing very little yolk, while the vegetative half of the egg is rich in yolk. The frog egg may be taken as an example. The blastomeres at the vegetal pole, therefore, are distinctly larger by reason of their large yolk content, and the cleavage cavity is pushed toward the animal pole. Such eggs necessarily have unequal cleavage, if the furrows are able to cleave the yolk at all.

In another type of telolecithal eggs the accumulation of yolk is so great that it cannot undergo cleavage. The protoplasm is thus limited by the yolk to a small disc at one pole of the egg while the yolk fills the rest of the space. The eggs of birds and of teleost fishes furnish excellent examples. When cleavage takes place it cuts through the disc only, and is therefore discoidal.

Telolecithal eggs are thus of two sorts: holoblastic, those in which the entire egg cleaves, although unequally; and meroblastic, in which only part of the egg mass can be divided, and that by either discoidal or superficial cleavage. The terms “partial” and “total” cleavage also apply to these types. Between these two types there are of course intermediate conditions shown by various eggs. These two extremes lead to two types of embryo formation; in the holoblastic egg the entire egg goes to form the embryo body, but in the meroblastic type the germ disc is all that is involved, and the yolk is in the form of an appendage, the yolk sac.

Centrolecithal eggs are richly yolk laden. The cleavage nucleus in a cytoplasmic area is located at the center of the egg surrounded by the yolk. A protoplasmic layer, however, covers the surface and is connected to the central mass by fine plasmic threads. Some centrolecithal eggs are so definitely oriented that the position in which they are laid indicates exactly the axes of the future embryo, but in general the primary axes are not well developed in eggs of this type, although bilaterality is to be noted. Cleavage begins by the plasma island in the center multiplying through several nuclear divisions, thus forming a syncytium. These “blastomeres” now move radially toward the periphery and unite with the plasma layer which is at once cut up into cytoplasmic areas of similar size, each supplied with a nucleus. The central yolk does not divide, or if division starts it is incomplete. This constitutes superficial cleavage, the blastoderm forming about the yolk which fills entirely the cleavage cavity (if one might use that expression). CLASSIfiCATION OF CLEAVAGE TYPES 25

2. Classification of Cleavage Types

Dependent upon the amount of yolk they contain, the first divisions of eggs are total or partial. Eggs having total cleavage are said to be holoblastic; those having partial cleavage are meroblastic. It is also customary to classify types upon the basis of the planes of symmetry which

EGG GERM C LEAVAG E STRUCTURE CLEAVAGE FORMATION TYPEs EXAMPLES

Porifera 1. Rmlial Cnidaria Echinoderma

Equal 2. Disymmetrical Ctenophorcs

Nematodes Rotifers Homolocithal Holoblast ic Ascidians

3. Bilateral Amphioxus Petromyzontidae Amphibia Incquul Higher mammals

Polyclads Nemertcans

[4, Spiral Annelids and moll11.~cs(ox<'(-pt(~(-pl1'l‘eloleci1lml alopods)

Scorpion Cephalopods Pyrosomcs

[ ‘ Myxinoids

[ Discoidal Elasmobranchs T eleosts Gymnophionans Reptiles

Birds Monotremes

5. Discoidal

Meroblastic

Arthropoda (except scorpions) Controlecitlml Superficial U}. Superficial Someotherscattered ' forms among coelenterates 26 EGG AND CLEAVAGE TYPES

are to be observed in the dividing egg. Thus in radial cleavage there is uniform distribution around the egg axis, but in disymmetrical cleavage there are two centers of symmetry, and in bilateral cleavage a single plane only will cut the egg in equal halves. In spiral cleavage the plane of the spindle"in the first divisions turns in a spiral with reference to the egg axis. These four cleavage types are holoblastic. Meroblastic eggs may be divided into superficial and discoidal. In the former case the blastodisc forms around the outside of the egg but involves practically the entire surface whereas in the latter only a small disc undergoes segmentation, owing to the extensive amount of yolk present. These relationships are shown by the accompanying table as are the animal groups to which they belong» We shall consider these types in order.

3. Classification on the Basis of Predelineation

Before considering the details of these different modes of cleavage it is desirable to mention certain qualities of eggs by which they are related to the later developing stages. With reference to the degree of predelineation shown, Conklin has recognized two types of eggs as follows:

a. Eggs with Determinative Cleavage. The best examples are the eggs of annelids, mo1‘uscs (except the cephalopods), and the ascidians. In eggs of these groups after fertilization, but before cleavage, there can be recognized in the one-cell stages regions or definite areas in the egg protoplasm, the organ-forming regions of His. These regions are distinguishable in various eggs by different means, among which are differences in yolk content, presence or absence of pigment, clear or granular condition of the cytoplasm, and the presence of very fine granules which can be demonstrated by definite staining methods. The centrifuge has also proved useful in detecting different substances in the egg which as cleavage advances become segregated into different blastorneres. (Cf. the work of Lyon, Lillie, Conklin, etc.) The study of the cell lineage of such an egg shows that these blastomeres are the beginnings of definite organs of the embryo. In other words the egg substances which are thus localized into regions are determined for the production of definite organs of the later stages. During the progress of the investigations which established the determinative character of certain eggs there was a great deal of discussion, and even controversy, as to whether blastemeres were totipotent, that is, interchangeable, or constituted a mosaic work, each being capable of taking only its own special place. We now understand that eggs which have determinative cleavage have an operative mechanism of great precision, and that correspondingly they have lost much of their power of regulation. Because of their content of organforming substances they are apparently destined for a particular fate, EGGS WITH IN DETERMINATE CLEAVAGE 27

and can undergo very little regulation. These statements of fact for determinative eggs do not apply to eggs of the next type.

b. Eggs with Indeterminate Cleavage. The problem of determination, after all, is a problem of differentiation. In eggs of this indeterminative type differentiation sets in only relatively late after the embryo consists of many cells. In the preceding case the marks of differentiation are recognizable from the very first. In indeterminative eggs, there are no orgamforming regions, little histological differentiation is found, and the blastomeres appear to be alike. Such eggs are simple in structure and are accompanied by high capacity for regulation. Examples are: vertebrates, some insects, most arthropods, cephalopods, most eehinoderms. In them the power of regulation is much greater than in the determinative type, and there is much evidence to indicate that the fate of a blastomere is often a function of its position, or that the blastomeres are totipotent and without special “prospective significance.” In Part Two the chapter on the determination problem gives the evidence in more detail.

BIBLIOGRAPHIC N OTE

Among the more important accounts of the subjects contained in this chapter are the following: Korsehelt and Heider, Conklin. Morgan in “Experimental Embryology,” Cowdry’s “General Cytology” (especially the article by Conklin on "Cellular Difierentiation”). These works are cited in full in the bibliography on page 406.


Chapter IV Holoblastic Types of Cleavage

I. RADIAL CLEAVAGE

The eggs of the Porifera, of all the coelenterates, except the ctenophores, and of the echinoderrns have radial cleavage. Formerly amphioxus was given as a type of this class, but it has been shown that the older accounts were in error, and that its cleavage is really bilateral.

@I 83%?

flu. 10. The vleiivage of sea cucumber Synapta dig/Lluta. (Redrawn from horsehclt and Heider after Selcnka.)

A. 2-cell stage; B, polar View of 4-cell stage; C, D, lateral views of 8- and 16—cell stages.

Radial cleavage includes eggs of both homolecithal and teloleeithal types, although of the latter of course only those which have holoblastie cleavage belong here. In the typical and simple cases such as that of Synapta (which as described by Selenka may be taken as most nearly

corresponding to the ideal form of radial cleavage), the division planes 28 RADIAL CLEAVAGE 29

succeed each other in regular alternation dividing the egg first meridionally and then equatorially into equal blastomeres. It very nearly cor— responds to the Sachs’ principle of the alternation at right angles of successive planes of cell division. The first furrow is meridional and divides the egg equally. The second furrow is also meridional and

1 It: 11 Continuation of fig 10 32-, 64-, and 128-cell st Lges of S:/napta dmztata

divides each of the first two blastomeres equally. The third furrow is equatorial and the blastomeres are equal, making eight cells arranged in two rows about the two poles. By this time a tiny cavity is discoverable at the center of the mass which is to become the cleavage cavity or blastocoele. The furrows of the next cleavage are meridional but at an angle of 45 degrees to the first and second. The furrows of the fifth are again latitudinal, dividing all the blastomeres equally. Subsequently the divisions keep their regular alternation for a period, forming a blastula 30 HOLOBLASTIC TYPES OF CLEAVAGE

in which the cells are arranged in horizontal and vertical rows. With 2 shift of the blastomeres about the pole by which the opening there is closed, a spherical blastula consisting of a single layer of cells (a typical coeloblastula) is formed.

The cleavage of many jellyfishes, though in general radial, undergoes many modifications due to yolk distribution, loose arrangement of cells, and to other factors.

Radial cleavage undergoes some interesting modifications in some of the sea-urchins, notably Strongylocentrotus lividus, as shown by Boveri (1901). In this form cleavage is unequal and differential. The egg is of a clearly determinative type, a jelly canal indicating the position in which the polar bodies will be given Off. It is the place at which, in the oocyte stage, there is uniformly distributed an orange—yellow pigment which, upon fertilization of the egg, at once rearranges itself as a band about the lower half of the egg, leaving a cap without pigment about the vegetal pole. This cap is destined to produce in subsequent cleavages small cells known as inicromcres, a phenomenon which in itself is striking since in most eggs the cells at the vegetative pole are commonly larger than those of the animal half. The egg nucleus is not limited to the animal half of the egg, nor is the spermatozoon restricted to the jelly canal.

The first two cleavages are meridional and equal, resulting in foul blastomeres which receive equal amounts of the three kinds of egg materials, the pigment—free animal half, the pigment zone, and the clear polar cap. With the next cleavage which is nearly equal (latitudinal) the four animal blastomeres receive but a small portion of the pigment, the remainder being in the four blastomeres of the vegetal half of the egg. Now follows a peculiar differential cleavage, the upper four cells dividing meridionally while the lower four are unequally divided latitudinally. This results in the immediate segregation of the pigment-free cap into four vegetative cells, the micromeres. The descendants of these are later to form the primary mesoderm.

In producing the next stage (32 cells) the eight cells of the animal half (mesomeres) divide equally and latitudinally producing two wreaths of eight cells each. The four larger pigmented macromcres divide meridionally, and the four micromeres of the unpigmented cap latitudina.lly and unequally. Subsequent divisions tend to equalize the size differences and the blastula is regular and consists of equal—sized cells, but from the substance of the mesomeres comes the ectoderm, except that of the lower pigmented area which is contributed to the secondary mesoderm; from the macromeres come the endoderm and secondary mesoderm; and the primary mesoderm is from the micromeres. fiG 1! (‘tonvage of sea.-urchm Strormylorerwrotm (Rcdnuvn from Korschelt and Hmder after Boven )

Lateral vlesw shmx 1212. Lhe three zones and their dxsmbutxon 1n the blastomerea 32 HOLOBLASTIC TYPES OF CLEAVAGE

II. DISYMMETRICAL CLEAVAGE

The ctenophores are the sole representatives of the disymmetrical type of cleavage, and to the average student of embryology the fact 

3 F

fiG. 13. Cleavage of Baron. (Rcdruwn from Korsclu-It and Heidcr after Zoigler.)

A. second division. The vegetative pole is the upper, as in other figure showing lateral view; B. 4-cell stage; C, 8-cell stage from animal pole, as, median plane; bl), transverse plane; D. same from lateral view; E, F, 16—cell stages from animal pole and from side View respectively.

that they constitute a remarkable exception to the general rules is their greatest interest. Although the peculiarities of these forms early stimulated a great deal of investigation, Ziegler’s findings (1898) form the basis of our present understanding of this type of development. DISYMMETRICAL CLEAVAGE 33

The eggs of ctenophores have an ectoplasmic surface layer and an inner vaeuolated yolk mass; the nucleus lies in the ectoplasm near the vegetative pole of the egg where the polar bodies are given off (Hatschek). In no other case in the animal kingdom is this type of egg organization found. The first and second cleavage furrows begin at the vegetative pole, advancing meridionally to the animal pole, dividing the egg equally. The first furrow corresponds to the median plane of the adult and the second to a plane connecting the two long tentacles; each blastomere is therefore one-fourth (one quadrant) of the body.

The third division is spoken of as diagonal. It runs obliquely from near the animal pole to the lateral part of the vegetative half of the egg,


Fm. 14. A, continuation of fig. 13. 40~('ell stage of Iftrut; B, g.-1-«it|ul.r of ('ulluum4L bialnta. (After Metelmlkoff.)

er. outer cells, eetoderm; en. large inner cells, endoderni; in. small inner cells, niesoderm

giving rise to a curved plate of eight cells of which the four larger middle ones are called submedian and the four somewhat smaller ones are the subtentacular cells. This curved plate, concave on the animal side, is thus divided symmetrically in two directions, but is elongated in the tentacle plane, thus giving the impression that there are two centers of symmetry, one in each half, right and left, of the embryo. This impression is accentuated in the next stage in which eight micromeres in two distinct groups are given off on the concave side (animal half) of the embryo. The 32-cell stage is reached as each of the eight macromeres gives off another micromere and each of the old micromeres divides. The micromeres of the submedian octants divide equally, those of the subtentacular ones very unequally.

By subsequent divisions the micromeres come to form an ectodermal cap which gradually grows over the macromeres. now increased to 16. 34 IIOLOBLASTIC TYPES OF CLEAVAGE

The cap of ectomeres closes up late at the animal pole, a point at whit.-. the sense organ later develops. In the formation of the eetodermal cap of micromeres gastrulation is accomplished and the endoderm is marked off from the eetoderm. Endoderm formation in the animal kingdom may be accomplished by several methods which are described in Chapter VII. Although invagination is the most common of these methods it is by no means a necessary process in endoderm formation. In this case it plays no part at all, for the large maeromeres that are the primordia of the endoderni are simply overgrown by the micromeres. This process is known as epiboly. The epibolic gastrula of Callianira is shown in fig. 14B. For further details in the development of ctenophores the student is referred to the descriptions of Ziegler, Metchnikoff, and others.

III. BILATERAL CLEAVAGE

Bilateral cleavage is so called because of a bilateral arrangement of the egg substances which is very often recognizable before cleavage, indeed before fertilization in some cases, and certainly early in cleavage. Examples include rotifers, nematodes. and those vertebrates which have holoblastic cleavage. Thus it occurs in eggs which belong to homolecithal and to holoblastic teloleeithal types, and either equal or decidedly unequal cleavage may result. It will be recalled that telolecithal eggs may have holoblastic or meroblastic cleavage depending on the degree in which the yolk mass forces the cytoplasm to be localized on one side. In the extreme cases discoidal cleavage results, which is thus related to the bilateral types. On the other hand it will later appear that the discoidal type is also related to the superficial type.

1 . Amphioxus

As a first type amphioxus may be chosen. It was formerly the custom to class amphioxus as of the radial type. This is perhaps to be ascribed to the fact that there is some variability in the behavior of different eggs. Cerfontaine carefully restudied the case, however (1906), and found that in the majority of cases the following description holds true. Since his work, nevertheless, it should perhaps be pointed out, as Dean has done, that the cleavage of amphioxus may be polymorphic, that is, in one case radial and in another bilateral.

The egg of amphioxus is clearly bilateral in structure before cleavage. The animal pole is marked by the second polar body, the first being given off before the formation of the vitelline membrane and so lost. It is said that the animal pole is the point of attachment of the oocyte to the germinal epithelium. If the egg is oriented according to the planes of the future embryo the animal pole is found to be in the center of the AMI’HI()XI'S 35

antcro-ventral iegion and the vegetal in that of the postei'o—dorsu.l. In the anterior half of the egg may be distinguished a clear mass of yolk-free cytoplasm, in which the nucleus lies, although part of this mass extends a little into the posterior half on the ventral side; most of the cytoplasm of the posterior half of the egg is well filled with yolk globules. Yolk granules also are found in the animal half outside the clear cytoplasmic area. The distinction of yolk-free and yolk-laden halves of the egg is indicative of its bilateral symmetry. The telolecithal character of the egg is peculiar in that the yolk mass is not only in the vegetative half, but toward the


Tie 15 Median section through egg of amphioxus arranged to show relation of egg AXIS to future orientation of body (After (‘erfoiit.iine)

.in -\ egg ‘LXIS terniiimtiiig in the two poles, A, P l), V, the future dlll(‘l‘10I‘, posterior, dors ll and Ventral I‘('§Il01I\ of the egg

posterior end. The first furrow is meridional and corresponds to the median plane, dividing the egg into right and left halves. The second furrow is meridional, but slightly unequal blastoineres are separated by it. The antero-dorsal are the smaller. The third furrow is latitudinal, cutting off four micromeres at the animal pole. Owing to the inequality of the 4-cell stage there are really four pairs of cells of different sizes in the 8-cell stage.

The 16-cell stage is not reached by meridional furrows as is to be expected. The four micromeres each divide by a furrow more or less at right angles to the median plane, and the four macromei-es by a parallel 36 HOLOBLASTIC TYPES OF CLEAVAGE

furrow. Thus there arise two plates of eight cells each, those of the animal half curving from front to back, while the others curve from right to left.

From this stage on, development becomes irregular, and characteristic differentlations appear. The typical coeloblastula characteristic of

P10. 16 Cleavage of amphioxus (Redrawn from Korschelt and Herder, after Cerfontame)

A, second cleavage, B, 4—cell stage from left side C, D, 8-cell stage from side view and from animal pole

amphioxus is formed with smaller ectoderm—producing cells at the animal pole and the larger endoderm-forming ones at the vegetative. By invagination, epiboly, and involution the gastrula is formed.

2. Ascidians

The bilateral cleavage of the ascidians has been studied by many embryologists, but Conklin’s work on Cynthza, Cwna, and Mogula IS E f 16-cell stage 111 left sxde

0 um 3. mm. H mm nb EC Lu BM mh aL .0. E] S e V 1 6|.‘ 8 38 HOLOBLASTIC TYPES OF CLEAVAGE

probably the most complete. These eggs have typical determinative cleavage, with definite orrgamforming regions which are recognizable by «color difference of the cytoplasm.

The newly extruded egg surrounded by a layer of test has a conical layer of texoplasm in which is uniformly distributed a yellow pigment. Soon after fertilization the polar bodies are given off and peculiar rearrangements of substance take place. About five minutes after fertiliza


F

fiG. 15. The egg of Cynthia partzta. (After Conklm.)

A. unfertilized em: with germinal vesicle, central gray yolk 111.158, peripheral yellow protoplasm, and test cells; B, five minutes after fertilization showing streaming of yellow protoplasm to vegetative pole; (‘, streaming of yellow protoplasm nearly completed, clear protoplasm lies beneath it and is visible at its upper edge. On the top of the cm: the germinal vesicle is still seen; D, the light creseentic area at the vegetative pole represents the male pronueleus; the unstippled area is the gray central yolk mass of A; E, polyspermic egg: F. formation of yellow crescent (heavily stippled) with the light gray trescent above it.

tion the yellow pigment, mesoplasm, may be seen streaming toward the vegetal pole, leaving behind the gray yolk mass, endoplasm, which fills most of the cytoplasm of the egg. The yellow mesoplasm arranges itself in a crescent in the posterior half and will, later in development, give rise to mesoderm. The large germinal vesicle contains material in addition to that which goes to form the cleavage nucleus, which is liberated at the time of formation of the maturation spindle. This material, the clear protoplasm, is the ectoplasm of the fertilized egg; it shifts its position to lie in a clear gray crescent next to the yellow crescent but on the side of Ab(.‘lDlAl\h .39)

the animal pole. It IS the neurochordal anlage (or fundainent from which will arise the neural canal and notochord). The animal pole is suiirounded by ectoplasm from which ectoderm arises, and the vegetative Iby endoplasm producing endoderm.

The first division, a meridional one, divides the egg and likewise each of the oigan-foiming rogiorns into «two equal halves Since tliere is but a

fiG 10 A, continuation of fig 18 B, showing aggregriiion of test cells over the crescent and the protrusion of the ehorion, (‘, 2-cell stage with formative substances outlined Uniform stipples, volk, light stipples, clear protoplisni eiilarged and extended toward the animal pole, grouped stipples, yellow crescent m Lterial

single plane which can do this it is evident that the cleavage is bilateral in character. The separation of the egg substance into organ—forming regions, which had started during the first cleavage, is completed now, although it must be recognized that it is never as sharp as the boundaries of the regions shown in_the usual diagrams. It is not possible, however, that living protoplasms could be entirely and sharply separated from each other while in a single cell. Indeed, we may regard the process of 40 HOLOBLASTIC TYPES OF CLEAVAGE

cleavage as having the especial function of distributing these substances into the appropriate cells.

The second division is meridional and displays the beginning of inequality. The orientation of the ascidian egg is similar to that of amphioxus. Therefore, two antero-dorsal cells are separated by this division from two postero—ventral ones. It is customary to designate the anterior cells by the letter A and the posterior by the letter B. In each case the right blastomere is indicated by underlining the letter

fiG. 20. Cleavage of Cynthia (Redmwn from Korschclt and H0|dOf, after Conklm )

A. 4-cell stage from left side, B, from animal pole, C‘, 8-coll stage from left side, I), from animal pole.

as 51} or E‘. The exponent 3 indicates that this is the third cell generation, counting the single-celled egg as 1. The division of A3 results in two blastomeres which are designated A‘ 1 and A4 2. The exponent 4 indicates the fourth cell generation, and the 1 or 2 after the period shows that it is the first or second cell from the vegetal pole. These principles of nomenclature are used throughout the cell lineage of the ascidian.

The third division is somewhat unequal and latitudinal, resulting in 4 cells of the animal half of the embryo (a”, b‘ 2, g4-2, lg‘-2) which are smaller than the corresponding ones of the vegetative half (A44, 51“, B‘ 1, Q‘ ‘). Due to a shift in the position of the spindles of the animal ASCIDIANS 41

half which converge toward the plane, the nuclei of a4 7 and Q” lie nearer to each other than do those of A4-7 and 44'”. We may take the A or the anterior half of the embryo as the type; the cells of the posterior half are to be regarded similarly.

The next division is therefore not strictly meridional as is to be expected. The spindles of the small animal cells (a‘‘-‘’, 9”) lie nearly parallel to the median plane, but those of the broader animal cells are more transversely placed. Thereupon the cells 115-3 and a5-4 seem to be behind each other, while 125-3 an(l I)“ are side by side. In the vegetative half the converse relations hold: A“ and A7’-7 lie side by side and B5-7


A B C fiG. ‘.21. Later stages of ('ymhia cleavage. (Redrawn from Korschelt and Heider, after Conklin.)

A, the fourth cleavage seen from animal pole; B, vegetative half of embryo in 32-cell stage; C. same in 64-cell stage.

A7 7, A7 7, B7 7, B7 7, are pure endoderm cells; A“ 7, A“ ‘, are cells of neuroehnrda anlage; B“ 7, B“ -'5, B" 4, mesoderm crescent; A7 G, A7 7, go to form the notochord; A7 '7. A7 ‘. form hinder part of neural plate. A7 " contains gray yolk (endoderm), but it eonmins material uhieh will be segregated as mesenehyme. B7 ‘, is muscle forming; B7 3 mesem-hyme. In each case the symmetrical mates of the left side have a similar fate.

and B5-7 lie behind one another. B” and half of B5-7 are the material from the yellow crescent. The left half is similar.

From here on all the cells of the animal half produce only eetoderm cells. The cells of the vegetative half are more diversely differentiated. B“-7 and Q“-7 consist only of yellow protoplasm and are purely mesodermal; A”, A“, and B“ with their mates of the right side are almost purely endodermal. The neurochordal cells A“ and A“ lie next to them anteriorly, and the crescentie mesoderm anlage, B”, B”, and B“, behind.

From this it will be seen without going into further details that the cleavage of the ascidians is a very good example of the determinative type. Thus organ-forming regions are definitely localized during the maturation and fertilization processes and by the process of cleavage 42 H()L()BLAS'l‘IC TYPES OF CLII«‘.AV.A'(:I«:

are segregated into definite cells from wvlficln arcise the organs of the lafterfembryo in the characteristic ascidian manner.

I 2 3 4 5 ‘5 Result U7) W0) W9) ‘K 19) ‘( 32*) l( 54» an I 3" ' ectoderm an A: A“ A‘-4 neurochordal A” endodermal , At! A” A” neurochordal A A‘-‘ endodermal ‘ an _¢_i_” { ectoderm 55.3 As — A53 33-4 neurochordal _ A‘-9 endodermal A4 I A“ A“ neurochordal Egg — A‘-‘ endodermal b5.4 b” { ectoderm has 33 35-! BM mesoder Be 3 m 34.1 B“ B‘-2 yellow protoplasm—mesodermal B B54 endodermal bu L‘-" { } ectoderm has is 5 4 .13.” %6'3 } mesoderm B4 1 -‘ B5‘, §__‘-’ yellow protoplasm " B“ endodermal

CELL LINEAGE OF CYNTHIA FROM DESCRIPTION OF CONKLIN

3. Vertebrates

The cleavage of the vertebrates is not usually of a determinative character as is that of the ascidians, and there are many variations in the characters it presents throughout the different groups. In general, however, they may all be referred to the bilateral type or derived from it, although the very considerable amounts of yolk present in the teloVER'1‘EBRA'l‘ES 43

lecithal eggs bring about important modifications in the modes of cleavage. This account leaves out of consideration the cleavage of mammals which is modified in an extreme manner in spite of the lack eofiyolk. Several groups of vertebrates have discoidal cleavage; this type,

fiG. ‘.32. Cleavage of the frog egg. A, B. C, D, 2-. 4-. 8-. 32—eell stages; E. lutor cleavage stage: 1“. dorsal lip of blastopore; G. circular blastoporc.

however, is joined to the holoblastic egg types by many transitional stages and types.

All amphibia have total, unequal cleavage in correlation with the telolecithal type of egg structure which characterizes this group. The egg of the frog has been studied by many investigators and may be taken as an example of holoblastic cleavage in the vertebrates. A dark 44 HOLOBLASTIC TYPES OF CLEAVAGE

brown or blackish pigment distinguishes the animal from the vegetative portions of the egg. About the vegetative pole extending perhaps onethird upwards is a white region which contains the material that will later go to form the endoderm.

In some form of amphibians, as of other groups, it is impossible to relate the cleavage planes to the later axes of symmetry of the embryo or larva. In other forms the bilateral arrangement of the blastomeres is unmistakable.


fiG 23 Cleavage of the frog egg seen from the animal or pigmented pole A. B, C. 4-, 8-, 32-cell stages

In the frog there is considerable variation as to the relations of the cleavage planes. Brachet found in 48 per cent of the cases which he observed that the first cleavage plane and the median plane coincided; in another 20 per cent the deviation was not more than 20 degrees. However, the bilaterality of the egg may often be shown to be independent of the cleavage figures. In certain amphibian eggs it has been shown that there is present in both fertilized and unfertilized eggs a bilateral arrangement of part of the egg substance, the so-called “gray crescent,” which appears at the edge of the white part of the egg against the dark portion, recalling the condition in ascidians.

The first cleavage divides the egg meridionally, the formation of the VER’l‘EBRA'l‘ES 45

furrow beginning at the animal pole and extending to the vegetal pole. The second is similar to the first but at right angles to it. The third cleavage is latitudinal and the blastomeres resulting form two circlets, one of four large cells and the other of four smaller. The fourth cleavages are meridional again. In later cleavages the yolk in the vegetative region causes a retardation in the rate of division so that the animal cells become much more numerous. In the fifth and sixth cleavages only the small

fiG. 24. Sections through blastulue up to the beginning of gastrulation in the frog“; egg. (B, (‘, D, after Ziegler) These show the clmracter of the octoderm and endoderm cells, the nature of the blastoeoelc, and the first sign of gastrular invagmation.

upper cirelets of cells are divided and even in those disturbances in the pattern of the blastomeres shortly appear. No longer is the wreath-like arrangement of the cells maintained and they become relatively smaller and much more numerous as compared with the large yolk-laden cells of the vegetal region.

The cleavage cavity which may be discerned in the 8-cell stage is smaller than that of almphioxus or the ascidian and is pushed toward the animal pole by the larger yolk cells. It gradually becomes more 46 HOLOBLASTIC TYPES OF CLEAVAGE

extended laterally, but in places it is reduced to a mere slit as development proceeds. When the fully formed blastula is reached in the frog, a difference, which is characteristic between vertebrates and invertebrates, becomes apparent in that the wall consists of many cells. In the invertebrates the octoderm and later the endoderm consist of a single layer of columnar or cuboidal epithelium, but in the vertebrates these germ layers are of several cells in thickness and many of the cells do not lie in contact with either the outer or inner surface.

4. Nematodes

The cleavage of nematodes may be illustrated by reference to the development of Ascaris worked out by Boveri; a number of other investigators have worked on other forms and have shown that they are in agreement with the Ascaris type.

The egg is small and practically yolk—free, and no evidences of differentiation are visible in the uncleaved egg, nor of relation between cleavage planes and polar bodies, but as soon as the 4-cell condition is reached the orientation is complete. In addition, however, to the differentiation which is expressed in the. orientation of the 4-cell stage, another mark of differentiation is evident in the nuclear processes. This is the chromatin diminution which occurs in the cells which are somatic in character, and is lacking in the prospective germ cell line, that is, in P1, P2, P3, P4, and G and G1.

The first cleavage plane results in the formation of two cells somewhat unequal. Of these the larger is designated as S1 01' AB and the smaller as P1. S, is shown by its subsequent development to contain only material which is to be distributed to somatic cells, while the P1 contains materials which will contribute to both soma and germ plasm. The next cleavage planes are not parallel to each other, for the spindle of the AB cell lies parallel to the first division plane, but that of the P1 cell is perpendicular to it. Thus there arises a T-shaped figure, the top being formed by the cells A and B and the stem at first by P1, which divides more slowly than the S1 cell, and later by the derivatives, cells S2 and Pa. Subsequently the P2 cell shifts posteriorly so that it comes to lie in contact with both S2 and B, forming a rhomboidal figure.

Now the bilateral character of the embryo becomes apparent. The cells A and B are dorsal, A being anterior; S2 and P2 are ventral, 83 being anterior. The dorsal cells now divide somewhat ahead of the ventral by a plane of cleavage which lies in the median line; A thus divides into a on the right side and 0: on the left, and B into b and 6. The embryo for a brief time, therefore, is in a 6-celled condition, but the division of the two ventral cells follows shortly, the planes of diviNEMATODES 47

sion lying perpendicular to the median plane. The 8-cell stage, therefore, consists of 9. plate of four dorsal ectomeres (two right and two left) and

flu. 2.3. (‘leuvage of Ascaris ntcgalocephala. (Rt.-drawn from Korschelt and Heider after Bovcri.)

A. 2-coll stage with spindles for the third cleavage; S; which equals AB is the first somatic cell and P1 is the blnstomoro from which the germ line will be segregated (stem cell); B. C‘, D, 4-celled stages showing in B the characteristic T-form resulting from the spindle directions of the second cleavage in C the Pa cell swinging around to form the characteristic rhomboidnl figure of the 4—cell stage. P2 is the stem cell.

8. row of four ventral cells slightly curved. S2 (EM St) divides into M St and E, the former being the anlage of mesoderm and stomodaeum and the latter that of the primitive endoderm. P2 divides into S3, an ecto48 HOLOBLASTIC TYPES OF CLEAVAGE

mesoderm cell, and P3, a continuation of the germ line. In this 8-cell stage the cleavage cavity makes its first appearance.

While the cleavage processes are taking place in Ascaris as described they are accompanied by nuclear changes of a character which has occasioned much study and discussion. In certain of the cells there occurs a process known as chromatin diminution by means of which

flu. 26. Continuation of fig. 25.

A. 6-cell stage. Blastomcres A and B divided into a and a. and b and Li; B. 7-cell stage I’2 having divided into Pa and S3. A and B are seen from the right side; C‘, seen from the dorsal side; D, 8-cell stage. S2 having divided into E and MSt.

the thickened ends of the chromosomes are left behind in the cytoplasm as the telophases of the cleavage divisions take place. Chromatin diminution never occurs in those blastomeres which are antecedent to the germ cells of the later stages; but every blastomere which will produce only somatic cells goes through the process of chromatin diminution once. In the 2-cell stage S1 undergoes chromatin diminution while P1 does not. In the 4-cell stage S2 repeats the process but P2 does not. In NEMATODES 49

the 8-cell stage again P3 retains its entire chromatin complement while its sister cell S3 shows the differential loss. This setting aside of the germ

3 I a I‘ a,I‘ a H a II‘ 8 all’ A ad “P 0‘ 0:1‘ an an‘ E all‘ 0 s. b I. 3 bI 3 bl‘ b bII bm bII’ B I /3 I‘ K3 /3 I,

3

/3 II‘ /3 II p 11* Egg mst { m st. Mst mesoderm zmlage luau’ ,L-L stomodeum anlage (TT EMSt I EI ° 51 E primitive endoderm EII ° " \ 8 II P‘ cl C {en C ectomesoderm yl y { yII P, d D {5 secondary mesoderm P: { G . P4 _ germ line (:1

CELL LINEAGE OF ASCAEIS FROM DESCRIPTIONS OF ZUR HTRASSEN AND BOVERI

line continues for five cell generations, at the end of which time no further somatic cells are produced from this line and the cells rest from further division until the organism has reached a considerable degree 50 IIOLOBLASTIC TYPES OF CLEAVAGE

of maturity. The distinction which is made possible by following through the chromatin diminution between germ plasm and soma in these early blastomeres of Ascaris has been of great theoretical significance and often referred to as evidence in support of the theory of germinal continuity. In this connection it is further discussed in Part Two, Chapter I. The process will be more clearly understood by referring to that discussion and also to the table showing the cleavage of Ascaris which appears herewith.

5. Rotifers

The remaining example of the bilateral type of cleavage is that of the rotifers. This example is not in many respects characteristic of the type and its development is not fully understood. It is to a certain extent intermediate between the bilateral and the spiral types. The retifers have no cleavage cavity or gastrula cavity. (That is, they have stereoblastulae and stereogastrulae.) The resemblance between the developmental conditions of annelids and rnolluscs and of the rotifers is perhaps not so surprising in view of the fact that all these groups pass through larval stages which are_ morphologically trochophores.

Although the character of the cleavage of rotifers is sufiieiently bilateral to be placed with other forms of this type, the peculiarities are such that it seems unnecessary to follow out the details for these forms.

IV. SPIRAL CLEAVAGE

Spiral cleavage is characteristic of polyelads, nemerteans, polychaetes and many molluscs. Eggs which cleave spirally are with few exceptions well filled with yolk and therefore segment unequally. Frequently the inequality is so great that only a small cap of cells comprising the ectoderm lies on the large endodermal cells with a consequent more or less complete reduction of the cleavage cavity. This condition also results in a much modified type of gastrulation from that which is characteristic of holoblastic eggs.

Nevertheless it is not difficult to derive the spiral type of cleavage from the equal radial type. The first two cleavages are meridional and about at right angles to each other, thus dividing the egg into four nearly equal blastomeres. In the 4-cell stage blastomeres A and C (see nomenclature below) are nearer the animal pole than B and D and form with each other what is known as a polar furrow, as do B and D at the vegetal pole. But the polar furrows at the two poles are perpendicular to each other. The departure from the radial type becomes clearly distinguished in the third cleavage, owing to an oblique shift in spindle direction so that when viewed from the animal pole the upper end of SPIRAL CLEAVAG E 5 1

the spindle is turned either to the right (which is the usual ease) or to the left. Bearing in mind the fact that the yolk is massed at the vegetal end of each blastomerc and the pure cytoplasm at the other ends, and the general rule (Sachs-Hertwig laws) that a spindle axis tends to lie in the center of the cytoplasmic mass, one sees that an unequal cleavage of each of the four blastomeres will occur. They are divided into small upper cells or micromeres, and large ones in the lower hemisphere or macromeres, and the upper quartette of cells thus arising alternates in


fiG. 27. (‘nmp:mLti\'o diugrzuns of radial and spiral cle:tvn.ge. (Redrawn from Korsehelt and Helder.)

A, mdinl type; B, spiral type in third cleavage; C, D, rudial and the spiral type respectively in fourth cleavage.

position with the lower (fig. 30 c, e). The upper quartette of cells, called ectomeres, appears to be given off spirally from the lower endomeres, although of course speaking strictly it is not correct to think of these cells in this manner, for both quartettes are composed merely of the daughter cells of the preceding 4-cell stage. This third cleavage is said to be a dexiotropic or right-handed division since the cells of the ectomere quartette are turned 45 degrees from those of the macromeres in a right spiral.

The fourth cleavage ‘spindles are now formed in accordance with the general tendency expressed by the so-called alternation rule that suc52 HOLOBLASTIC TYPES OF CLEAVAGE

cessive cleavage planes tend to intersect each other at right angles. The spindles, therefore, take up such positions that the next divisions are laco @® @@

fiG. 28. (‘ontinuutinn of fig. 27. Polar views.

A, 13. 8- and 113-0011 stages rarlinl type; (3, I), third and fourth cleavages, spiral typo; E. 1". 8- and 16-cell stages spiral typo.

tropic, that is in the direction of left-handed spirals. This alternation continues in regular order until four quartettes have been produced, and meanwhile each of the cells divides according to the same general laws of E

fiG. 29. Cleavage of Crcpzdula. (Redrawn from (‘onklin.)

A. resting stage after the first cleavage; blastomeres flattening against each other and nuclei. asters, and protoplasmic area rotated dexiotropically; B, anaphase of the second cleavage. The shift which will result in the formation of a polar furrow just beneath the polar bodies is already making its appearance, C‘, completion of the second cleavage Polar furrow well formed; D. third r-leavage; E, side view of egg in 29-cell stage. The relation of the mesontoblast coll 4d is shown to the macromere D. 54 HOLOBLASTIC TYPES Oli‘ CLEAVAGE

cleavage. Since the blastomeres of spirally cleaving eggs are always unequal, differences occurring even within a quartette as well as between different quartettes, it follows that the cleavages cannot long remain entirely regular, for differentiation is rapidly taking place.

Owing to the fact that spiral cleavage is one of the most markedly determinative in character, this form presents an unusually good example for the study of cell lineage. To bring out the relationships between cells it is found to be necessary to have a definite terminology and nomenclature for the blastomeres of eggs of this type. The system adopted by Conklin for expressing the relationships in the case of Crepidula is now in general use. Certain special cells should be given special names, but in general the system adopted should show immediately the derivation of each cell by its name. For this purpose Conklin modified the system previously introduced by Wilson to describe the cell lineage of Nereis.

In the nomenclature used in Crepidula Conklin designated the quartettes of cells by coefficients: “e.g., the first quartette of micromeres and all their derivatives are designated by the coefficient 1 (la, ld, la‘-2, 1c”, etc.), the second quartette and its progeny by the coefficient 2 (2a, 2d, 2c3-1, etc.), the third quartette by the coefficient 3 (3a, 3d, etc.), and the fourth quartette by 4 (4a, 4d, etc.).” It is desirable to emphasize in this manner “the differences between the quartcttes of micromeres because in general their histories are very different,” and because the distinctions afford the basis for tracing the cell lineage in the more advanced stages. The coefficients designating the quartettes are retained in all subsequent stages and the further cell lineage indicated by exponents. The cell la divides to form la‘ and la“. Then further exponents are added for each new cell generation always retaining the complete designation of the parent cell. The cell la“ produces la?‘ and la”; la“ produces la?“ and 1am, etc. These are the designations used for the micromeres and their descendants.

The second division resulted in the formation of four blastomeres, A, B, C, and D. (Capital letters are used to indicate macromeres.) These divided in turn to produce 1A and la in the A quadrant of the egg and similarly in the other quadrants. Each successive macromere receives a new coeflicient as it divides into a new macromere and a micromere; thus 1A produces 2A and 2a; 2A in turn 3A and 3a. Numerical coefficients are used to designate successive quartettes, while the exponents indicate the products of their division. Cleavage is dexiotropic, or oblique to the right, if the spindle direction is turned clockwise from the axis of the egg, and laeotropic when turned to the left.

By reference to the accompanying table the relationships of the blastofiG. 30. first cleavage of Crezridula plana. (After Conklin.)

A, approach of sperm and egg pronuclei; B, nuclei in contact, asters and centrosomcs at their pole, central spindle not yet formed; C, central spindle appearing between the two cleavage centrosomes; chromosomes aggregating on the spindle; other granules dis— solving. Sphere substance increased in size and radiating into the cytoplasm; D, prophase of the first cleavage. Chromatin granules assuming their relation to the spindle fibers; E, metaphase of the first cleavage; F, telophase of the first cleavage; spindle axis bending. Nuclei of left cell partially divided indicating origin of upper part from egg pronucleus from female and lower from-the male. 56 HOLOBLASTIC TYPES OI" CLEAVAGE

meres and their fate will be more clearly understood and the application of the system of nomenclature shown for this case.

In general the 8-cell stage of an egg with spiral cleavage consists of four micromeres, 1a, 1b, 1c, 1d about the animal pole, and four macromeres, 1A, 1B, 1C, ID, at the vegetative pole. In most cases the third cleavage is dexiotropic. The 16-cell stage is reached by a aeotropic division and consists of the quartettes of micromeres, la‘,1b‘,lc’,1d‘, 1a’,1b’,1c2,1d?, 2a,2b,2c,2d,andonequartetteof1nacr0meres,2A ,2B,2(,‘, 2D. There is an intermediate condition in eggs having spiral cleavage in which there are actually twelve cells only, for the second quartette, 2a to 2d, is budded off before the division of the first, 1a to 1d, is completed. There is a similar lack of regularity of division in other stages, some quartettes dividing while others hold back even to the extent that some cells may be an entire cell generation behind others. In the transl A B Fm. 31. Cleavage of Trochus. (Redmwn from Korsehelt and Heider, after Robert.) A, 8-cell stage viewed from the side (the D quadrant will become the dorsal side); 13.

similar view of 16-cell stage. tion to the 32-cell stage there is actually no resting stage in the sense that all the cells are at once in that same state of progress.

The division producing the 32-cell stage is usually a dexiotropic one. The cells of the first quartette receive their second exponent, la‘ becoming la" and la”; those of the second quartette their first, 2a‘ and 2a’; and the four macromeres divide, producing 3A and 3a (using the A quadrant as a sample). There are now sixteen descendants of the first quartette and eight of the second.

The 32-cell stage brings to the spiral type of cleavage a certain degree of completeness, for three successive divisions have produced three quartettes of ectomeres that represent chiefly ectoderm-forming cells, although larval mesenehyme is also produced from some of the derivatives of the second quartette. The four macromeres subsequently produce two more quartettes of micromeres and are in general endodermforming cells. An exception is found in the cell 4d in the higher forms having spiral cleavage, for it is the parent cell of the mesoderm. SPIRAL CLEAVAGE 57

In later stages some blastomeres are found to divide meridionally, and the necessity appears of a new criterion for numbering the products. In such a case the dcxtral cell is given the exponent 1 and the sinistral 2. The succession of alternating left and right divisions continues to the 64-cell stage. Later on bilateral conditions develop and the embryo takes on the symmetry of the adult.

Spiral cleavage, as already indicated, occurs in several of the great divisions of the animal kingdom. It first appears in the polyclads. Our knowledge of the cleavage of this group is based especially upon the


Fm. 3'2. (-‘i(‘.’!\’:lL!(‘ of ('4-rt-bralrz/u~c marginalus. (Redrawn from Korschelt, and Heider, after Zeleny.)

.\. R-cell stage; B. 16-r-ell stage; (‘, :.’.2s’»cell stage from side view; D. 28-cell stage from \'egetati\"e pole.

study of Discocoelis by Lang, of Leploplana by Wilson and of Pltmocera by Surface. Cleavage in these forms follows the general scheme as previously given for all of its main features. There are variations due to differences in the size of the blastomeres and other such factors, but the general plan as described is entirely applicable here. There are certain features in the development of these forms which suggest a relationship to the cleavage of the other flatworms, but there are a great many points of agreement between the method of cleavage of polyclads on one side and that of the annelids and inolluscs on the other, and it has been held by the most careful investigators that a true homology exists with respect 58 HOLOBLASTIC TYPES OF CLEAVAGE

to the early development of these forms. The points on which the agreement is observed are sufficiently important that they seem to indicate more than a mere adaptive coincidence on the part of the previous types of the two groups. The formation of three ectomere quartettes which alternate in dexiotropic and laeotropic formations, the agreement in the relationships of the cells of the quartette 1a2—1d2 with the primary trochoblasts of the annelids and molluscs, and complete homology in the development of the mesoderm and also in the formation of the ectodermal structures near the animal pole, all seem important in bringing the polyclads into line with the annelids and molluscs.

The nemerteans also conform to the general method of spiral cleavage, and indeed they are almost diagrammatic in the regularity which they show. The studies of Coe on Micrura, of C. B. Wilson on Cerebratulus lacteus, and of Zeleny on Cerebratulus marginalis are sufficient to establish the important features of cleavage in this type. The work on these forms as well as upon others of this group is so similar to that described for other cases that it does not seem necessary to consider it in detail although it is important and of excellent character.

Spiral cleavage is especially developed among the polychaetous annelids. Of special importance are the studies of E. B. Wilson on Nerezls-, of Child on Arenicola, as well as the observations of Mead, Treadwell, Nelson, Torrey, and Gerould on other forms of polychaetes. The later stages have been made more clear by the work of Woltcreck on Polygordius. The cleavage of Arenicola, which leads to the development of the trochophore larvae in its fundamental features, corresponds to that of the general type already described. The cleavage axis running from animal to vegetative pole corresponds to the chief axis of the troehophore larva, and although the first cleavages present slight differences in order and in the angles they make with the egg axis the result is the same as in the general type, for by the time of the 8- and 16-cell stages the normal relationships have been returned although there are certain marks of size differentiation among the various blastomeres. The differences which exist between the cell lineage of Arenicola and that of the type form are minor differences only. There are, however, some special features about the cleavage of the annelids which deserve mention. In the animal half of the egg there presently develop certain configurations which are especially useful in homologizing the blastomeres of these forms with those of the very similarly cleaving eggs of the gastropod molluscs. The blastomeres about the animal pole arrange themselves to form what is known as the cross of the annelids, and this becomes the chief characteristic of the embryo for the stages immediately following the 64-091] condition. As will be seen by consulting the accompanying fiG 33 ('le.nu.go stage of Anmcula cnstata (RC-drawn from Korichelt and Helder, after (‘hxld )

A, 1)-coll stage, B, 4-coll stage C, “Hell stage I), 16-coll stage Pnmary trochoblasts are stxppled, E, the apu-nl stun culls la"-Id“ are dwldmg to produce m F the apical rosette cells 19.1”-ld'“ and the stem cells of the cross 1a“‘-Id“? The primary trochoblasts are la"-Id" and 121”-Id” 60 HOLOBLASTIC TYPES OF CLEAVAGE

figure there are in each quadrant apical rosette cells, stem cells of the cross and intermediate cells. These cells when the four quadrants are considered together form a very definite picture of a cross, and not only are the cells themselves homologous with the similar condition found in the gastropods but there is a decided similarity in their arrangement, as will be seen by comparing fig. 33 for Arenicola with the similar figure of Crepidula (fig. 29).

The first appearance of the mesoderm in Arenicola is from the cell 4d which has come to be known as cell 111. Here again the homology between the annelid and gastropod types is quite complete. The study of cell lineage in the annelids was carried on so thoroughly and the results were so beautifully worked out that there are many other features in the development of this group that call forth the admiration of the observer to the precision of the developmental mechanism. This is determinative cleavage at its best and the specialist in this field of embryology finds a great deal here to interest him.

The cleavage of the Oligochaeta and the Hirudinca with certain modifications shows the general agreement with the type just discussed. These differences are correlated with the differences in the mode of existence between the water-living polychaetes and the other more specialized classes of annelids. In one of these forms, Clepsine, a leech, the first study of cell lineage was made by Whitman in 1878.

As already indicated, the most important studies of the spiral type of cleavage have been made in various molluscan eggs. Here there is a wealth of observation and the literature contains many excellent accounts of the cell lineage of these forms. Only a very few can be mentioned including the following. For the Amphineura there are the observations of Metcalf on ('hz'ton and Heath on I schnochiton; for the Lamellibranchia those of Lillie on U me. The gastropod eggs have been especially studied as is indicated by the following investigations on the three subdivisions of this class. Conklin on Crepidula, Robert on Trochus are especially important contributions to our knowledge of the development of the Prosobranchia, as is the work of Heymons on Umbrella, Casteel on fiona for the Opisthobranchia, and Holmes on Planorbis and Wierzejski on Physa for the Pulmonata. Many other forms have been studied, but these are examples of the various conditions found here. It may be noted that the cleavage of Planorbis and of Physa may be readily followed in the laboratory, at least during very early stages, and they present perhaps the best opportunities for a student to observe this type of development.

Spiral cleavage in the molluscs conforms to the type and indeed might serve as the type, as may be seen from the table summarizing the develSPIRAL CLEAVAGE 61

opment of Crepidula. The importance of the homologies existing between the blastomeres of the annelids and of the molluscs have already been pointed out and need not again be referred to. Certain other interesting features, however, should be noted. One of these is the presence of the yolk lobe described by a number of investigators in heavily yolk-laden Inollusc eggs. A similar structure has been described also in some annelids. Here there appears at the vegetative pole in each of the first few cleavages a lobe Inore or less clearly marked but never completely cut off from one of the blastomercs. It is known as the yolk lobe and is of varying size in different animals. Before each succeeding cleavage it unites again with its blastomere, only to present itself in the interim before the next cleavage. finally it becomes completely united with the cell D and development proceeds. Experiments have been performed in which this lobe has been cut off with the result that the larvae lack the ectoderm of the posterior portion of the body. Another interesting phenomenon observed in some cases of spiral cleavage concerns the relation between the symmetry of the adult and that of the embryo. Crampton pointed out as a result of studying the cleavage of Physa that the reversed spiral of the shell of this snail is not a matter of adult life only but is so definitely impressed upon the nature of the species that the direction of the cleavage planes from the third division 011 is exactly reversed from what is seen in eggs in which there is a shell coiled in a right-handed spiral.

The later stages in the cell lineage of spirally cleaving eggs lead us to a consideration of the methods of gastrulation and of mesoderm formation and as such seem more properly to be considered in the chaptels which deal with these matters.

BIBLIOGRAPHIC Note

Among the more important accounts of the subjects contained in this chapter are the following: Echinoderms: Korsehelt and Heider, Selenka, Boveri, Plough, Morgan (Experimental Embryology); Ctenophores: Ziegler, Metchnikoff; Amphioxus: Cerfontaine, Hatschek; Ascidians: Conklin, Chabry, Castle, Drieseh; Frog: Brachet, Morgan; Ascaris: Boveri; Spiral types: Conklin, Holmes, Wilson, Child, Lillie, Robert, Coe, Lang, Surface, Whitman, Metealf, Casteel, Wierzejski, Crampton. These works are cited in full in the bibliography on page 406.


Chapter V Meroblastic Types of Cleavage

I . SUPERfiCIAL CLEAVAGE

Superficial cleavage is found to occur most extensively among the arthropod classes and indeed by many it is supposed to be coextensive with this phylum of animals. There are, however, some other cases which may be properly spoken of as superficial cleavage. Among these latter are the eggs of some eoelenterates which are heavily laden with yolk, for example, Renilla, hydrocorals and Alcyonium. In addition it has been described for the holothurean, Cucumaria glacialis.

Furthermore, it is by no means true that all arthropods undergo superficial cleavage. Among the Crustacea there are many cases of total cleavage in holoblastic eggs, and at the other extreme of the phylum the scorpions have discoidal cleavage. Examples of holoblastic cleavage may be chosen from Branchipus (Brauer, 1892), Artemia, Lucifer, some parasitic copepods, the cirripeds and most frec—living copcpods. These examples include cases in which cleavage is very nearly equal and in others, as the cirripeds, distinctly unequal. One illuminating study has been made on the cleavage of the barnacle Lepas, which suggests relationship to the annelid type and even has certain characteristics of the rotifers. In view of the generally assumed fact that the arthropods are derived from annelid ancestry, the case of Lepas as studied by Bigelow seems to have unusual importance.

With the exceptions of the forms mentioned the arthropods have superficial cleavage. It will be observed that the diversity of this phylum is so great that many different conditions of cleavage are found here and even among the cases of superficial cleavage there will be seen to be a great variety. To such an extent is this true that we cannot describe as typical of superficially cleaving eggs any one particular form, and, although we may classify superficial cleavage into subdivisions, these are by no means separated from each other sharply but gradations exist between them. Superficial cleavage is characteristic of eggs which are centrolecithal in character; eggs of the centrolecithal type are derived from forms having total and in most cases equal cleavage, while on the other hand they lead to an extreme type of superficial cleavage which is so different from the usual arthropod eg as to

62 SUPERfiCIAL CLEAVAGE 63

be classified with eggs having discoidal cleavage rather than superficial. Reference is made to the eggs of the scorpion which are without question derived from the extreme superficial type but which as a result of parallel convergence resemble most clearly the discoidal type of vertebrates. In eentrolecithal eggs the cleavage nucleus is usually at the center of the egg and is surrounded by the mass of yolk spherules and fat droplets. Penetrating this mass in every part is a network of cytoplasm which is continuous with the central cytoplasmic portion around the nucleus and also with a very thin superficial cytoplasmic layer on the outside of the egg. This latter layer is in some cases so delicate as to be difficult to make out, whereas in other cases it is clearly visible. It is to be regarded as characteristic of the centrolecithal egg, however. The shape of these eggs varies from spherical or elliptical to a greatly elongated, almost cylindrical type, but they are seldom “egg shaped” in the sense that they have one blunt and one pointed end. There is practically no trace of an axial structure which is characteristic of so many other egg types.

As a first type of superficial cleavage we may take up one of the insects, for in this form it is especially clearly developed. The well-known figures of the cleavage of Hydrophilus suggest the early course of this type of development. The cleavage nucleus lying at the center of the egg in the midst of its plasma island divides into 2, 4, 8. 16 nuclei, each surrounded by a small portion of cytoplasm and each somewhat separated from the others in the form of amoeboid or star-shaped areas. Actually all are in communication through the plasma. network that penetrates the yolk mass. At this stage and for some time later the egg actually is a syncytiuln, for there are no definite cell boundaries marked off around any nucleated areas. It has been the practice on the part of some writers to speak of these areas as cleavage cells, although they are not cells in the sense of other types of cleaving eggs. After a few divisions these cleavage cells come to form a layer within the yolk which by one continued division tends to approach the periphery of the egg. At length they unite with the superficial cytoplasmic layer in Hg/drophilus near the middle of the egg first and at the ends only some time later. Then cytoplasmic boundaries become visible and the cleavage is truly superficial, although of course only partial, since the divisions do not extend through the yolk mass.

In insect eggs it frequently occurs that some of the cleavage cells do not take part in the formation of the blastoderm but remain in the yolk while the others pass to the surface. They take on special functions for the assimilation of the yolk substance and become known as the mellophages. In some cases incomplete cell boundaries seem to be formed fiG. 34. Blasboderm formation in the water beetle Hydrophilus. (Redruwn from Korschelt and Heidcr. after Heider.)

b, blastoderm cells; 0, “cleavage cells"; p, peripheral layer of protoplasm; y, yolk. CLEAVAGE AT fiRST TOTAL BUT LATER SUPERfiCIAL 65

around these vitellophages, giving rise to the so-called secondary yolk cleavage. The vitellophages are to be regarded as endoderm, and for that reason some investigators have described superficial cleavage as leading directly to the formation of a gastrula-like stage since two kinds of cells, ectoderm and endoderm, are formed about the same time. This view has not been widely adopted.

Superficial cleavage usually results in the formation of blastomeres of equal size and cleavage is indcterminativc.* Inequalities appear very early in some forms, however, and there are many variations from the forms of the cleavage as already given for Ilytlrophilus. These variations seem at first sight to correspond in a general fashion to the systematic groups of the arthropods, for the crustacean eggs are distinguishable from the spiders and from tl1e insects, by certain characteristic features; but these differences do not lend themselves to accuracy of statement nor form a satisfactory basis for classification. It is wiser therefore to classify the superficial cleavage under the following heads: Group 1. Cleavage at first total but later superficial. Group 2. Cleavage purely superficial. Both of these groups in their turn may be divided into two subdivisions in one of which the blastoderm forms on all sides simultaneously and in the other on the ventral side precociously.

1. Cleavage at first Total but Later Superficial

This type of cleavage, which is typical of many crustaceans, begins with the division of the plasma island into 2, 4, and perhaps 8 blastemcres about which all cell boundaries are cut off at once. (‘leavage during this period of the development and for some successive cell divisions thereafter is total and approximately equal. Presently there comes a time when the furrows at the surface are unable to cut entirely through the egg, or if they do the yolk masses at the center must fuse together and cleavage becomes superficial with a cellular region sharply separated from the yolk mass. The blastula consists of a layer of superficial cells of cq11al size and an inner yolk mass replacing the cleavage cavity. In many cases there is a (listinction between the central-lying yolk mass and the yolk which formed the inner end of the blastomcre. They were left incomplete by the failure of the furrows to penetrate to the center of the egg. These inner ends are spoken of as the yolk pyra

  • Nevertheless, experiments on the egg of the house fly, M usca domestica, made

by Reith (1925) show for this animal (and make it probable for others having this type of cleavage) that the egg is highly determinative. The embryo is fore-shadowed in the cytoplasm of the egg and the regions are clearly organized in relation to their future destiny. Add to this.the very definite nuclear determination which the experiments on the genetics of Drosophila have demonstrated, and it is clear that the eggs of Dipteru can by no means he called indeterminative. 66 MEROBLASTIC TYPES OF CLEAVAGE

mids (sometimes as Rathke’s yolk pyramids). The significance of these structures is not entirely clear but their appearance is characteristic. This type of cleavage easily suggests a transition from the holoblastic eggs of other Crustacea to the form in which cleavage is purely super. ficial. This type of cleavage, as already pointed out, occurs in two subdivisions :

fiG. 35. Cleavage of Macrutoma vulgaris. (Redmwn from Korsehelt and Heider, after Uzel.)

A, two cleavage nuclei; B, four cleavage nuclei; C, section through 16-cell stage with blastomeres completely separated from one another; D, similar section through 32-cell stage. E, F, later stages in the formation of the blastoderm. the yolk mass in the center having fused.

a. Eggs in which the superficial cleavage leads to blastoderni formation simultaneously all over the egg. To this subdivision belong the eggs of those free-living copepods which are not holoblastic, some parasitic copepods, the ostraeods, spiders, and some isolated forms in various groups of the arthropods.

b. Eggs in which the blastoderm develops early on the ventral side, a condition which foretells the position of the forming germ streak. The EGGS WITH PURELY SUPERfiCIAL CLEAVAGE 67

dccapods in part come under this subdivision as do some of the amphipods as well as other scattering forms.

2. Eggs with Purely Superficial Cleavage

Eggs which come under this subdivision carry still farther those tendencies which are beginning to be expressed in the previous group.

fiG. 36. Cleavage of the crab Dromfa. (Redrawn from Korschelt and Heider. after Cane.) Successive stages showing “cleavage cells," the yolk pyramids, and the blastoderm.

The cytoplasmic portion of the egg is quite unable to control the yolk mass and therefore the cleavage cannot be complete. The central-lying nucleus with its surrounding plasmic layer divides several times but no cell boundaries are formed by the separate areas. The only indication of division now to be seen is the occasional presence of superficial furrows 68 MEROBLASTIC TYPES OF CLEAVAGE

which do not penetrate far into the yolk. As the cleavage nuclei increase they approach the surface and furrows become more pronounced. The result is a blastoderm with the cell boundaries cutting in to the yolk although not completely delimiting definite cell bodies from it until a. later stage when the blastoderm takes on the form of the definite layer. Cleavage of this type occurs among the Crustacea commonly, although it is much more widespread in the Malacostraca than in the Entomostraca. In some of the latter, however, this condition has been described. In the Malacostraca it is the most common form, occurring in the Decapoda (with the exception of those previously mentioned), Nebalia, Cumaceae, the Schizopoda, and Isopoda. It is found also in some of the mites, in nearly all insects, in the Myriapoda and in the ()nychophora. With a distribution so widespread as this it is obvious that many variations will be found, although in general the description of Ilyrlrophilus as already given is quite applicable. There are cases in which the superficial plasma layer is so thin as to be almost absent and other cases in which it is Very definitely marked and these varying conditions have an effect upon the appearance of the blastoderm. There is also variation in the extent to which the blastoderm is formed over the surface of the egg. This latter feature is the basis for the further classification of these eggs into two types as in the previous group.

1. Eggs which have simultaneous formations of the blastoderm all

over the egg. Most of the cases of purely superficial cleavage come here, specifically the Cladocera, most decapods, the myriapods, most insects and many other scattered forms.

b. Eggs with precocious development of the blastoderm on the ventral side. Here belong Ncbalia, the schizopods, the Cumaceae, the isopods, and some decapods,including the lobster. The restriction of the blastederm to a small portion of the surface of the egg is so marked in some of these forms that it was formerly the practice of some investigators to regard these as cases of diseoidal cleavage. We do not at the present time, however, so regard them. Nevertheless this subdivision of superficial cleavage clearly leads to the conditions found in the scorpions as an extreme case, and these latter forms are commonly included with the cephalopods and meroblastie vertebrates under the head of discoidal cleavage.

II. DISCOIDAL CLEAVAGE

Discoidal cleavage is the type generally found among the meroblastic vertebrates, and it occurs also in the ascidian group, the pyrosomes, and in two separate invertebrate classes, the cephalopods and the scorpions. This distribution suggests what is found to be the case, namely that fiG. 37. Cleavage of (”am7mdz'a staphulinus. (Rcdrawn from Korschelt and Heider, after Uzel.)

Sections showing cleavage and formation of the blastoderm. In F the thickening on the ventral side which will give rise to the blastoderm is to be noted. 70 MEROBLASTIC TYPES OF CLEAVAGE

discoidal cleavage is derived from simpler, unlike, and unrelated cleavage forms. It may be assumed that the vertebrate type is derived from an extreme case of telolecithal egg in which there is sufficient yolk present to prevent the cleavage furrows from cutting entirely through the egg. This results ‘in a certain degree of opposition between the animal or protoplasmic portion of the egg as contrasted with the vegetative or yolk region. Similar relationships obtain for the other groups having discoidal cleavage except the scorpions in which the discoidal type is derived, as may be inferred from the preceding discussion (page 68) from the extreme case of purely superficial cleavage. Only a small portion of the egg surface is involved in the formation of the embryo body in the superficial forms mentioned.

It is evident that not much in common is to be expected in the elemental features of these two characteristic modes of discoidal cleavage.

@@

A B C

fiG. 38. Germ disc of the scorpion Euscorpius carpathicus. Polar views. (Redrawn from Korschelt and Heider, after Brauer.)

It was formerly said that discoidal cleavage occurs also in some crustaceans but it seems wiser to regard these as within the limits of superficial cleavage than as examples of the true discoidal type. Because of the separate origin of these cleavage types it will be convenient to begin this discussion with the cleavage of the scorpion.

1. Scorpions

Only one important piece of investigation, namely the study of the cleavage of Euscorpius, by Brauer, is available upon which to base our knowledge of this type. The egg is richly yolk laden and the protoplasmic portion is limited to a disc-shaped area which corresponds to the point of attachment within the egg follicle. With the exception of perhaps a very thin filament over the surface of the egg no other protoplasmic portion can be demonstrated. Segmentation is limited to the protoplasmic disc which divides with fair regularity. About the third or fourth cleavage there is oftentimes what seems superficially to be a bilateral arrangement of the blastomeres, but the appearance is only superficial for the cleavages from here on become quite irregular. The SCORPIO NS 71

result of cleavage is a round or oval blastodisc consisting of at first but a single layer of cells. The single-celled condition does not remain long because a number of cells wander down below the surface from a definitely recognizable white speck. This speck is important in determining the plane of symmetry and the hinder end of the embryo. The first cells which wander in are transformed into yolk cells and although they form an irregular layer they take no further part in the development of the embryo. Very shortly after the migration of the yolk cells a group of cells becomes differentiated as a result of ingrowth from the same region and is said to give rise to all the genital cells. True endoderm


fiG '3‘) Set tions of stages similar to lig .58, and of two liter stages.

A, immature germinal vesicle, B, early cleavage, C‘, l)l‘1‘lt()(l(‘l‘II1 formed, D, beginning of germ layer forniition showing segregation of the germ cell g < and of the endodi-rm, en E, later stage in germ layer form then cc cctoderm, mes mesoderin, so serosa

cells also appear in like manner at the same time. Brauer holds that the endoderin cells do not contribute to the formation of yolk cells nor do the yolk cells take part in the formation of the endoderm.

Mesoderm arises from a division of cctoderm cells near those which are to produce genital cells. The subsequent development of the blastedisc shows the formation of a segmented germ streak which gradually develops into the typical body form of the scorpion and which grows finally to include entirely the yolk in the middle region of the gut. The forming embryo is suggestive of certain stages in the later development of eggs having superficial cleavage but it is likewise very similar in a number of particulars to the conditions found in vertebrate embryos 72 MEROBLASTIC TYPES OF CLEAVAGE

which develop by diseoidal clcivage. There are clearly produced in these different groups similarities which are purely embryonic and therefore transitory; they have no evolutionary significance.

2. Cephalopods

The cleavage of cephalopod eggs differs in many particulars from that of other molluscs and also from the forms within the groups having discoidal cleavage. The differences seem to be in keeping with the peculiarities of egg structure, which are pronounced.

The eggs are laid in large numbers, usually together, and the mass may assume various forms. There is always a protective covering which is the means of attaching the mass of spawn. In Sepia the eggs are dis av


A v B C fiG. 40. Eggs of the squid Loligo pmlii. (Redmwn from Korsehelt and Heider, after Watase.)

d. dorsal, v. ventral, a. anterior, p. posterior, r. right, I. left.

crete and each is in its own capsule. In Loligo many are laid together in a gelatinous tube and numerous tubes are attached in one mass, known to the sailors as “dead men’s fingers.” Fertilization follows after various peculiar types of copulation in which spermatozoa are transferrerl in spermatophores; fertilization is internal in some groups, and external in others, of which the squids mentioned are examples.

The eggs themselves are relatively large for marine eggs and all contain very much yolk. The development of the squids, particularly of Sepia and of Loligo, are best known and will be used from here on as examples of this form of development. Sepia eggs have the size of ordinary peas, whereas those of Loligo are much smaller, but even they are larger than the eggs of most marine molluscs.

Cephalopod eggs have been studied by numerous investigators, but our knowledge of the cleavage depends chiefly upon the work of Vialleton on Sepia ofiicinalis and of Watase on Loligo pealii. The eggs of Loligo, at the time they are ready for cleavage, are somewhat oblong in shape, CEPHALOPODS 73

one end being more pointed than the ot.her. The egg consists of a mass of fine granules of food yolk surrounded entirely by a thin protoplasmic layer. This layer is thicker at the pointed end of the egg where the germ disc will form. Thus this egg represents an extreme telolecithal type and is a perfect example of meroblastic cleavage.

The uncleaved egg from surface study alone gives evidence of bilateral symmetry which bears a definite relation to the subsequent history of the embryo, and it is possible to distinguish an anterior border from a posterior as well as right from left sides of the organism. The germ disc end of the egg corresponds to the dorsal side of the embryo and the


fiG. 41. Germ disc of the squid Sepia 0j7'i(‘inaIi.~r. (Redrawn from Korsehelt and Heider, after Vialleton.)

I to III, indicates direction of su('r'essive cleavage planes.

yolk pole to the ventral side. On the anterior side the germ disc extends farther down toward the equator than upon the opposite side, but it is symmetrical with respect to right and left. The animal pole of the egg is slightly eccentric to the center of the germ disc, being nearer its posterior edge. Here in Loligo may be seen three polar bodies in the perivitelline fold inside the chorion. The egg is surrounded by chorion which is secreted by the follicular epithelium and is often very tough. The sperm enters through a mieropyle in this chorion.

The early cleavages are limited to the germ disc. The first furrow corresponds to the median plane of the future embryo, dividing the egg into right and left halves. In the center of the blastodisc it cuts in 74 MEROBLASTIC TYPES OF CLEAVAGE

deeply, dividing the entire protoplasmic cap at this point, but toward the edges of the disc it becomes shallower until it is a mere groove and finally disappears entirely. The successive cleavages behave in a similar manner. Thus cleavage is incomplete even with respect to the protoplasmic layer. ,The second furrow is at right angles to the first, and like it, fades away into the thin protoplasm. The later furrows which extend outward likewise fade away and the cells thus formed are incompletely separated peripherally. This gives rise to the distinction made by Vialleton of the products of cleavage into blastomeres and blastocones,

1

o 6% " “

69°a° »( ‘-‘ 9

_r ”‘o,w"{§y,_ 01¢)‘: 501,1‘-xv «.91? -I. - v ‘,Q°.. _v'5 6 b


Fm 42 Older germ disc of S(’[)’LLl ofiicmalzs from the beginning of germ layer form itu n The darker cells iiidimte the region where the disc is of several cells in llll( kiiess L itcr stage than fig 41

the term blastomere being applied only to those cells which are conipletely cut off, while the peripheral ones which have no outer boundary are spoken of as blastocones.

In the preceding types of cleavage we have seen that the cleavage cells have usually received special designations. In the present case, on the other hand, it has been found more convenient to indicate a distinction between the various cleavage cells by numbering the furrows which separate them, the first furrow lying in the median plane and indicated by the polar body numbered I. The second furrow, II, is at right angles to it. The third furrow likewise is meridional but it divides CEPHALOPODS 75

the two anterior blastomeres and blastocones equally and runs obliquely to the previous furrows. The two hinder blastocones are divided very unequally, for furrow III is almost parallel to the median plane and cuts off two very narrow segments. In the fourth division the inner ends of these narrow segments are cut off to form the first two blastomeres by the transverse plane. The remaining six cells are again divided in a direction which is correctly spoken of as meridional, although the various planes are not entirely regular and do not converge at the center


fit. 4i Se: tioim ilirmigh the edge of the germ (.lls( in suctessiic stagm B, corresponds to fig 42 y, yolk, y 0 , yolk epithelium, e, embryonic cells

of the disc. By this time the bilaterality which existed in the uneleaved egg has become very appaient, each half of the egg consisting of seven blastocones and one blastomere. The 32-cell stage is reached partly by nieiidional and partly by transverse furrows. Numbering the blastocones of each half of the egg from the anterior side backwards as one to six, the following divisions occur. Number one divides transversally, producing a blastoinere and a blastocone. Numbers two and three divide meridionally, each producing two blastocones. Numbers four and five each cut off a blastomere by a transverse division, and number six divides meridionally. The posterior narrow pair of blastocones again 76 MEROBLASTIC TYPES OF CLEAVAGE

divide transversally, cutting off blastomeres, and the two first blastemeres likewise divide. The 32-cell stage thus consists of fourteen blastemeres and eighteen blastocones symmetrically arranged. Thus the center of the disc comes to be filled up with a compact layer of blastomeres radiating from ‘which are the blastocones.

Subsequent cleavages bring about a decrease in the size of the blastemeres and are responsible for their regular disposition. The germ disc thus comes to consist of a one—layered plate of polygonal cells with peripheral blastocones passing over into the mass of formative yolk. Gradually these peripheral cells detach themselves from the germ disc and scatter about the surface of the food yolk. It is claimed that they even wander beneath the cells of the germ disc and gradually form a layer which spreads over the entire yolk. The solid blastodisc at length becomes many-layered and by its extension grows over the layer of yolk cells derived from the blastocones.

The relationship of the primary germ layers of the cephalopods is complicated, and the manner in which the embryo body is formed is not properly a subject for detailed discussion here. The reader is referred to the descriptions of these processes in more extensive works.

3. Vertebrates

The most characteristic and best-known cases of discoidal cleavage occur among the chordates. There is a single example among the lower chordates, that of the pyrosomes, which has some resemblance to the discoidal type as found in teleost eggs. In pyrosome eggs, however, certain cells around the edge of the disc recall the blastoconcs of the cephalopods.

Among the vertebrates proper discoidal cleavage occurs widely in scattered groups. It is found in the myxinoids, the elasmobranehs, teleosts, Gymnophiona, all reptiles and birds, in the inonotremes, and it has been recorded for some Inarsupial eggs. In the opossum, however, according to the accurate and clear description of Hartman, cleavage is certainly not disceidal, nor is that of Dasyurus as figured by Hill. Thus it occurs in five classes of vertebrates, and possibly in the sixth; in seine of these it is the characteristic method and in others it is quite exceptional. This distribution points out, as has been noted previously, that there is no taxonomic or phylogenetic significance in the classification of cleavage types. An inspection of the list as given shows discoidal cleavage alongside of the holoblastic type in many of these groups. The myxinoids are discoidal while the lampreys have holoblastic cleavage in the class Cyclostomata. Among the fishes, elasmobranchs and teleosts are extremely disceidal, but the dipnoid and the ganoid VERTEBRATES 7 7

fishes are holoblastic in type. The typical amphibian egg is holoblastic, but ‘the Gymnophiona show discoidal cleavage. Instead of having taxonomic significance, the distribution of discoidal cleavage is related entirely to the amount of yolk present in the egg.

The relationship between the holoblastic and ineroblastic types of cleavage will be best understood by recalling the cleavage of the frog egg (figs. 22 and 26). From the condition found in the frog egg we may pass by a consideration of the cleavage of /icipenser, the sturgeon, Amia, the bowfin, and Lepidosteus, the gar pike, to those found in the tcleost egg. That is, we pass from the telolecithal egg of the amphibian or lamprey by increasing degrees of separation of yolk and protoplasmic portions to the nieroblastic type of the modern tcleost.


A B

l*'I<.. 44. A, ('l(‘.l\:U.EL‘ slag!-\ of the sturgeon .l(i;unxu zulhcnus, B, section through ~mme. (l{e(lr'.u\'n from Ziegler, after Whiunan and E_v(-leshymer.)

The cleavages of the lamprey and of the frog show remarkable similarity. In both there is a large proportion of yolk, but it is still suffieiently separated into spherules for the cytoplasm to cut cntirelv through it. Cleavage is total and unequal, the first two furrows being meridional and separating the eggs into four blastomeres. The third furrow is latitudinal. In Petromyzon the fourth furrows mark the beginning of irregularities in cleavages whereby the cells of the animal half cleave more rapidly than the vegetative half, some of the furrows not being completed until very late.

In the sturgeon, according to the description of Dean, the first cleavages separate the blastomeres but do not penetrate deeply into the yolk. The egg in the late segmentation stages shows a protoplasmic cap of small cells of irregular size and outline. Horizontal cleavages have also occurred and meridional cleavages have separated off marginal cells in an irregular manner so that the surface of the yolk half of the egg becomes subdivided into many-sized polygonal cells. While the protoplasmic cap of small cells constitutes a blastodisc, it does not include all the protoplasmic portion of the egg, as in the case of the true discoidal 78 MEROBLASTIC TYPES OF CLEAVAGE

types. The cells adjacent to it are connected with the yolk. The blastedisc proper, however, is separated from the yolk by the cleavage cavity, the floor of which consists at first of a few irregular yolk-bearing cells. There is no sharp distinction between these cells and the yolk which they are doubtless helping to elaborate into nutritive supplies for the growing blastodisc. Obviously the blastula here, which consists of a. blastodisc grading into shallow cells covering the yolk mass and separated by the segmentation cavity from the yolk-laden cells beneath it, has points of marked similarity with the telolecithal type of the lamprey.


fiG. 45. A, B. cleavage stages of Potromyzon fluviatilis; C, D, cleavage stages of Primmyzon. plancri. (Redrawn from Ziegler, from Hatschek.)

The inner yolk-containing cells of the latter are not represented in the sturgeon, in the yolk of which no cell boundaries are to be distinguished although the outer polygonal cells of the yolk hemisphere possess dividing nuclei. The formation of the body of the embryo is more distinctly limited to the blastodisc in the case of the sturgeon.

The next step toward the meroblastic type is seen in Amia. Here the cleavage furrows begin much as in the previous cases but the furrows are more retarded in spreading over the egg surfaces. While at first the meridional furrows are making their way toward the opposite pole, four vertical furrows appear near the apical pole and extend downward. The next cleavage is the meridional one, cutting off thus a group of eight micromeres. At the next division these then divide into a superficial and a deeper segment and the macromeres divide by vertical furrows. A new latitudinal furrow cuts off additional micromeres and VERTEBRATES 79

there is thus formed an apical disc limited to one end of the egg and much larger cell areas over the yolk portion; in the latter portion some of the developing furrows never become entirely completed. In Lepzdosteus the protoplasmic cap is still more sharply distinguished. The early furrows spreading downward over the egg’s surface never reach much


B

fiG 46 Cleavage of Amza calm (Redrawn from Ziegler, after Whitman and Eycleshymer )

beyond the equator so that the yolk hemisphele does not normally segment at all, that is, it more nearly attains the mcroblastic condition. The furrows which extend from the blastoderm over the yolk mass seem in later stages to disappear, and the protoplasmic layer in connection with the yolk contains numerous nuclei forming the so—called syncytium. These transitional stages bring us to the true discoidal cleavage as shown,

for example, in teleosts. Eggs in which the distinction between the yolk and protoplasm is 80 MEROBLASTIC TYPES OF CLEAVAGE

very sharply apparent have meroblastic cleavage, in the cases under consideration here, of the discoidal type. The first group of the vertebrates in which discoidal cleavage occurs is the Myxinoidae. Of the myxinoids the development of Bdellostoma is best known. It has been studied by a' number of investigators, notably by Doflein and by Dean. The egg is quite large, being in the neighborhood of an inch long and shaped something like a banana. It is well filled with dense yolk and the germinal disc is limited to one end. Its cleavage is very similar to that of the bony fishes which are shortly to be described. The first two furrows are approximately meridional, but irregularities begin with the direction of the third furrow and very shortly the arrangement of the furrows is that of a network enclosing the blastomeres. The outer cells are in continuation with the yolk and form a layer known as periblast. The divisions continue and the blastoderm comes to consist of several layers forming a cap covering the animal pole of the egg and gradually growing farther back over the egg. No blastocoele has been observed. The further development of the blastoderm is not entirely symmetrical, for the cells become more numerous on one side and on this side a separation of the thickened edge into two layers begins which represents the process of gastrulation in that

Fm 47 Egg of the gm PM the endoderm is separated off and with it Iaerndoetcue osemr»: In (leavaLt(' mesoderm. A gastrula cavity is not present. 

£‘°"I°r' "W" Thus there is no definite end to the processes

of cleavage and blastula formation after which gastrulation may be said to have begun, for the proliferation which permits the separation of the germ layers is entirely continuous with the cleavage processes. This type of development is seen to be totally different from that of the lampreys, which is so much like that of the amphibians as to require no special description.

So far as known all selachian eggs are extremely meroblastic and have discoidal cleavage. If a member of this group of fishes should be found with small holoblastie eggs, it would be a matter of considerable interest from the standpoint of the gradual adaptations which accomplish those modifications that are secondary to yolk accumulation. Dean has found a condition in the shark, Cestraczon, which suggests the approach of cleavage to the total, unequal type as described for Amw and Leprdosteus. Among the selachians are found genera which are viviparous as

well as others which are oviparous. The former include, among others, VERTEBRATES 8 l.

the following genera: Hecvzmchus, N otodanus, Acanthias, Galeus, Squalus, M ustelus, Carcharias, and Torpedo. The egg-laying selachians include Scyllium, Pristiurus, Cestracion, and Raja. The oviparous species produce eggs enclosed in a horny characteristic shell oftentimes equipped with long processes by which they are attached to the water plants. The egg itself is spherical or ellipsoidal and consists of a germ disc lying upon a very large yolk mass. The yolk is of the consistency of a rather


fiG. 48. (‘leav-age stages of Bdelloslcmuz stouti. (Redrawn from Ziegler. after Dean.) A, B, 0. surface views; D, section through edge of blustoderm showing dorsal lip.

ropy liquid, pale yellowish with perhaps a greenish cast. Our knowledge of the early development of the selachian goes back chiefly to Ruckcrt.

In a number of selachians the fertilization process is completed and the fusion nucleus undergoes two mitoses before any cytoplasmic division is to be seen, although there are exceptions to this condition. The first furrow then makes its appearance as a slight groove across the disc and a second follows more or less at right angles to it. It is an interesting deviation from the expected sequence of events that oftentimes the second furrow corresponds to the first nuclear division. The divisions continue, and by the time the 16-cell stage has been reached the furrows separating the blastomeres form a network over the surface of the egg. fiG. 49. Cleavage of A. Torpedo ocellata (16 ce1ls), B, C, Scyllmm canicula. the dog shark (64 and 145 cells respectively) (Rod:-awn from Zwgler, nftu Ruchert) VERTEBRATES 83

The direction of the cleavage spindles in the fifth division is such that part of the cells are cut off under the others and of the 32 blastomeres,

one sees at most only 20 to 24. In each case the peripheral divisions do

fiG. 50. Sections through 16- 64-cell stages and through hlastoderm at the end of the cleavage period. (Redrawn from Ziegler, after Ruchert.)

In fig. C the posterior is toward the right, and tho blastoderm, cleavage cavity,bl., periblast cells, p., and supemumerary spermatozoa, 3., are shown.

not entirely cut off the corresponding cells but some remain in connection with the yolk by means of the continuous protoplasm which surrounds the blastodisc. The progress of cleavage now serves always to increase the number of free blastorneres and the cells below the surface likewise 84 MEROBLASTIC TYPES OF CLEAVAGE

become. more numerous. For example, in a Torpedo, in which the blastodisc consists of 128 cells, it is said that about 70 of these are at the surface. In more advanced stages of cleavage the blastococle appears at first as a space beneath the growing disc. This completes the formation of the blastula.

C

fiG 51 Comparative diagrams of holoblastic and dlS(‘0ld'll eggs (Redrawn from Ziegler, after Boaz )

A, B, blastula and gastrula of the amphibian, C, D, blastula and gastrula of selachian

D

During the formation of the blastula there are to be observed around its edge, on the floor of the blastula cavity, nuclei scattered heie and there singly or in groups. These differ in appearance from the nuclei of the blastomeres, in that the chromatin is arranged in thicker masses and stains more darkly. They may be spoken of as yolk nuclei. The yolk nuclei are of double origin. The peripheral blastomeres which are in communication by means of a common circular band of protoplasm produce some of these yolk or periblast nuclei. The remaining yolk VERTEBRATES 85

nuclei are derived from supernumerary spermatozoa which enter the egg at the time of fertilization. These yolk nuclei constitute a syncytium, a layer of protoplasm with scattered nuclei which surrounds the edge of the blastoderm and is continuous with the yolk. They are concerned with the nutritive changes involved in utilization of the yolk as food material. They disappear in the later stages and take no further part in the formation of the embryo proper.

The homology of the diseoidal type of cleavage as shown by the selachian and the holoblastic as shown by the amphibian is made clear by the accompanying diagrams from Boas. The blastula stages of the two show that the blastoderm of the selachian type is comparable to the small-celled animal half of the amphibian egg, a comparison which suggests the reason why the ectoderm of the amphibian is many-celled in thickness. In the amphibian egg the floor of the blastocoele is a mass of large yolk-filled cells; in selachians it is a layer of sub—blastocoele endoderm covering the yolk sphere and the scattered periblast nuclei. The linings or the floor coverings of the blastocoeles in the two cases are homologous, and periblast plus yolk cells of the selachians is homologous to the large, yolk-filled endoderm cells of the amphibian. In the gastrula stage this homology is emphasized by the fact that the gastrular invagination takes place at a point which is the morphological equivalent of the hinder edge of the selachian blastoderm where also the gastrulation will occur in this form.

These comparisons serve to point out that there is much less of a distinction between the cleavage types of holoblastic and meroblastic eggs than seems to be the case upon superficial observation.

The cleavage of the teleosts has been described for a great many forms and there is in general a fairly close agreement in the details. The eggs show the most complete segregation of protoplasm and yolk of all the Vertebrates. Among the teleosts of the present day it is the rule that very large numbers of eggs are produced, and in line with this fact the eggs are uniformly small, varying‘ in size from that of a small pea to that of a pinhead. There are a few exceptions to this statement among some fresh-water fishes, and these, together with the sharp segregation of yolk and protoplasm, suggest that in ancestral forms the yolk may have been very much larger in quantity and the egg more comparable in size to that of a selachian or of a bird. In most selachians the yolk is spherical and the protoplasmic layer which before fertilization shows but very slight localization accumulates at one place as a distinct elevation, after the entrance of the sperm. During polar body formation and cleavage, the protoplasmic portion is sharply distinguished from the yolk, but with the growth of the blastodisc the separation becomes less 86 MEROBLASTIC TYPES OF CLEAVAGE

marked and at length the germ layers completely enclose the yolk mass. The yolk itself is at first in the form of spherules, but at the time of fertilization these run together to form a single spherical mass of glassy transparency. In many eggs, oil droplets are to be noted within the yolk which are presumed to regulate the specific gravity of the egg during

Fro. 52. Diagram of teleost cleavage. (After Ziegler)

m., egg membrane, bl, blastodisc, ps., perivitellme space, 37., yolk; 0., Oil drople pb., perxblast.

development. In the great majority of marine fishes the eggs float ai the surface of the water during their early stages.

Except for the fact that the planes of cleavage are much more regular, the segmentation of the germinal disc of the teleost egg does not differ in principle from that of the other types having discoidal cleavage. The first two furrows are meridional, the first one appearing in the shorter diameter of the ellipse, the form assumed by the blastodisc with the beginning of cleavage. The third and fourth furrows are vertical, becomVERTEBRATES 87

ing arranged so that they are practically parallel to the first and second. Thus, it is the rule that in the 16~ce1l stage the teleost egg consists of four rows of four cells each. In section it is to be noted that the first furrows do not extend to the yolk, but a continuous basal layer of protoplasm is left between the cleaving blastoderm and the yolk. The blastocoele appears at the end of the fourth cleavage by the third and

fiG. 53 Cleavage and formation of the blastoderm of the sea bass, Scrranus strarws (Redrawn from Ziegler, after H B Wilson )

A, B, C, D, are surface views, E, F, sections

fourth furrows curving around in their deeper portions to meet the preceding division planes which were perpendicular to the surface. Thus the 32-cell stage consists of a layer of superficial cells and a deeper-lying layer.

The next division results in the blastoderm becoming three-layered, and in the fourth another layer is added, while at the same time the superficial cells also become more numerous. In subsequent stages it is seen that the cells of the basal portion will divide less rapidly but with 88 MEROBLASTIC TYPES OF CLEAVAGE

this exception up to the twelfth division the nuclei divide regularly. The basal, uncleaved protoplasm gives rise to the yolk syncytium, the nuclei dividing repeatedly without cell boundaries being cut off about them. The peripheral layer of protoplasm, the periblast, enclosing the yolk mass, is continuous with this basal yolk syncytium. As development progresses, the nuclei of this layer divide regularly and assume appear— ances which are characteristic of cells whose chief function is concerned with digestion of the yolk. Multiple mitoses are observed, nuclei become numerous, are strangely lobed, and present appearances which are unlike

fiG. 54. Cleavage of the salmon, Salmo salar. (After Ziegler.) A, 16-cell stage; B, blastula.

the nuclei of normal cells but are understood when it is realized that their function requires immensely increased surface area. The cleavage cavity forms between the blastoderm and the periblast. The edges of the blastodisc thicken and gastrulation begins at a spot upon one edge of the blastoderm. The subsequent stages involve a gradual extension of the blastoderm over the entire yolk mass, steps which are concerned with the processes of gastrulation and subsequent development.

The cleavage of the eggs of Gymnophiona are among those which show the discoidal type. The earliest stages have not been observed, but the egg and the later cleavage stages are so similar to those of birds and VERTEBRATES 89

reptiles, particularly of the former, that it seems unnecessary to devote space to that here. The student of general embryology is interested in them for the contrast which they present to other types of amphibian development.

The eggs of birds and reptiles are very much alike in all fundamental respects and resemble also those of the elasmobranchs. The amount of yolk present is large and the protoplasm and yolk are distinctly separated from each other, although the segregation is less sharp. The germinal disc is more intimately connected with the yolk and at its edges


fiG. 55. Cross sections through the germ disc of the teleost, Ctenolabrus. (Redrawn from Korschelt and Heider. after Agassiz.)

gradually passes over into yolk in distinction to the sharp line of separation noted in the teleosts. The eggs of birds have been studied by many investigators and the early stages are quite thoroughly understood. The general procedure is similar to that of elasmobranchs, but the early furrows are more regular, the first two being meridional and at right angles to each other. They are then followed by a pair of vertical furrows. The irregularities are many, however, and in certain species they occur earlier than in others. In the early cleavage of the chick, for example, Patterson found that the third cleavage furrows may not be clearly recognizable. Accessory sperms enter the eggs of birds, and the phenomenon known as accessory cleavage is due to an attempt at segmentation on the part of the yolk in which these accessory sperm nuclei 90 MEROBLASTIC TYPES OF CLEAVAGE

I

come to lie. The attempt is transitory, however, and subsequently the partial furrows disappear and the nuclei degenerate. The first cleavages result in the formation of the central cells which are completely out off from the unsegmented protoplasxn, and of marginal cells which are still connected with the surrounding protoplasm. From the marginal cells new central cells are constantly cut off and new marginal cells arise peripherally. With the formation of the central cells, due to horizontal cleavages, a space is formed between them and the underlying protoplasm. This space becomes filled with fluid and is the segmentation cavity. In general the processes already described for the formation of discoidal cleavage in the lower vertebrates also apply to that in reptiles


fiG. 56. Periblast cells showing many mitoses from a. cleavage stage of Belone. (Redrawn from Ziegler, after Kopsch.)

and birds. For more detailed descriptions the reader is referred to such comprehensive accounts as those of the chick which are easily available.

III. IRREGULAR CLEAVAGE

In bringing to a close the sections dealing with cleavage it is necessary to mention certain irregular cleavages which do not fall in any of the classes previously discussed, or at least are so modified that their relationships have not yet been certainly made out. The cleavages of some sponges and of some coelenteratcs, though undoubtedly fundamentally radial, present variations from the normal type that are so great as to be understood only with difficulty. The cleavages of the trematodes and cestodes are among the most irregular of all forms. The cleavages of brachiopods and of bryozoans, although total and equal, do not follow the usual pattern. In most of the cleavage classes discussed an occasional irregular case is also to be found. Perhaps further work will bring many of these into line with the more regular forms.

BIBLIOGRAPHIC Nors

Among the more important accounts of the subjects contained in this chapter are the following: Superficial: Brauer, Korschelt and Heider, Bigelow, Heider on Hydrophilus, Cano; Cephalopods: Watase, Vialleton; Vertebrates: Dean, Whitman and Eycleshymer, H. V. Wilson, Agassiz, Kopsch, Patterson. These works are cited in full in the bibliography on page 406.

Chapter VI Types of Blastulae

It is customary to say that cleavage continues from the fertilization of the cell to the formation of the blastula. We usually think of a blastula as a hollow spherical embryo consisting of a single layer of cells, and indeed the most typical blastulae are so constructed. Actually, however, there are many different forms of blastulae, of which the hollow, onelayered type is but a single one, and these different types of blastulae are now to be .considered.

The different forms of blastulae occur as the end stage of many varied cleavage processes, as has been seen in the foregoing sections. The cleavage types are largely traceable to the amount and distribution of yolk present in the egg, a factor which differs widely in the several groups of animals. For the same reasons it is to be expected that the different cleavage types will lead to difierent kinds of blastulae, and this expectation is borne out. There are seven types of blastulae as follows: coeloblastula, stereoblastula, morula, placula, amphiblastula, superficial blastula, and discoblastula.

A. COELOBLASTULA

The simplest type of blastula is that known as a eoeloblastula, the kind having a cavity at the center. Coeloblastulae may be further subdivided, depending upon the size of the segmentation cavity and upon the relative sizes of the cells. They include both equal and unequal blastulae, distinguished as to whether the cells are of uniform size throughout the embryo, and each of these is again of two distinct subtypes, depending upon the size of the blastocoele cavity. If the altitude of the cells is low so that they resemble a sort of cuboidal epithelium, then necessarily the cavity is very large, and we have the simplest type, the equal eoel0blastula—the one with which we are most familiar, since it occurs in amphioxus. If, on the other hand, the altitudes of the cells are greater than their breadth, the cavity is correspondingly reduced; there is still a blastocoele but it is very tiny and is surrounded by a very thick cell wall (consisting nevertheless of only a single layer of cells). This occurs in Sagitta, a member of a group closely related to nematodes.

Usually in the equal coeloblastulae the cells are about the same size

91 92 TYPES OF BLASTULAE

and in about the same condition. Very evidently the equal coeloblastula is a type in which there is very little differentiation among the cells of the embryo as the cells are in approximately the same condition and of about the same size. Those at the vegetative pole usually show a slight size difference because of their content of yolk, but these cells do not have much yolk and the distinction is not very great.

Equal coeloblastulae occur in the following groups but do not include all members of these divisions. They are found in coelenterates, in nematodes, Sagztta, echinoderms, Phoroms, brachiopods, Balanoglossus, and amphioxus. It will be seen that these forms have equal cleavage which is mostly radial or bilateral cleavage. (The spiral type, however, does not entirely lack the coeloblastula, and there are a few annelids


fiG 57 Blastula of amphioxus. Fm 58 (‘oc[0b1astu1,; of 30,. (After C0I‘f0flWm0) mtta (Redrawn from Korsehelt and Heider, after Hertwig )

which rather closely approach the coeloblastula type.) Gastrula formation in types having coeloblastulae is usually by invagination; however, the method to be discussed presently, polar ingrowth, sometimes applies to this type.

The unequal type of coeloblastula is derived from the equal, with increased difference in size of the blastomeres at the animal and vegetal poles. Those at the animal pole are shorter than those at the vegetal pole. The blastocoele is not often very large and, owing to the larger size of the vegetative cells, it is pushed into the animal hemisphere. Eggs of this kind are characterized by a more sharp differentiation between yolk cells which are to form endoderm and animal cells which are to form ectoderm. The eggs are mostly spherical, sometimes a little elongated, and because of the difference in yolk content variations appear, just as in the equal type of coeloblastulae; among them are variations in the thickness of the wall, and in the size of the cleavage cavity.

The unequal coeloblastula is widespread in eggs which cleave spirally. STEREOBLASTULA 93

Therefore we should expect to find it in the polyclads, annelids, molluscs, Bryozoa (fig. 59) and among the holoblastic eggs of vertebrates (fig. 26). The blastulae of vertebrates can readily be distinguished from the other types, for in them we always find a great many cells in the wall. In the vertebrates, epithelium is differentiated into many layers of cells. It is as if this differentiation that is characteristic of adult vertebrates makes itself felt even in the cleavage stages, so that the wall of the blastula consists of many cells, and each germ layer, ectoderm and endoderm, is several cells thick. This characteristic is clearly seen in the amphibian type, the frog and salamander, with such modifications as the difference in yolk would involve. Unequal coeloblastulae are derived from unequal

.\l7i/" silt»


fiG 59 Unequal eoeloblastula fiG 60 Equal stereoblastula of flustrella hzsmda (Redrawn of Lucernaruz (Redrawn from from Korschelt and Herder, after Kcrsehelt and Heider, after Pace) Bergh)

total cleavage. Gastrulation is commonly through invagination, although polar ingrowth and epiboly also are found in these eggs.

B. STEREOBLASTULA

The stereoblastula (the term means a solid blastula) is obviously derived from the coeloblastula, and may be equal or unequal, depending upon whether it is produced from the equal or unequal type of c0eloblastula. If the cleavage cavity in the type of equal coeloblastula with small blastoeoele continues to be reduced until it vanishes, we have the equal type of stereoblastula such as is found in Lucernarza. With increase in volume of cells and decrease in size of blastocoele we get a stereoblastula.

More common than this, however, is the unequal type of stereoblastula such as we find in Crepzdula. The unequal stereoblastula is derived through unequal cleavage and may occur either in the spiral types or the more extreme of the bilateral types. Gastrulation regularly occurs in this 94 TYPES OF BLASTULAE

type by epiboly. The spiral types lead easily to this type of blastula in which by continued growth the ectoderm cells will surround the endoderm cells and so form a gastrula by epiboly.

r C. MORULA

A second type of blastula in which there is no blastocoele is the morula. It was formerly customary to include this stage in almost all the types; that is, it was said that the morula followed the 16-cell stage, and in the strictly radial type there is some reason for that description, but we do not speak now of a morula stage. However, in some types there are formed blastulae which can best be described as morulae or solid blastulae. In Clava we have an example of the solid blastula which illustrates the difference from the stereoblastula type, for inside the morula there are cells, whereas in the stereoblastula there were no cells which did not


fiG. 61. Unequal storeoblustulu of Crepidula. (After Conklin.)

have a boundary at the surface of the egg. Superficially the two are quite alike, but actually there is an important distinguishing feature. The morula is produced by a characteristic shifting of the spindle position during cleavage. In all the other cases that we have dealt with the spindle may be said to occupy a paratangential position; the result is that the new cleavage plane divides the cell in such a way that part of it touches the surface and part the center of the egg. However, the morula comes about by a shifting of the spindle to a radial rather than a paratangential position, and the result is that some of the daughter cells touch the surface and others are only in the interior of the egg. So the morula, although superficially similar to the stereoblastula, is really a distinct and different type. Morulae occur chiefly in coelenterates.

D. PLACULA

The placula presents another kind of modification which has been produced from the equal coeloblastula. Let us suppose that, instead of SUPERfiCIAL BLASTULA 95

the cavity vanishing, the egg is compressed from the animal to the vegetative pole. The result would be a flattened blastula consisting of two plates of cells. This is the placula and is found especially well developed in the ascidians and to a less extent in the nematodes. The edge of the placula corresponds to the equator of the coeloblastula, the upper layer

of cells to the animal hemisphere, and the lower layer to the vegetative hemisphere.


Tie. 62 Morula of (‘lava 9qua- fiG 63 Placula of Cynthia pamta (After mam (Redmwn from Korschelt and Conklin) Heider, after Harm )

Gastrulation takes place by two different methods, epiboly and the sinking in of the flattened plates; that is, it is accomplished by a combination of epiboly and invagination.

E. AMPHIBLASTULA

The amphiblastula of the sponge is of somewhat different type. This structure was first described by Haeckel for the free-swimming larval stage of calcareous sponges, and hence does not strictly correspond to other blastulae which we have described. This larval form, however, is usually spoken of as an amphiblastula. The cells at the animal half are very sharply distinguished by their small size and ciliated covering from those in the vegetative part of the egg. This type is not particularly important although it is necessary to include it.

F. SUPERfiCIAL BLASTULA

The superficial blastula, or periblastula, is characteristic of those forms having superficial cleavage, an example of which is the crab, Dromza (figs. 36f and 37d). The result of superficial cleavage is the formation of a layer of cells around the inner yolk mass. There is no blastocoele and it is usual to say that the blastocoele is occupied by the 96 TYPES OF BLASTULAE

yolk mass. But the case is not quite so simple. Actually it will be recalled that the superficial cleavage resulted in the formation of blastomeres which at first were continuous with the yolk at their inner end. These blastomeres presently are completely out off, a protoplasmic blastomere being separated from the yolk-laden inner mass. Their inner ends, or the outer part of the yolk mass, therefore, is not homologous to the cavity. It is only that very small part of the mass which was never segmented at all which is homologous to the cavity.

Reference has already been made to the role of the yolk cells, the vitellophages within the yolk mass Some of the nuclei during cleavage remain behind and are presently to be described as yolk cells for they


fiG 64. Amphiblastula of Sycandra mphanuv (Redrawn from Korschelt and Helder. after Schulze )

digest the yolk. In this process the yolk becomes divided into areas around these nuclei, a process of division which is often spoken of as the yolk cleavage. But by some these nuclei are regarded as endoderm. If this latter VIOW is adopted, there would be no such thing as a superficial blastula because the embryo would consist mostly of two cell layers, the outer being ectoderm, and these internal yolk cells endoderm. This designation of these cells as endoderm has not, however, come into general use. Rather we say that the superficial is a true blastula.

G. DISCOBLASTULA

finally we have the discoblastula, the end stage of the eggs having discoidal cleavage. It is derived from the unequal coeloblastula (fig. 52) upon the assumption that the yolk becomes so abundant and so dense as DISCO BLASTULA 97

to hinder quite completely the separation of the cells in the vegetative half of the egg. Recalling that discoidal cleavage occurs both in the vertebrates and invertebrates we should say at once that discoblastulae are of two sorts, the vertebrate type (fig. 55) and the invertebrate (fig. 44); the latter consists of the single layer of cells which is found in all invertebrates having diseoidal cleavage in contrast to the former which is of many cells. Usually in all types having discoidal cleavage there are some cells, perhaps around the edge of the disc or perhaps elsewhere, which are continuous with the yolk. These cells, however, usually do not take an active part in the formation of the body of the embryo. In the vertebrates these cells are designated as the periblast or the yolk sac endoderm. In the cephalopods they are the blastocones. Gastrulation is usually by the limited type of invagination, invagination taking place in one segment of the disc only.

These are‘ the different types of blastulae. They are obviously related by the differing types of cleavages and they lead us to the different types of gastrulation which is the next step in the development of the animal’s body.

BIBLIOGRAPHIC Nora

Among the more important accounts of the subjects contained in this chapter are the following: Korschelt and Heider, Minehin, Maas, Hertwig, Wilson, Conklin, Schultze, Brauer, Whitman and Eyclcshymer, O. Herting, Ziegler, Brooks and Bittenhaus. These works are cited in full in the bibliography on page 406.


Chapter VII Endoderm Formation

I. METHODS OF GASTRULATION

After the formation of the blastula, which in its simplest condition is a spherical mass (usually hollow) of more or less undifferentiated



\\

I 


is


fiG 65 Two stages in the gastrulation of Terebratulma septentnonalts (After Conklm.)

cells, the next stage in the development of the embryo is the formation of a gastrula. The gastrula develops from the blastula by the differentiation of two layers of cells, an outer or cctodermal layer, and an inner or endodermal layer. From the eetoderm develops the nervous system and the outer parts of the future animal, and from the endoderm comes the lining of the alimentary canal.

There are several different types of gastrula formation, depending partly on the type of blastula preceding the gastrula. We shall consider each of these types and describe its method of formation.

A. EMBOLIC GASTRULATION

The best-known type of gastrula is the embolie or invaginate gastrula. Gastrulae of this kind occur in embryos with total cleavage, resulting in cells of either equal or slightly unequal size. The blastula resembles

a. hollow sphere whose wall, except in vertebrates, has a. thickness of one cell. A blastoeoele cavity is often, though not always, present inside the sphere, but sometimes it is quite restricted, as in Terebratulina, a. brachiopod which has a thick-walled type of coeloblastula. The cells of the blastula are often wedge shaped, with the wedge narrowing inwardly.

98 EMBOLIC GASTRULATION 99

In one part, the vegetative half, the cells are typically larger than elsewhere, and sometimes markedly so.

The first sign of gastrulation is a slight flattening of the vegetative region. This flattening gradually deepens and the resulting gastrula has the appearance of a rubber ball which has been pushed in at one point by pressure with a finger. The inpushing of the cells at the vegetative pole continues until this invaginated layer lies close to the cells of the outer wall. In this way a two-layered gastrula is formed and two cell layers are differentiated. The outer or ectodermal layer covers the gastrula and is continuous with the inner or endodermal layer at the


fiG. 66. Gastrula of amphioxus. (After Cerfontaine.) Oriented with respect to the future embryonic axis.

point of invagination. Between the two layers there remains for a while a cavity which is the remnant of the segmentation cavity or blastocoele. The blind cavity, which communicates with the outside through a single blastoporal opening and which is formed by the inturned cells as the lip of the depression gradually narrows, is the primitive gut cavity, or the archenteron.

It will be seen at once that the conditions in an invaginate gastrula closely resemble those of the adult coelenterate which has two cell layers and whose gut has a single opening to the outside. However, it is to be noted that in only a few coelenterates are the gastrulae formed by invagination, and that the same result in these forms is attained in another way.

The mechanism which causes invagination has been attributed by different workers to different causes. Rhumbler regarded it as an active 100 ENDODERM FORMATION

attempt at migration by the cells of the vegetative half, a process which in the last analysis is to be attributed to chemotactic influences. If this explanation is correct, then the migration of the endodermal cells must be connected with a change in surface tension at the boundary between the endoderm and the blastocoele content, especially in the region of the cells which undergo invagination.

Some of the causes which play a part in the invagination may be the following: (a) Differences in the rate of growth between the ectodermal and endodermal portions of the blastodcrm by which a lateral pressure is exerted on the endodermal plate. (b) Resistance of the closely pressed egg membrane, so that the surface increase of the blastodcrm is possible only internally. This factor is probably not often effective, for in many cases the egg membrane appears pushed away by the pcrivitelline fluid and the blastocoele is not an empty cavity but is filled with fluid which would have to be displaced. (c) The constantly decreasing fluid of the blastocoele which perhaps exerts a sucking effect on the endodermal plate. We must at the present time regard this factor as of doubtful occurrence and significance.

The size of that part of the old segmentation cavity or blastocoele which remains after gastrulation may be very small, as in amphioxus, or it may be quite extensive, as in the echinoderms in whose embryos the primitive gut is relatively small. The fate of the fluid or gelatinous content of the blastocoele is uncertain; some authors think that it is resorbed by the endoderm cells. If this process could be satisfactorily demonstrated it would be regarded as a causal factor in gastrulation.

A monaxial structure, with the axis from the middle of the blastopore opening to the opposite pole, is characteristic of the early gastrula. In many forms the gastrula becomes later bilaterally symmetrical as the blastopore becomes narrowed and the gut laterally compressed. In most coelenterates the monaxial structure remains.

A special type of gastrulation occurs in Lumbricus and the ascidians. Here the blastula is a placula having a two-layered, plate-like structure. Gastrulation is brought about by the hemispherical inbending of the placula which then rounds out so that a complete sphere is formed. In some cases there is an active increase by epiboly in the ectodermal cells preceding invagination. This may be one of the causes for the invagination in placulae, but on the other hand the process may be due to the same causes that lie back of typical invagination.

Invagination occurs in the following forms: some actinians, some syphopolyps; Sagitta, Pedicellina, brachiopods; Phoronis, nemerteans; echinoderms; some arthropods, as crayfish, Palimonetes; some insects; many annelids, as Polygordius, Podarke, Eupomotus; some molluscs, as EPIBOLIC GASTRULATION 101

Chiton, Dentalium, Dondersia; lamellibranchs, as Cyclas, Pisidium, Unio, Ostrea; gasteropods, as Paludina, Planorbis; Balanoglossus, amphioxus; the vertebrates in general.

It will be observed that this type of gastrulation is typical of primitive forms. Hence it is most striking that very few eoelenterates belong to this group. Invagination with a preceding placula includes the following: some nematodes, some ascidians, some Lumbricidae. Many forms are transitional between the type of pure invagination and the Dlacula type.

B. EPIBOLIC GASTRULATION

In the invaginate or embolic gastrula just described, the blastomeres were approximately equal in size. In many other embryos, however,

fiG. 67. Gastrulation by epiboly in Crepidula. (After Conklin.)

there is a great difference in size between the small cells at the upper or animal pole and the large cells at the lower or vegetative pole. The small cells are called micromeres, and the large ones which contain much yolk and are few in number are called the macromeres. In the blastulae of embryos which have undergone this kind of cleavage, the cleavage cavity is small or absent.

It is obvious that there is no room for invagination of endoderm cells 102 EN DODERM FORMATION

in embryos with practically no cleavage cavity. Gastrulation, which cannot be embolic, occurs in the following way. There is a multiplication of the small cells at the animal pole and an overgrowth or migration of these cells down over the larger cells at the vegetative pole. These large yolk-filled cells seem to take no active part in the process. The free edge of the growing cap is called the blastopore, and the protruding yolkfilled cells, the yolk plug. When the overgrowth by the small cells is complete, the blastopore usually closes and the large cells are enclosed. The small, overgrowing cells are ectodermal and the large yolk cells endodermal. A gut cavity is not present at first but is formed later by a splitting and solution of the yolk in the solid endoderm cells. The cause of epiboly, or gastrulation of this kind, has usually been ascribed to the activity of the micromeres, but there is no evidence of a lack of activity on the part of the large, inwardly migrating macromeres.

The part of the gut so formed is known as the mesenteron, for it is the middle portion of the entire tract. The anterior end, or stomodaeum, and the posterior end, or proctodaeum, are formed by ingrowth of the ectodermal cells which later unite with the mesenteron so that there is a continuous lumen through the gut.

There are many transitions between epibolic and embolic gastrulation. If in the embolic gastrula the endoderm cells are larger and the lumen of the invagination correspondingly smaller, then the gastrulation approaches the epibolic type.

Epiboly is very widespread and occurs in all cases where the eggs are sharply telolecithal and where there are, as a result, size differences of the cells at the animal and vegetative poles.

Epibolic gastrulation occurs in ctenophores (fig. 14B), rotifers, turbellarians, some molluscs, some annelids, and many crustaceans including many parasitic copepods.

C. POLAR INGRESSION

1. Restricted Unipolar Ingression

In some cases of gastrulation there is neither a sharp invagination nor an epibolic overgrowth. In these cases there is a total, unequal cleavage, resulting in an embryo with a micromere cap resting on a few large yolk-laden cells. The micromeres continue to multiply, and a blastula is formed of cells of very unequal size; in it a well—developed blastocoele is present. The large cells, never many, the common anlage of mesoderm and endoderm, reach the interior not by invagination or epiboly, but through their own active inward migration.

The mechanism by which the large cells get into the interior is little MANY-CELLED UNIPOLAR INGRESSION 103

understood, and the term polar ingression is not adequately applied. This method of gastrulation is often not sharply separated from either of the preceding types.

The following forms have gastrulation by restricted unipolar ingression: some holoblastic Crustacea (some schizopods and Cladocera), Ascaris megalocephala and other nematodes, and some molluscs (Patella).

2. Many-Celled Unipolar Ingression

In the ciliated blastulae of the coelenterates occurs a second form of gastrulation by polar ingrowth. In it there is an elongated, oval or sausageshaped, free-swimming stage (called a planula) which is really a blastula with a large blastocoele and with thickened cells at the posterior pole. Here there takes place the migration of cells to a position within the blastula which is responsible for a second type of unipolar ingression. This migration extends from the pole over the nearby portion of the embryo. The cells which first migrated into the blastocoele lie isolated in the jelly contents but, later,

when migration takes place en masse, Fm. ex. Endoderm formation in ‘the a plugof cells turns inward from the fgiggigfi 1;;j’;m”“,§,§r;$g;‘“;n';*8',§:§g;';; posterior pole and gradually fills the after Patten.)

blastocoele. The migration of cells in ward is not limited to the vegetative pole, but reaches to neighboring parts. There is no interruption in the continuity of cells at the hinder pole, and no gap in the outer superficial cell layer. At the end stage of the gastrulation, there is an embryo with an outer superficial epithelial layer and with a solid cell mass filling the interior of the larva. This stage is variously called a stereogastrula or a parenchymella.

The formation of the gut cavity follows later by dehiscenee. A gradually widening split occurs in the interior of the endoderm cell mass and later breaks through to the outside, forming the mouth. During this process, the endodermal cells become arranged in a layer.

It will be seen that there is a close relation between gastrulation by invagination and gastrulation by polar ingression. Both methods might be regarded as modifications of one process. In the invagination process a closed epithelial layer is shifted by infolding to the interior, and in the ingrowth process the cells of the vegetative half pass inward as a solid cell mass, later taking on an epithelial character, and develop104 EN DODERM FORMATION

ing a lumen. Metchnikoff concluded that the polar ingression was brought about by a simple migration of cells without differential division.

There are transitional types between gastrulation by invagination and gastrulation by polar ingrowth. In many forms, as in Aurelia aurita

fiG. 69. Endodenn formation by unipolar ingression in the plrmuln of Aequoria according to Claus. (Redruwn from Korschelt and Heider.)

and Eupomotus, there are invaginate gastrulae in which the gut lumen is reduced to a very narrow split. If we think of the originally solid invaginated mass as broken up into cellular parts, we have a picture of

unipolar ingression. DELAM INATION 105

Examples of unipolar ingression are found in the following forms: hydroids which have free medusae and whose eggs produce ciliated swimming blastulae (Tima and Obelia), some anthomedusae, some scyphomedusae, and some leptomedusae. This type of gastrulation is widespread in arthropods.

3. Multipolar Ingression (Apolar Ingtession)

A process similar in many respects to the two types of polar ingrowth just described and perhaps related to those types is that of multipolar ingression. It differs from the preceding only in the inward movement of a small number of cells from several places instead of a single one on the surface of the blastula. It might be spoken of as apolar ingrowth as distinguished from that which proceeds from a single restricted portion of the blastula. However, since the processes are so similar to those already described in this section it seems desirable to assign this type to the same division even if it presents some departures from the other cases placed here.

Multipolar ingression occurs in coeleblastulae when cells, few in number at first, pass inside the embryo from various places on the surface. The blastocoele is in this way filled up with endoderm. The resulting stage is a solidly built mass of cells like a morula. It may be called a pseudo-morula, differing from the typical morula in that there is no differentiation of cells in the latter _ Fm. 70. Multipolar ingreswhereas here the endodermal cells, now a ?‘§:d‘?a$:”°;::f:‘§’Zg;;:fl“Z:‘§ solid mass, have already arisen by an inward Heider. after Metchnikofi.) movement of some of the outer cells. The gut cavity appears later inside the endoderm. Cases of this sort of endodermal formation seem to be rare. The best investigated case is that of Aeginopsis (Metchnikoff).



D. DELAMINATION

In the cases already studied, there was a separation of the inner or endodermal layer from the vegetative pole, or from the vegetative half of the embryo. There is, however, another type of endodermal formation, common in coelenterates, in which there is no polar localiza106 ENDODERM FORMATION

tion of endoderm-forming cells, for in these the endoderm comes from diffused parts of the embryo. The endoderm may arise in one of the following ways: by migration into the coeloblastula from visible spots in the embryo, by cutting off from the cell wall of the coeloblastula by division, or, when the end stage of cleavage is a solid embryo, by histological differentiation of an epithelial outer layer from the parenchymous inner mass. There are many types which belong here. It will be observed that multipolar ingrowth might from some points of view be included under this heading. The term delamination has been used to bring together processes of different kinds and is no longer a definite term of definite meaning. Many of the forms intergrade with each other through transitional stages. It is best to consider, under the head of delamination, all cases of endoderm formation which are not derived from invagination, epiboly, or polar ingression (including multipolar ingression).

Delamination occurs in those forms whose embryos are set free late in development either from spore sacs or from eggs with membranous and gelatinous coverings. Many forms classified here belong to the intergrading or mixed type of endoderm formation.

1. Coeloblastic or Mixed Delamination

When, in a coeloblastula, paratangential division planes which are differential in character cut off single cells into the interior of the blastoeoele and these subsequently become arranged into a layer, coeloblastic delamination may be said to occur. These inner cells constitute the endoderm and at length fill the blastocoele. By dehiscence within them the gut subsequently arises. In many cases of this mixed delamination, there is a combination of the origin of endoderm by cell division and by multipolar migration. Many of the hydroids, of which Hydra is the best example, show this mixed delamination. Geryonia, the actinians, and some syphomedusae have coeloblastic delamination.

2. Morula Delamination

In morula delamination, also called secondary delamination, cleavage results in the formation of an embryo without a blastocoele, that is, in one solid from the first. Early in cleavage there occur both radial and paratangential division planes with no histological differentiation resulting between the inner and outer cells. An embryo arising in this manner is a true morula in which a cleavage cavity never develops. Haeckel thought that the morula, the stage of solid aggregates of blastomeres, always preceded the blastocoele. But it is now well known that a MORULA DELAMINATION 107

blastocoele cavity appears in some forms as early as the 4-cell stage, and that true morulae, as the above, are formed only in certain cases. In multipolar ingrowth and in coeloblastic delamination, the pseudo fiG 71. Hydra embryo (Redrawn from Korschelt and Heider. after Brauer)

A, showing early migration of some endoderm cells inward and the origin of others by cell division. B, a later stage in which the endoderm fills up the cauty

morula follows the blastocoele stage instead of preceding it, differing from Ha.eckel’s description of a typical embryo.

In morula delamination, differentiation of layers follows the solid stage of undifferentiated cells. In Clava (fig. 62) the cells at the surface 108 EN DODERM FORMATION

take on a prismatic character and lose their polyhedral shape. An undulating line of separation is first formed between the outer or ectodermal cells and the inner or future endoderm cells. The basement membrane is later differentiated, and the inner cells connected with it become epithelial. The cells adjoining them lose their yolk content and take positions among the outer endodermal cells. The innermost cells of the yolk mass finally liquefy and are resorbed, thus giving rise to the gastrula cavity. The formation of a definite endoderm is accomplished, and the planulae, now ciliated, swarm out.

Morula delamination occurs also in

Trachymedusae, Siphonophora, in alcyonians, Stauromedusae, and Cubomedusae.

3. Syncytial Delamination

Syncytial delamination occurs in those coelenterates whose embryos show a similarity to the superficial cleavage of arthropods. In these embryos, only a few cell boundaries may be seen, and there is a solid syncytial inner mass, instead of a morula stage. The ectoderm becomes

fiG. 72. Endoderm formation separated from the inner mass, which in

3;affggaogmgfgjgggigglzfiggg; part forms the endoderm and in part

layers by difierentiation. (Redrawn gradually is used up. ‘mm K°“°h°” '”‘d Held” me’ In Turritopsis there is at first total Hum) cleavage, but in later stages the blastomeres flow together and form a syncytium. In this case the syncytial nuclei at the surface multiply, cell boundaries cut in and a delicate basement membrane is formed. Differentiation of the endoderm comes later, when its cell boundaries begin to appear. The primitive endoderm cells are irregularly disposed, but later, when a split forms inside, representing the gut cavity, they are definitely formed into an epithelial layer. In the hydrocorals, according to Hickson, there is no separation into blastomeres and the embryo is a syncytium from the first, recalling the cleavage of insects. Nuclear fragmentation of the first cleavage nucleus has been described in these forms as the source of the nuclei of the plasma islands, which arise, according to this account, from regenerating chromatin particles. About the plasma islands cell boundaries appear, and later the ectoderm becomes differentiated as a layer and development proceeds.

There is considerable doubt as to whether all the cases classified as SYNCYTIAL DELAMINATION 109

syncytial belong here, as different authors give different accounts for the same material and describe many doubtful processes. Some of their

fiG 73. Development of Turruopsts. (Redrawn from Korschelt and Helder, after Brooks and Rlttonhouse )

A. morula. B, fusion 01 blastomeres, C, young planula Wltl) definitely formed ectoderm.

material may be improperly fixed, and a reinvestigation may furnish more complete knowledge of their development. Many hydroids probably belong in this group which develops by

syncytial delamination. l 10 ENDODERM FORMATION

II. THE DISCOGASTRULA A. VERTEBRATES

All the forms of gastrulae studied so far have eggs in which there is not a great quantity of yolk. In those forms, however, which have a discoblastula, a mass of yolk occupies the greater part of the egg and

Fm 74. Gastrulation in Petromyzan fluvumlis (Redrawn from Ziegler, after Goette) A, B. beginnings of gastrulation, C, formation of an anlage of the medullary tube.

the protoplasmic part is limited to a small disc at one end. The inert yolk is incapable of division and the protoplasmic disc alone undergoes segmentation. Gastrulation usually takes place by the inturning of the edge of the disc and the spreading out of this inturned layer between the protoplasmic disc and the yolk mass. This inturned layer is the endoderm and the two—layered embryo thus formed is a. discogastrula. VERTEBRATES 1 1 1

The discogastrula lies on top of the yolk and spreads around it. The edge of the embryo is the blastopore.

In order to understand this process of gastrulation thus briefly described it will be necessary to take up at greater length the gastru |IIIIIIIlIn.,,’ __....§ 4"""lIIn\:

fiG. 75. Series of diagrams showing gastrulation. (After Ziegler.)

A, B. sections through embryos of an amphibian or a dipnoan in the stage of the circular blastopore; C, gastrula of a hypothetical intermediate between Amphibia and Amniota; D, gastrula of a reptile. y., yolk plug; ec., eetoderm; bl., blastocoele; g., gastrocoele; m., medullary plate; d.. dorsal lip of the blastopore; s., subgerminal cavity.

lation of the frog (figs. 22, 51, and 74-76); although its egg has total, unequal cleavage and gastrulation is therefore chiefly embolie, the study of its egg enables us to interpret much better the conditions in a true discogastrula. In the lower or vegetative part of the frog’s egg, the white portion, there is an accumulation of yolk material; the animal half or dark colored part of the egg, however, is not entirely devoid of it. I12 ENDODERM FORMATION

Because of the small amount of yolk the animal half divides more rapidly than does the vegetative half. Cleavage thus results in an embryo with large and small blastomeres, the larger ones serving to force the cleavage cavity nearer the animal pole. Between the pigmented and the lighter portions of the egg is the gray crescent. The bilateral arrangement of the egg substances is shown in some amphibia, but the appearance of the so-called gray crescent which is similar to that of the ascidians cannot always be made out.

fiG. 76. Development of embryo of Rana showing closure of blastopore, formation of neural folds, and development of body form.

Invagination begins as a slit-like groove at the border of the gray crescent somewhat below the equatorial region. The large amount of yolk in the vegetative region prevents an equal invagination. The slit—like invagination is the dorsal lip of the blastopore. The invagination gradually extends to each side of the gastrula and the groove becomes crescent shaped.

Previous to the invagination a change in the distribution of the black pigment has occurred, for the small black cells have started to move down over the white cells and the black pigment extends below the equator. It will be seen at once that overgrowth, or epiboly, as well as invagination, plays a part in gastrulation of the frog’s egg. VERTEBRATES 1 13

The crescent groove follows the border of the pigment zone as the latter gradually extends over the yolk and represents the dorsal side of the egg. The ventral hp of the blastopore appears later, when invagination takes place there, and the blastopore then becomes circular. The dorsal lip advances over the yolk more rapidly than does the ventral, probably on account of the greater amount of yolk in the latter region. The gullet, formed by invagination, is of a circular, s1it—like character, and the yolk mass extends as a plug in the primitive gut lumen. As the



. B Bio 77. Embryos of Rana A at time of first indication of gill slit, B, Just before appearance of external gills at time of hatching

ring-shaped blastopore grows together, owing to the greater downgrowth of the dorsal lip, it draws down on the yolk plug and finally becomes a small median, slit-like furrow. This process of the growing together of the edges of the blastopore is concrescence We may then regard concrescence as a third factor in the gastrulation of the frog.

At first the dorsal, and later the ventral, blastopore lips become differentiated with distinct ectodermal and endodermal layers. The cells of the yolk mass, which have extended as a plug in the blastopore, become pushed within as the blastopore grows together. We might thus 1 14 ENDODERM FORMATION

consider this kind as a solid cell ingrowth, perhaps a fourth factor in gastrulation.

Four factors may be said to enter into the gastrulation of the frog’s egg: invagipation, epiboly, concrescence, and a solid cell ingrowth.

a. Selachians. We may now contrast the selachian egg with that of the frog. In the former, a protoplasmic disc rests on the top of the yolk mass, and there is thus a sharp division between protoplasm and yolk, instead of a gradual transition as in the frog. The disc—shaped protoplasmic mass of the selachian becomes furrowcd by cleavage planes, but the yolk mass remains unsegmented. That part of the endodermal mass of the frog which we have called the yolk plug must be represented in the selachian by the uncleaved yolk mass. Although the yolk does not cleave, in it are to be found scattered nuclei of various origins, but these nuclei appear to take no further part in development. Some of the scattered nuclei may be metamorphosed sperm nuclei, for polyspermy exists in the selachians. A part of the nuclei originate from the peripheral cleavage


fiG. 78. Median section through the gastrula of Torpedo (After Ziegler)

cells and are called the periblast cells. These periblast nuclei are comparable to the eephalopod blastocones; that is, they are blastomeres not cut off from the yolk mass by cleavage.

In the selachians the cell mass of the germ disc forms a many-layered embryo which lies in a depression in the surface of the yolk. The cells of this mass are at first round, indifferent cells, not arranged in an epithelial layer. Between the cell mass and the surface of the depression a space known as the germ cavity appears which may be regarded as the cleavage cavity. It does not extend equally under the embryo, but is pushed toward one side which corresponds to the hinder end of the future embryo.

The first change in the germ disc of the selachian is the formation of an epithelial layer from the superficial cells which become flattened and broadened. This layer begins to form at the hinder part of the embryo where the cleavage cavity is larger and the germ disc thinner and spreads from this region over the whole germ disc.

Gastrulation begins as a depression at the hinder edge of the germ disc where the cells begin to turn under. Thus is formed the primitive gut cavity, lying between the inturned cells and the surface of the yolk VERTEBRATES 1 15

which has previously become covered with so-called periblast. The invaginating cells are formed from the round cells of the blastoderm, spreading as an iris-like ingrowth from the edge of the germ disc and of the growing epithelial endoderm. The invaginated gastrula cavity is at first crescent shaped, comparable to that of amphibians, but with an axial cavity in addition to the peripheral cavities of the crescent. The edge of the entire germ disc may be thought of as a blastopore.

fiG 7‘) G1-«itriilitiam of the salmon. Salmo salar; ll. growth of the bl i-itoderm of the salmon, (‘, emlirvonal shield stage, the germ ring covering one-li ilf of the yolk (After Ziegler )

The anterior edge of the blastopore becomes extremely active and begins to grow down over the yolk. finally it grows entiiely over the yolk, passing over the vegetative pole, and reappearing behind the embryo as the ventral lip of the blastopore. The yolk thus becomes entirely covered and the blastopore eventually closes.

b. Teleosts. In the teleosts the process of gastiulation is essentially similar to that in the selachians. The formation of the blastopore begins at the posterior edge of the germ disc where invagination bi iiigs about the origin of the primitive gut. There is a slight invagination at the lateral and anterior edges also, and the yolk is finally enclosed by the blastoderm, the anterior margin becoming the ventral lip of the blaste1 16 ENDODERM FORMATION

pore. In the elasmobranchs, teleosts, and also in the myxinoids, there are two periods in the closure of the blastopore. During the first period the overgrowth is practically limited to the dorsal lip, and the material for the formation of the body of the embryo is produced. During the second, the lateral and anterior margins of the blastoderm gradually cover the yolk. Thus only the dorsal lip takes part in the formation of the future embryo, while the lateral and ventral lips are entirely extraembryonic.

c. Reptiles and Birds. In all the vertebrates thus far described, the Anamnia, the blastoporic lip appears at the edge of the blastoderm. In the reptiles and birds, which have embryonic membranes and hence belong to the Amniota, the blastoporic lip lies wholly within the blastoderm. The archenteric cavity is well developed only in primitive forms and is usually represented only by the neurenteric canal. In most cases


fiG. 80. Gastrula of pigeon. (After Patterson.)

Thirty-six hours after fertilization. Section through the posterior portion of the blastodisc showing the blastopore and its dorsal lip, d.b.

the upper layer or future ectoderm alone gives rise to the blastopore and archenteron.

In the chick the blastoderm or germ disc lies on top of the yolk mass, as in the fish. The endoderm is formed by an inturning of the germ disc at the posterior margin and by ingrowth from the inturned portion. At the posterior part of the germ disc the primitive streak is formed by a linear thickening of the upper layer of the blastoderm. The endodermal layer in the chick gradually grows around the yolk and the yolk sac is thus formed. The ectoderm does not directly cover the yolk sac, however, as here conditions are complicated by the presence of embryonic membranes, the amnion, which encloses the embryo, the allantois, and the chorion.

In the chick the primitive streak represents the fused lips of the margin of invagination and therefore is to be considered as the closing blastopore. In the primitive streak the germ layers are fused, the differentiated part of the embryo being formed in front of it, the anus at the posterior end, and the neurenteric canal at the anterior end. We must o


d-b- v.b.

i J fiG 81 Dlagram to Illustrate dxfierence between the blastopores of Annmnm and Ammcte. (After Jenklnson )

a—c Closure of blastopore 1n frog or sxmxlar form Stlppled reglon 1s the blastoderm. The edge of the blnstoderm represents the edges of the blastopore d-—f Ventral hp of blustopore xs absent m such a. form as Lemdoszren The heavy solld lxne represents the portlon whmh forms the lips of the blastopore g, h Only a. small part at the postenor end becomes the blastopore as In the Gymnophlona. The yolk remams uncovered 1. J The condxtlon of the blastopore 1n Ammota The embryomc shleld IS darkly stlppled and Is equwalent to the entxre blastoderm of the Anamma The ammote blustoderm extends further as mdxcated by the hght stxpplmg 11 8 EN DODERM FORMATION

therefore consider the primitive streak of the bird as an elongated blastopore since the relations are similar to those found, for example, in the frog.

In the reptiles there IS a so-called embryonic shield at the posterior end of the blastoderm. This IS a circular or oval area of columnar cells resting upon a lower layer and surrounded by a region of flattened cells.


\


B C

fiG 82 Bali'our’s diagrams showing homology between bliistopore and the primitive streak (After Ziegler )

At the posterior margin of the embryonic shield the two layers come together A depression in the primitive plate appears here which is the beginning of the archenteron, and its anterior margin is the dorsal lip of the blastopore Lateral lips which are formed later turn back and fuse, in some cases forming a vertical or even actual ventral lip, although cases occur in which there is no ventral lip at all.

A mass of primitive cells surrounded by the dorsal and lateral lips SCORPIONS 1 19

corresponds to the yolk plug. It will be seen that cells which are the morphological equivalents of the yolk cells of the Amphibia are thus to be found in the reptilian blastoderm. Here, as in the birds, the blastopore arises inside the blastoderm and not from its edge as in the Anamnia. The comparison of the Anamnia and Amniota can best be understood by observing the development of the gymnophionan egg. Here the blastoderm is an oval layer of columnar cells resting upon a partly segmented yolk. Only a part of the edge of the blastoderm at its posterior end is converted into a blastoporic lip which is at first dorsal. Later the lateral lips turn back around a small part of the yolk, and then join to form the ventral lip. The anterior part of the blastoderm thus plays no part in the formation of the blastopore. In this form the yolk remains uncovered. We have seen that, in other Anamnia, the ventral lip develops from the anterior edge of the blastoderm and the yolk is necessarily covered where_the blastopore closes.

The embryonic shield of the Amniota must be represented, in the Gymnophiona, by the blastoderm, and the marginal zone of the amniotes, together with the lower layer with which it is connected at the primitive plate, must be represented by the yolk cells or nucleated yolk. It seems natural to suppose that in the transition from forms like the Gymnophiona to the higher vertebrates, as the yolk material in the egg increased in amount, segmentation has become restricted, not to the blastoderm alone as in the fishes, but to the blastoderm and those adjacent and subjacent cells which in the Gymnophiona are partly segmented from the yolk.

These points may make it clear why the blastopore of the amniote is formed inside the blastoderm but at the edge of the embryonic shield which is really equivalent to the anamnian blastopore.

B. SCORPIONS

The discoidal type of gastrulation is not limited to the vertebrates alone, for the scorpion and the eephalopod eggs are also of this type. Gastrulation is of course dependent on the structure of the egg, and an egg with a protoplasmic disc resting on a large yolk mass will belong to this type, regardless of whether it is an invertebrate or a vertebrate egg.

The scorpion egg (fig. 39) is rich in yolk and the cleavage of the egg is discoidal. In young stages there is found a small, one-layered cap on the yolk. The blastoderm spreads gradually from this point and advances over the yolk. Scorpion eggs, since they have cleavage of this type, are comparable to eggs in which there is superficial cleavage with early formation of the blastodisc on one portion of the egg only. The scorpion condition is probably an extreme case and is to be traced back to the 120 ENDODERM FORMATION

type which is widespread among the arachnids. The scorpion egg, therefore, represents a modification of the type common to its group (as is also indicated by its viviparous mode of development).

The endoderm arises by the differentiation of the cells of the germ disc which lie next to the yolk and form a regular epithelium. The irregular cells which remain between the outer layer or ectoderm and the inner or endodermal layer become arranged into two symmetrical mesodermal bands.

It will be seen at once that in the scorpions, as in the myxinoids, the endoderm does not develop from the edge of the germ disc and thus the edge of the germ disc cannot be regarded as the blastopore.

C. CEPHALOPODS

The cephalopod eggs are unusually rich in yolk and consequently they are considerably larger than are the eggs of other molluscs. There is a considerable difference in egg size throughout the group, but the yolk takes up by far the most of the egg. The entire egg is covered with a thin layer of protoplasm, which becomes thicker to form a disc at the upper or future animal pole. The germ disc thus formed is sharply marked off from the yolk mass.

The cephalopod egg is bilateral even before cleavage sets in. At the part of the germ disc which is to become the anterior end of the embryo, the disc extends farther down toward the equator. Since the cleavage furrows pass into the thin layer of protoplasm surrounding the yolk, the first cleavage cells and later the outer cells of the disc, the blastocones, are not cut off from the peripheral protoplasm. The germ disc spreads out and increases in size, at first chiefly at the expense of the formative yolk with which the blastocones are connected. The germ disc, one cell in thickness and covering only a small part of the egg, becomes thickened at the periphery as it spreads. When the cleavage cells have increased to a considerable number the peripheral blastocones become detached from the germ disc. These cells, according to Vialleton, wander beneath the germ disc and become arranged into a layer which spreads over the food yolk, forming a yolk epithelium. The exact origin of the yolk epithelium seems still to be in doubt. Some say it originates from the nuclei within the yolk, others from cells of the germ disc itself. The origin of the layer need not be of very special concern to us at this time, for the yolk epithelium, though it surrounds the yolk mass, does not become the endoderm.

While the yolk epithelium is forming and the edge of the germ disc is becoming thickened, the outer cells of the disc increase rapidly (fig. 44). This outer layer extends gradually over the whole egg (and thus CEPHALOPODS 121

covers the growing yolk epithelium) and forms the ectoderm. These two layers, the ectoderm and the yolk epithelium, are soon followed by a third or middle layer, which also covers the yolk. There are thus two definite regions in the egg at this time, the germ disc which forms the embryonic rudiment, and the yolk sac composed of three layers.

The function of the yolk epithelium is to form an envelope for the yolk and to make it available to the embryo. In later stages this envelope surrounds the yolk as in the earlier development. There gradually forms an outer yolk sac of part of the yolk not covered by the developing embryo, and an inner yolk sac of that part which is embraced by the embryo’s body; the latter remains always connected to the outer yolk sac, but the connection becomes restricted to a narrow duct. The external yolk sac evidently passes on its contents to the internal sac and then the nutritive material is conducted to the embryo from the inner yolk sac by aid of the yolk epithelium. This seems the most logical method of absorption, for there are no known vessels in the external sac.

The extension of the germ disc over the yolk varies greatly in different cephalopods. In Sepia the germ disc is very small and the yolk sac very large. In forms like Loligo and Octopus the external yolk sac is more reduced and the embryo contains the greater part of the yolk. Grenacher studied a form in which there was scarcely any external yolk sac and at an early stage the small yolk mass was enclosed by the embryonic rudiment.

We have seen how the yolk sac and germ disc are formed and how their outer layers become ectodermal. We have still to describe the method of formation of the endoderm. About the time when the first rudiments of organs appear externally in the embryo, there may be seen, next to the yolk, an epithelial plate of only a few cells. It is the first indication of the enteron. It soon increases in size and becomes sac like, finally separating from the yolk. The yolk epithelium, previously lacking at this point, now grows under the enteron. The origin of the endodermal plate thus described is probably from the thickened peripheral mass at the edge of the germ disc which evidently represents meso-endoderm. The whole process is thus to be regarded as a much modified invagination, and the edge of the germ disc is the blastopore filled by the large yolk plug, which also fills the whole enteric cavity.

BIBLIOGRAPHIC NOTE

Among the more important accounts of the subjects contained in this chapter are the following: Korschelt and Heider, Conklin, Selys-Longchamps, Patten, Claus, Lankester. These works are cited in full in the bibliography on page 406.

Chapter VIII Mesoderm Formation

Mesoderm is the layer between the outer epidermis and the midgut epithelium. It produces the muscles, coelome, and the structures belonging to the coelome, all the body and intestinal musculature, the gonads, the kidneys (except the Malpighian vessels) and the anlagen of connective tissue and blood vessels.

The concept mesoderm lacks a genetic unity throughout the animal kingdom and is really a collective name, since the mesoderm has a number of different origins within the same group. In spite of the lack of genetic unity of mesoderm, the anlagen of mesodermal structures have a common origin in single great groups of the rnetazoa. There is a definite homology in the mesoderm of all forms with a spiral type of cleavage, as turbellarians, nemertines, molluscs, annelids, and also the arthropods. The mesoderm of all these forms is endodermal, arising from the endoderm, and therefore the anlagen of the mesoderm bands are in genetic unity. It is also true that the ectomesoderm or mesoderm arising from the ectoderm of many forms is homologous. It is furthermore probable that the enterocoeles of echinoderms, Enteropneusta, and chordates are of common origin.

I. ECTOMESODERM

We will now consider the different kinds of mesoderm formation. Since the mesoderm is preceded by the ectoderm and endo(ler1n there are only these two possible origins for the third layer. We will consider first the eetomesoderm.

Ectomesoderm arises from the primary ectoderm and usually produces mesenchymatous muscle cells and connective tissue. This kind of mesoderm occurs in the flatworms, rotifers, nematodes, annelids, and molluses. Although the coelenterates are usually considered as two layered, there is often present a third layer, mesogloea, which, though not cellular, may be considered as eetomesodermal. In sponges, the dermal layer contains both ectoderm and mesoderm (using the term in a doubtful sense) and consists of (a) outer epithelium, (b) canal system except the flagellated chambers which are not included here, (c) connec— tive tissue, and (d) sex cells.

122 ECTOMESODERM 1 23

In coelenterates a distinction can hardly be made between ectoderm and mesoderm. Although hydroids have only two layers, still the interstitial cells which are at the bases of the epithelial cells and which later form the gonads may be considered as forerunners of the mesoderm.

In the Actinozoa, the distinction between ectoderm and endoderm is more sharply defined than in hydroids. In the Alcyonaria, there is often connective tissue with skeletal structure, and this layer is ectodermal. The ectoderm becomes many layered, and a jelly substance is secreted between the cells of the deeper layers which become separated from each other. Thus two layers are formed, an outer epithelium and an inner gelatinous layer which may be thought of as representing ectomesoderm.

In the ctenophores the mesoderm becomes more highly differentiated histologically. A definite mesodermal layer is here present and this layer is now known to be ectomesodermal in origin. Kowalevsky and Chun found that the mesoderm originates from ectoderm in the region of the gut. (See fig. 14B.) This is of particular interest because in forms with the spiral type of cleavage the larval mesoblast originates in relation to the blastomeres which produce the stomodacal invagination. In the polyclads, according to Surface, the ectomesoderm produces chiefly musculature of the pharynx.

Since the work on cell lineage, the development of annelids and molluscs is more definitely understoo(l, and we now know that the part of the mesoderm which is to become the mesenchyme of the trochophore arises from the ectoderm. In all forms with spiral type of cleavage, the first three quartettes form the ectoderm. Wilson has shown for polyelads that the mesoderm cells are formed by division of the cells of the second quartette, and that the third quartette probably also shares in the formation of mesoblast. The mesoderm formed in this way is the larval mesoblast, the adult mesoderm arising from cell 4d as in molluscs and annelids and therefore being endodermal in origin.

The relations in other flatworms, nernerteans and nematodes, is not clear. In rotifers the entire mesoderm appears to be larval mesoblast and some of this has been shown to be ectodermal. There are no mesoderm bands and the gonads come from primary endoderm and may represent the mesoderm bands of related forms.

In a number of the annelids the ectomesoderm arises definitely from three cells of the third quartette, 3a, 3c, 3d. The anlage is thus asymmetrical, being paired on the dorsal side, while on the ventral only the left forms it. In some molluscs the ectomesoderm arises exclusively from the third quartette. In Trochus (fig. 33, 34, Table p. 56) it arises from 3c and 3d from the dorsal cells of the quartette. In other forms the second 124 MESODERM FORMATION

quartette also contributes. Part of the body musculature of the annelids is also known to be of eetodermal origin. The presence of ectomesoderm in arthropods is not clearly shown.

Ectomesoderm produces connective tissue and larval musculature of the trochophore larva. For annelids and molluscs it seems to be a provisional tissue degenerating upon metamorphosis. It is doubtful whether the ectomesoderm produces excretory organs, but the kidneys of some molluscs are known to be of ectodermal origin.

We have seen that ectomesoderm occurs in many coelenterates and also in many groups which are near the trochophore type; these may be collectively called Prostomia. Endomesoderm appears to be lacking in the Molluscoidea. It seems striking that the entire group called Deuterostomia (composed of Enteropneusta, Echinodermata, and Chordata) shows scarcely any ectomesoderm. Thus we recognize two great stems of the animal kingdom, in so far as mesoderm formation is concerned.

II. ENDOMESODERM

We will now consider the formation of the endomesoderm, which includes all the mesodermal structures in the embryo that come from endoderm. Endomesoderm may arise as bands of cells, as hollow coelomic pouches or through the coming together of mesenchyme cells. We shall consider each of these cases separately under the following heads: (a) Teloblastic mesoderm band formation. In these cases paired mesoderm bands take their origin from two primitive mesoderm cells as in annelids and molluscs. (b) Secondary or derived mesoderm band formation. Those cases belong here in which paired mesoderm bands are laid down without primitive mesoderm cells. They are often modifications of the first type, since they occur among forms derived from annelids and molluscs. Examples are arthropods and cephalopods. (c) Enterocoele formation. The formation of coelomic sacs by outfolding from the primitive gut characterizes this type. (d) Coelome formation by solid ingrowth. Obviously this case is closely related to the foregoing type. (e) Mesenchymatous coelome formation. The coelome is formed through the coming together of mesenchyme cells.

It might seem natural to consider mesenchyme structures as different from mesoderm. Mesenchyme is, however, not a genetically uniform structure, but only a histological conception. It may arise by migration from various places of origin: (a) from the coelome walls, (b) from the primitive gut, (c) from the blastoderm of the coeloblastula, or (d) from the reduction of the mesoderm band, as in molluscs. Mesenchyme cells may come together and form a coelome as in the collar and body coelome TELOBLASTIC MESODERM BAND FORMATION 125

of some tornaria. The multiplicity of the origin of mesenchyme shows that there is no unity in the term.

1. Teloblastic Mesoderm Band Formation

In cases of teloblastic band formation, a pair of originally solid mesoderm bands is formed by the budding of two terminally lying primitive mesoderm cells. This type of mesoderm formation occurs in forms with the spiral type of cleavage.

The two primitive mesoderm cells arise always from the 4d and thus must be considered as primary endoderm, since the ectoderm is complete with the third quartette and whatever comes from blastomeres arising


fiG. 83. Mesoderm of the snail, Physa. (Redrawn from Korschelt and Heider, after Wierzejski.) The four larger cells M“, M", M“, and M“ and three pairs of micromeres m‘, m1, m3, give rise to the endomeeoderm.

later is to be regarded as endodermal. The two primitive mesodermal cells are more nearly like endoderm than ectoderm in appearance, size, and yolk content. This intimate relation of 4d to primary endoderm is shown by the fact that, besides the primitive mesoderm, 4d often produces other cells which contribute to the formation of the midgut.

In most forms the third quartette is given off dexiotropically and 4d by laeotropic division. The next division of cell 4d, now called M, is again dexiotropic or simply bilateral and the two daughter cells are symmetrical. Cell M, originally in the region of the endoderm plate, early sinks inside the remnant of the cleavage cavity and cells M1 and M 2 become symmetrically arranged. By these first divisions, small cells, enteroblasts which take part in midgut formation, are formed. An equal division of M1 and M 2 takes place and thus four large dorsal cells are 126 MESODERM FORMATION

formed, the two median ones of which, M 1’ and M?’-’, become the primitive cells of the mesoderm bands. The two other large cells in some forms (pulmonates) have been said to give rise to the primitive kidney of the trochophore, A series of divisions of primitive mesoderm cells now follows and two rows of small cells are formed. These become surrounded by the ectodermal products of the first quartettes.

In many yolk-poor eggs, as in oligochaetes, mesoderm bands are formed very early before the beginning of gastrulation, and lie in the blastocoele at the blastula stage. The mesoderm bands are at first dorsal and produce cells ventrally. With changes of body form they go through changes of position. The bands are given off horizontally and become lengthened parallel to the prototroch. (See p. 127.) Since the


fiG. 84. Embryo of Crepidula. at the time of the closure of the hlastopore and the formation of the stomodaeum. In addition mesodormal cells (In) and the gut cavity are to be seen. (After Conklin.)

middle of the embryo is taken up by the gut they must bend, so both become curved and form a right and a left curve lying in a horizontal plane. When later the blastopore closes and pushes ventrally, the bands shift and lengthen ventrally. The original large mesodermal cells soon divide into smaller ones.

In annelids, the mesoderm bands break up later into segments which hollow out and become coelomic sacs. From their walls develop the trunk and gut musculature, gonads, and nephridia. Ectodermal cells, however, often take part in the formation of the nephridia.

In molluscs, mesoderm bands do not elongate as in annelids. Early in development they are lost in the mesenchyme and, according to one author, produce only connective tissue and musculature while the anlagen of the definitive kidney, pericardium, and gonads are from the ectoderm. Subsequent authors indicate that, in some molluscs, kidney, SECONDARY OR DERIVED MESODERM BAND FORMATION 127

gonads, and pericardium come from the mesoderm, bringing the later development of mesoderm bands of molluscs more nearly in line with that of the annelids.

2. Secondary or Derived Mesoderm Band Formation

In the arthropods, as in the annelids, we find a pair of mesoderm bands. At first solid and sometimes single layered, these bands later

fiG 85 Diagrams of the development of Trochophorn showing the shift in position of the mesoderm bands (After Korsehelt and Heider)

g, gut, t , teloblast cells, t b , teloblastic mesoderm bands

become segmented and coelomic cavities develop in them. We cannot doubt the homology of the mesoderm bands of arthropods and annelids, but the method of formation of these bands is very different. In the few-celled embryo of the annelids, as we have seen, the combined anlage of the entomesoderm sinks into the cleavage cavity as two cells, the 128 MESODERM FORMATION

paired mesoderm cells, and from them mesodermal bands develop. These bands arise through teloblastic growth, by successive cell proliferation from the sides of the original mesoderm cells. In the arthropods, on the other hand, the anlage of the mesoderm bands is many layered from the beginning. From the moment that they may be recognized as separate cell groups no original mesodermal cells are observed and no teleblastic cells increase. Gastrulation in most of the arthropods is in the form of a many-celled solid ingrowth. The ingrowing cells form the primitive entoderm which spreads itself under the ectoderm as a so-called under layer since it pushes up to the opposite side of the central yolk mass. Now there is a division into an endodermal cell mass and into paired mesoderm bands. These latter spread out and divide into segmented sections.

In some few arthropods there has been observed a special place of ingrowth for the mesoderm. In the crustaceans, Astacus and Asellus, this special place is the region of the forward blastopore lip; in Peripatus, at the hinder blastopore region. Certain crustacea deviate from the general scheme given for mesoderm formation in the annelids, because their cleavage is more nearly total. In these forms (e.g., Branchipus) there are paired mesoderm cells or cells which because of their position and fate may be compared to paired mesoderm cells. They are similar to the annelid type.

A teloblastic method of mesoderm growth is found in the isopods. Here there is at the hinder end a cross row of eight teloblasts which through division.produce the mesoderm of the metanauplius germ band. There is here only a distant relation to the annelid type as the conditions are entirely different.

In the cephalopods there is no trace of the spiral type of cleavage and cleavage is typically discoidal. The growth at the edge of the germ disc leads to the formation of the endoderm. Later a cell ingrowth in the hinder part of the germ disc takes place and this produces mesoderm and gonad cells. Thus we see that the arthropods and cephalopods are sharply contrasted to the annelids, for in many arthropods and in the cephalopods the mesoderm originates from groups of cells rather than from a single mesodermal cell anlage.

A consideration of the mesoderm formation of the Enteropneusta will lead us naturally to the other chordates. The Enteropneusta form an ancestral group through which the echinoderms are brought into connection with the chordates. In this small group different types of coelome formation may be observed, the type of simple enterocoele formation and the type of coelome formation by the coming together of single SECONDARY OR DERIVED MESODERM BAND FORMATION 129

mesenchyme cells. Since all these types of mesoderm formation belong in such a small genetic group of animals, they evidently must belong together. Let us consider first the coelome of Balanoglossus. Here there are, corresponding to the three body regions, three coelomic cavities; the head, unpaired but showing by its two pores and incomplete mesentery a double nature, the collar, and the body coelornes. The latter coelome consists of paired spaces separated by a median mesentery. The head coelome is known to be formed by the cutting off of a vesicle at the forward end of the primitive gut, the end opposite the blastopore. The water vesicle of the tornaria larva is the anlage of the head coelome.

There are several descriptions of the method of formation of collar and body coelome. In those forms of Balanoglossus which have no tornaria, but develop directly, two pairs of gut diverticula become_ the collar and body coelomes. In another form these two pairs of sacs are cut off behind from the first-formed coelomic vesicle, the water vesicle. Here in a form without tornaria there is a similarity to the formation of the enterecoele in most echinoderms which also form an originally forward vesicle through the fusion of three pairs of coelomic sacs, the forward enterocoele, the hydrocoele, and the hinder enterocoele.

In the New England tornaria the collar coelome is formed by paired cell proliferations at the side of the stomach, the trunk F“, 86. Diagram of the coelome coelome by solid evaginations of the intes- forrxxzmtion of Balanoalossus Kowalevtine. In the tornaria from the Bahamas, §aft'e‘;':n§°’s°h°lt and on the other hand, these coelomic spaces are formed at a considerable distance from the gut by aggregations of single mesenchyme cells. In one form they arise from the wall of the acorn coelome.

There are thus, in this one group of Enteropneusta, three types of coelome formation: (a) through diverticula of the gut, (b) through cell proliferation, (c) through aggregations of mesenchyme cells.

The second type is easily derived from the first, as solid cell proliferation is one step beyond a diverticulum. The third type differs, but may be considered to fall into line if we think of the cells of a solid proliferation as having lost their connection and become scattered mesenchyme

cells. 130 MESODERM FORMATION

3. Enterocoele Formation

In the eehinoderms and also in amphioxus the coelome is formed by outpocketings from the alimentary canal, that is, by the formation of

  • an enterocoele. We must first consider the

inesoderm formation of echinodeiins.

In eehinoderms, niesoderm formation is in general like that of Enteropneusta, by an evagination of the ceeloinic sac fiom the primitive gut. At the same time iiiesenchyine cells migrate into the blastocoele. Mesonchyme formation may begin very early, even before the beginning of gastrulation, or may not begin until later. Following this process there occurs in echiiioids and in Comatula, at the place which will become the top of the

Fm 87 Diagram of the me_ primitive gut, a cell migration into the gelati lgiimg forniation Km Cgnlnatulad nous blastocoele. By the time gastrulation is ra n rom orse e 1; an - Hefdenvvufter Scehger ) completed, cell migration from the top of the

gut has already been going on for some time. There are two types of coelome formation in the echinodeims. Com atula is an example of one type. In this form the hydiocoele develops


"1


0 at

V e h CT2 mg 0 C2 3. mg i A B C fiG 88 Metamorphosis of the coelome sacs in the eehinoids (A, B. redrawn from Korschelt and Heider after Theel, C, redrawn from Korsehelt and I-Ieider after Bury)

a, anus, C1, left anterior enterocoele, 02, left posterior enterocoele, en, right anterior enterocoele, crz, right posterior enterocoele, h, left hydrocoele anlage, 1. intestine, mg, stomach, in, ectodermal mouth invagmatien, oe, oesophagus.


as an outgrowth of the forward part of the gut and the enterocoele as

outgrowths from the posterior part of the gut. The hydrocoele is the anlage of the ambulacral system. COELOME FORMATION BY SOLID INGROWTH 131

The other type of coelome formation in the echinoderms is illustrated by the echinoids. In these forms coelomic spaces arise from the division of an unpaired coelomic pouch given off at the top of the primitive gut. This vesicle soon divides into right and left halves, each of which divides again producing anterior and posterior right and left enterocoeles. The anlage of the hydroeoele or ambulacral system develops from the left forward enterocoele sac.

In chaetognaths and the brachiopods also we find enterocoele formation. Amphioxus must also be considered since its mesoderm is formed as an enterocoele, paired diverticula originating on the dorsal side of the embryo and later surrounding the gut. Hatschek thought that there were primitive mesoderm cells in amphioxus, and such cells are figured in many text-books, but they do not exist. The enterocoelous diverticula of the alimentary canal occur shortly after gastrulation when the embryo is lengthening. The notochord forms on the dorsal side of the alimentary canal by folding and is cut off lengthwise. At the sides of the notochord are the two Fm. 89. Cross section of an grooves at the anterior end of which paired inS:‘0‘:l“:)i;‘cff evagmations occur. These evaginations are tion with the enterou. (Rethe anlagen of the segments and increase in “"d number as new ones are formed behind.

They become completely separated from the gut and form paired coelomic sacs which are the primitive segments of the embryo.


4. Coelome Formation by Solid Ingrowth

In many cases the coelomic sacs are formed by solid outgrowth from the gut. As already mentioned, the collar and body cavities of the New England tornaria originate by outgrowths from the gut. There are similar cases among the eehinoderms, for in Ophiothrix fragz'l2's the two coelome anlagen have at first no lumen, and also among the brachiopods a similar condition prevails. In the tunicates likewise mesoderm originates as a solid outgrowth from the primitive gut.

The mesoderm formation of vertebrates may also be considered to belong to this type. In the embryo of Triton there is at each side of the notochord a small region of the gut from which coelomic sacs take their origin. These sacs appear as two many-layered cell masses which push in at the sides between the ectoderm and the entoderm. A split occurs in each mass and thus is begun the separation between the outer somatic 132 MESODERM FORMATION

and inner splanchnic layers of the mesodermal sacs. The vertebrates do not show the division of the mesodcrm into primitive segments from the first, as does amphioxus, but the segmentation appears later in the form of ring-shaped invaginations. Under the dorsal lip of the blastepore the invagination is deep and elsewhere it is hollow. The mesodcrm formed near the dorsal lip is called the gastral mesodcrm, and the mesoderm formed all around the blastopore itself is called the peristemial mesodcrm.


fiG. 90. Gastrula of Rana fusca. (Redrawn from Ziegler, after Schwink.) ch, chorda anluge; ec, ectederm; en, endoderm. n1, mesodcrm, g, gastral cavity.

In the frog there is a trace of the outpoeketing of the endodcrm to form the mesoderm sacs, for a groove occurs on each side of the notochord so that the notochord endedcrm is separated from the lateral endoderm.

In selachians mesodcrm formation occurs around the entire disc edge. At the anterior region and on the forward parts of the lateral edges the mesodcrm un(ler the blastocoele becomes split and later the blood islands form here. In the more posterior region of the embryo the mesodcrm is formed by ingrowth of cells from mesodcrm forming grooves of the endoderm. One of these grooves is adjacent to the notechordal region and the other is peripheral. From these grooves groups of cells grow into the peripheral blastocoele. THEORIES OF THE ORIGIN OF THE COELOME 133

5. Mesenchymatous Coelome Formation

The origin of coelomic sacs by combination of originally free or independent cells seems to occur. It has already been stated that Morgan found this method of mesoderm formation to occur in the tornaria from the Bahamas.

In general the mesoderm formation of Phoromls-, one of the Molluseoidea, is from scattered mesenehyme. Phoronis has an invaginate gastrula. At this stage single endodermal cells migrate into the blastoeoele and become mesenehyme. This migration appears to be especially great in the region of the edge of the blastopore. The mesenchyme cells which are at first scattered in the blastecoele early show an inclination to lie on the inner surface of the ectoderm, and later on the gut endoderm. Thus are formed the somatopleure and the splanchnopleure.

It is doubtful whether or not such a method of mesoderm formation is

fiG. 91. Oblique section through gas prhnltiva We "light infer that Such trula of Phm-om's sahatieri. (Redrawn from

is the case since Morgan’s tornaria Iforst-halt and H_eidor. after Selys-Lomzfrom the Bahamas shows this kind cmnms) Sh°w‘(';§es_;'_"°s°n°hyme cells of mesoderm formation and other

Enteropneusta do not. It may be, however, that a secondary change

has occurred in the matter of mesoderm formation.

III. THEORIES OF THE ORIGIN OF THE COELOME

A discussion of the origin of the mesoderm involves also a consideration of the origin of the coelome. We might define the coelome as a body cavity lined by peritoneum from which arise the gonads. The tissue of the coelome, as of all other mesoderm, must necessarily arise from the ectodcrm or endoderm. We have already discussed the double origin of the mesoderm, but have not yet considered the origin of the coelomic cavity itself.

The theories of the origin of the coelome are of course hypothetical. There are three main theories, the enteroeoele theory, the gonoeoele theory, and the nephrocoele theory. The enteroeoele theory was first suggested by Leuekart in 1848 in one of his first papers on the coelenterates. According to this theory, the coelome of higher forms is represented by the radial canals and gastric pouches of medusae. The gastric cavity of coelenterates thus corresponds to both the gastric cavity and coelome of worms and higher forms. This original idea was suggested 134 MESODERM FORMATION

long before Kowalevsky and Metchnikofi found that the coelome of forms such as Sagitta, brachiopods, echinoderms, and amphioxus really develops from gut pouches. The enterocoele or gut-po11ch theory was taken up with enthusiasm by many, including Balfour and Lang. Lang developed the theory, illustrating it by Gunda. He regarded the metamerism of higher animals as resulting from the separation of paired gastric pouches. Each diverticulum of the gut had perhaps originally the task of producing genital products as well as the excretory function. As the diverticula separated from the gut, new structures must be formed to bear the functions of gonoducts or nephridia. Since the ancestry of the vertebrates is so problematical, this theory as applied to them must be largely conjectural. Lang finally gave up this theory for another.

This theory may be true as applied to the entcrocoelous or vertebrate series of animals, but is evidently not true in the old sense as applied to the teloblastic series of animals where the coelome is derived from a pair of pole cells.

Hatschek is responsible for the gonocoele theory of coelome formation, suggesting it in 1876. According to this theory, the pole cells of the teleblasts are primordial germ cells, and the germ band, in which the coelome develops, is homologous to a gonad. Lang and others took 11p this theory and assumed that the original ancestral type has essentially the same morphology as a rotifer or flatworm. They suggested that the original gonad cavity was still connected to the outside by the gonoduct. Along with the extensions of the gonad cavity, a corresponding reduction in the parenchyma took place and the walls of the gonad became partly sterile, muscles developing in them. It is thus clear why the gonoduct does not connect directly with the gonad, for since the walls of the gonad are partly sterile, the eggs or sperm fall into the coelome and are taken up by the gonoducts. This theory explains also the reduction of the spaces in the flat worm occupied by the circulatory fluid. These spaces are entirely outside the body cavity and from them are formed the blood vessels. In some annelids there is a sinus-like blood system in at least part of the body and this is regarded by Lang as a primitive condition.

The nephrocoele theory is due chiefly to Ziegler, who regards the coelome as primarily and originally an organ of excretion. This organ consisted of a vesicle, the nephrocoele, and its duct. By its expansion a modification of the coelome is produced.

These three views are not as sharply distinguished from each other as might perhaps seem, since cases may be cited in which the coelome functions in such a manner as to suggest all of them. THEORIES OF THE ORIGIN OF THE COELOME . 135

BIBLIOGRAPHIC Non:

Among the more important accounts of the subjects contained in this chapter are the following: Korschclt and Heider. See also note at end of Chapter VII, and Hatschek, Wicrzejski. Buteson. These works are cited in full in the bibliography on page 406. 136

Phylum

Porifera.

Coelenterata.

Ctenophora Platyhelminthes

Annelida.

Molluscoidea.

TYPES OF INVERTEBRATE LARVAE

Larger Group

Hydrozoa.

Scyphozoa

Actinozoa

Turbellaria Polyclads Trematodes

Cestodes

Nemertinea.

Chaetopoda. Gephyrea Phoronidn

Polyzoa.

Brachiopoda

Larva

AMPHIBLASTULA (Pseudogastrula)

Parenchymula. Actinula. PLANULA

SCYPHISTOMA (Hydratuba) Scyphula Ephyra Strobila.

Arachnactes

Zoanthella _ _ _ . _ I . _ . _ Zoanthins. Cydippid larvae

MI’JrLLEn’s Larva Sporocyst, Miricidium, Redia, Cercaria. Cysticercus PILIDIUM Larva of Desor Tnocnopuonn Mitraria Trochophore

Actinotrocha. Cyphonautes (Closely related to trocho phore) (Related to trochophore)

TYPES OF INVERTEBRATE LARVAE

Type Genus

Sycandra raphnnus

Leucosolenia vari abilis Clathrina blancu Tubularia Most Hydrozon Many Actinozon Aurelia

Actinia urticinia In family Cere:Lnthidue

Zoanthidac Order Cydippidae

Planocera

Cerebratulus Lineus

Phascolosoma. Sipunculus Phoronis Mcmbranopnra

Terebratulina TYPES OF INVERTEBRATE LARVAE 137



Phylum R Larger Group Larva Type Genus

'l‘ro<:l1clmintl1e.s Rotifora (Supposed to be per sistent trochophore,

but early develop ment is not in ac cord with this view) Cllrzetognzltlla (Fairly direct) Sagitta AI'f_‘1I‘()])0dd. Crustncea NAUPLIUS A few schizopods

A few decapods

Metanauplius, Protozoaea, Zoaea, Calyptopsis, Copepodid, Metazoaea, Mysis, Phyllosoma, Mega— lops, Cypris

Erichthoidina Erichthus (Pseud0- Stomotopod zoaea) Alima Insecta Larva, pupa, caterpillar (eruoiform) Campodeiform Mollusca Gastropoda Ctenophore stage Patella TROCHOPHORE Drcissensia. Lamellibranchia VELIGER Unio, Dreissensia Glochidium Echinodermata Asteroidea BIPINNARIA Asterias Ophiuroidea Ophiopluteus Ophiothrix Echinoidea. Echino- Pluteus Echinus pluteus Holothuroidea Auricularia Synapta ' Crinoidea Pentacrinoid Antedon I’rotochordata Enteropneusta Tornaria Balanoglossus Tunicata. Tadpole oozoid Cyathozoid Ascidiozooid Salpa. Trochozooid

Phorozooid

Chapter IX Types of Invertebrate Larvae

The development of the eggs of the many invertebrate animals shows an amazing diversity in the methods by which the adult is reached after the period of germ-layer formation has been passed through. In some groups most complicated life histories involving adaptations to environments that are totally different from that in which the cleaving egg found itself are present, while in other groups development is simple and direct. Of these many types of invertebrate larvae it is possible to describe only a few in this chapter. No attempt is made here to describe the cases of direct development as they occ11r in the various phyla, but it is desired to explain how certain important invertebrate larval types undergo their metamorphoses and reach the adult condition. In the table showing the occurrence of the Various types of invertebrate larvae these forms which are selected for description are indicated by small capitals, while the others mentioned are of less general

significance and are for reference.

I. THE PORIFERA The Amphiblastula

The free—swimming larva which occurs in all families of the Porifera is known as an amphiblastula. Its development has been investigated in a number of forms, among the best known of which is Sycandra raphanus (see fig. 64) studied by Schultze in 1875. Other important studies are the series of papers of Maas on various sponges, and the studies of Minehin on Leucosolenia.

The eggs are fertilized in the supporting jelly of the sponge wall, a position which they occupy when ripe and where the early stages of development are passed. (In Cliona, the boring sponge, the early stages of development take place externally.) In a cavity near a flagellated chamber which has a definite cellular lining the cleavage stages are undergone, forming an embryo of characteristic appearance known as an amphiblastula. At length the embryo emerges into the flagellated chamber and thence passes to the outside to become free swimming. After twenty—four to forty-eight hours of swimming about, it gradually finds lodgment and attachment to a substratum, a process which is

138 THE AMPHIBLASTULA 139 spoken of as fixation, and which involves a complete and quite sudden metamorphosis. In different genera of sponges the events do not all take place in exactly the same order nor do the larvae reach the same degree of advancement at the time of emergence or of fixation. The essential principles of development are probably not dissimilar, however.

The free-swimming larva is at first an ovoid blastula in which there are cells of two obviously different sorts. The large anterior portion of the embryo is composed of flagellated cells and the posterior portion of larger, non-flagellated, granular cells. Originally open at both ends, the blastula soon grows so that the pointed end is closed and rounded out and the cells become columnar in form and flagellated. The opening at the other end is surrounded by the granular cells which upon its closure take the form of a flat layer, some of whose cells proliferate and presently push into the cavity. It is supposed that the flattening is due to pressure against the unyielding Inass of spicules, while the columnar cells produce a swelling into the space of the flagellated chamber adjacent. This is the condition in which the embryos are extruded to form free-swimming larvae.

In Leucosolenia, Minchin has described the columnar cells each as differentiated into two regions, a refractile portion at the internal end and a sharply marked-off granular part at the outer end‘. In living embryos the two.portions fiG 92‘ Amphiblasmln of are so distinct as to give superficially the Sycandra. (After Schultze.) appearance of an inner layer of refractile cells covered by an outer granular layer of cells; they are, however, merely parts of the same layer. Between the columnar and the posterior granular cells of this form is a zone of intermediate cells which are flagellated and entirely granular. The flagellated cells are much more numerous but much smaller than the granular cells. As development proceeds, the number of granular cells increases at the expense of the flagellated ones.

The larvae of Leucosolenia are transparent so that a mass of yellowishbrown pigment at the center may be easily seen. This is shown by sections to have the form of a tube open in front and behind, enclosing a lens-like body of gelatinous character which fills the central, blasteaoelic space. The central cells are so arranged that Minchin regarded this structure as a premature, light-perceiving organ of larval significance only. i

The free-swimming stage of the amphiblastulae is not of long duration. 140 TYPES OF INVERTEBRATE LARVAE

They remain at the surface for perhaps a day, then sink to the bottom and after another twelve hours of swimming there they are ready for fixation. fixation takes place at the anterior pole, the granular cells growing about and enclosing the flagellated cells in the process of metamorphosis. This process involves in some genera also the active invagination of the flagellated cells. At this stage only the two kinds of cells may be distinguished, the central cells appearing to be thrown out with the pigment in metamorphosis (Minchin). The outer cells become the dermal or covering layer, the inner the gastral tissues.

Postlarval changes in both layers now set in by which the adult condition is reached. The dermal layer differentiates and two kinds of cells result, one superficial, the other migrating beneath the former. They differ also in the type of spicules which they are to secrete, the superficial producing the monaxones and the other the triradiate spicules. The gastral cells take on a radial ar~ rangement, a cavity appears in the center of the organism which



F10. 93.

fixation of the larx a of Sycandra

Iaphanus. (After Sehultze)

A, flagellated cells retreating into the interior; B, cup—shaped larva attached by amocboid processes of the outer granular layer, f.c., flagellated cells; g.c., granular cells.

presently (in five or six days) dcvelops an opening to the outside, the osculum, and becomes more complicated. The cells themselves elongate and assume the typical

collared appearance of choanocytes. The development of the pores and canals is a matter of slow growth, involving the formation of pouches and the rearrangement of cells, the secretion of spicules and gelatinous intercellular substance. Other types of larvae have been described for sponges but they may all be regarded as modifications of the amphiblastula type just described, as was shown by Maas (1898). Some sponges also reproduce by formation of gemmules, but this is a process of budding and no free-swimming larvae are developed. THE PLAN ULA 141

II. THE COELENTERATA

The larvae of the coelenterates exhibit a considerable variation in appearance in conformity to the wide range of adult conditions to be met with in the phylum. Like the adults, the embryos have, in spite of dissimilarities of form, a fundamentally common type of structure. Numerous experiments into developmental possibilities seem to have been tried out by the coelenterates with many diverse results, considering the paucity of material and restricted structural limitations. The structural simplicity is visible throughout the general similarities that may be discovered in the different kinds of embryos.

1. The Planula

The typical eoelenterate swimming larva is a planula. It occurs in nearly all_Hydroz0a (Tubularia is an exception) and in very many


and the character of the ciliated planula. (After Metschnikofi.)

Actinozoa and Seyphozoa. Because of its simple character and its widespread occurrence, an evolutionary significance as the ancestral coelenterate is suggested. It is the most important larval stage of this phylum.

The term planula was formerly applied to a blastula stage, but the usage is now obsolete. The blastula develops by the migration of cells inward, and by cell division into a two—layered, ciliated, swimming larva. The outer layer is in the form of a ciliated, columnar ectoderm; the inner is usually, in the Hydrozoa, a solid endoderm mass formed by many-celled, unipolar ingressions. There are numerous cases in both Actinozoa and Scyphozoa in which the endoderm is hollow. The gastral cavity does not appear in the hydroids until about the time of attachment of the swimming larvae. In Pennaria the hydranths are not covered by a hydrotheea; each has two circles of tentacles, one about the 142 TYPES OF INVERTEBRATE LARVAE

oral end and another at the aboral end. At the time of maturity a row of medusa buds appears around the middle of each zooid which gradually enlarges and differentiates into the somewhat reduced medusae characteristic of the genus. These p1'0duce the germ cells and do not become free until the sex products are shed. Sexes are separate. After fertilization inside the bell of the medusa, the eggs are immediately shed. The medusae are then free, and after a few hours of feeble swimming, they die. In this genus the Inedusa is the less important of the two generations. The fertilized egg as described by Hargitt goes through a very irregular cleavage, forming an irregular cell mass which differentiates into a solid planula of two layers, the outer ciliate(l. After perhaps twelve hours of swimming about, the planula begins to settle down and at length attaches to grow into a new hydroid colony.

2. The Actinula

In some forms, notably Tubularia, an intermediate larval form, the aetinula, intervenes between the planula and the attached stage. It is neither fixed nor swimming, but creeping, and is formed by the appearance upon the planula of blunt protuberances, the

Fm 95_ Enema, features of tentacle buds, which gradually grow longer. the various stages of develop- first appear the rudiments of the aboral

ment of the embryo of Tubularm _ - , mdmm (Rcdmwn fmmmlmen ) tentacles dnected toward the future aboral

A, plnnnln beginning to bud on end. The gastral cavity now is evident with ‘*b°ml t°"“1°1°5-B-CvA°“““l‘*e- thinned walls at one point where the mouth ab.t., aboral tentacles; o.t., oral . . n,nn,n1es_ opening Wlll presently break through about

the time when the buds of the oral tentacles appear. The aetinula now escapes and creeps about on the bottom, oral end downwards. It later tips over, attaches by the aboral end, elongates rapidly and gives rise to the buds which are to form the different zooids of the colony. Thus the aetinula larva is important as the ancestor hypothecated by Brooks for the origin of the diverse kinds of coelen terates.


3. Origin of Coelenterate Larvae

The grouping of the various members of this phylum depends upon the presence and degree of development of two primary structural forms, the polyp and the medusa. In the Hydrozoa both are present; in the Actinozoa the polyp form is especially developed, and in the Scyphozoa ORIGIN OF COELENTERATE LARVAE 143

the medusa. is the structural type. Within the Hydrozoa it is possible, as is commonly done, to form a series with Cumna and Lmope at one end,

fiG 96 A, gonophores of Tubularuz mdwzsa containing embryos B, creeping Actinula larvae, C, attached form of Tubularza, mdwzsa (Redmwn from Allman )

in which the hydranth generation is quite lacking, and Hydra at the other end, in which there is no medusa. These forms are as follows:

Cumna, Lmope (meduszi only) Gommwmus (very rndnnentary hydmnth ulternatmg with medusa generation) ‘ 144 TYPES OF INVERTEBRATE LARVAE

Obelia, Bougainvillea (medusa and hydranth alternating and of equal importance) Pennaria (medusa fixed during sex cell stage, and of reduced importance) Gonothryca

Tubularia (In these four cases the fixed medusa undergoes more and Claw, Hydfactinia more reduction in structure and importance.) Campanularia, female

Judendrium, Oampanularia, male (remnant of mcdusa bud) Hydra (no medusa, hydranth only)

It is evident for reasons that need not be gone into here that the evolution of this series cannot have been gone through from Hydra toward Cunina. On the other hand to assume the medusa. to be the more primitive form of the two types is hardly in keeping with obvious structural features, and for this reason it is not possible to regard this series as having begun with a form similar to Cunina and to have been evolved in the reverse order. Rather some such suggestion as that made long ago by Brooks (1885) seems better adapted to the facts. According to this suggestion the most primitive type is neither a medusa nor a hydranth, but some small generalized form like the actinula. From this it may be supposed that four, perhaps five, series of forms have been derived. first there is the hydroid colony like Obelia in which both medusae and hydranths are present in alternating fashion. The remainder of the series from Obelia through Pennaria to Eudendrium and possibly to Hydra may be derived from this hydroid by the gradual degeneration of the medusa. A second series radiating from the actinula-like ancestor produced Cunina and Aeginopsis in which no hydranth is present. Perhaps a third produced hydra-like forms at the other end with no medusae. The Scyphozoa and the Actinozoa are the fourth and fifth series respectively which owe their origin to this primitive form of coelenterate, the actinula—like form.

Of this form the planula is the larval type (fig. 94). It is the freeswimming larva common to all coelenterate groups. In some, the Hydrozoa and many Aetinozoa, it is a solid mass of endoderm with an ectodermal covering. In others, the Scyphozoa and some Actinozoa, the endoderm is a definite layer with a gastral cavity. The latter is held by some workers to be the more primitive of the two, for it is argued that as the organisms were evolved an animal with a solid internal mass of cells would be quite unable to support itself. An embryonic type developing from stored yolk material would find no such difliculty, and so the solid form of the planula was thought to be secondary.

The general plan of coelenterate embryology is now clear. The fertilized egg develops gradually into a planula which swims about for a time and, it may be after intervening larval stages have been passed SCYPHOZOAN LARVAE ' 145

through, settles down, attaches, and elongates into a hydra-like form representing the hydranth generation. This may grow into a hydroid colony or into the coral polyp or actinian, or go through further development processes to produce asexually a. rnedusa which in turn produces new germ cells.

4. Actinozoan Development

In the Aetinozoa the development of the sea anemones is very similar to that of the Seyphozoa up to a certain point. The planula is reached in the usual manner. The early stages of their development may be undergone in the gastral cavity of the mother in some cases, shedding of the embryos in the gastrula stage or thereabouts occurring through the mouth, or the eggs may be discharged from the mouth and fertilized among the tentacles or free in the sea water. After the free-swimming period the attachment at the broader end takes place. At the other end a narrow pit forms asthe beginning of thestomodaeum ; it deepens and its lower end breaks through, connecting the gastral cavity with the outside. The subsequent history is largely one of differentiation especially of the mesenteries. Some special forms of larvae occur in various subdivisions of this group but the general features are similar.

5. Scyphozoan Larvae

In the Scyphozoa the development of Aurelia may serve as a convenient type. F1 G. 97.

_ _ . A, free-swimming plaThe eggs are shed 1nto the digestive nula of Aurclia aurita; B. section

through s(-yplustoma having four

cavity’ pass out through the mouth after tentacles. (Redmwn from Hein.)

fertilization to pockets on the inside of

the oral arms where they undergo those processes which lead to the planula stages. Then they emerge and swim about freely. Histological differentiation continues, and the larvae are ready for attachment in four or five days. After attachment the larva elongates and broadens out, the mouth opening becomes widened and four tentacle buds appear between which the taenolae, endodermal ridges projecting into the gastral 146 TYPES OF INVERTEBRATE LARVAE

cavity, develop. This larva with its flattened, broadly open, oral disc is spoken of variously as a scyphistoma, scyphula, or hydra-tuba. Secondary tentacles develop between the original four and then continue to form until the appropriate number is reached. After further differentiation, the process sets in which distinguishes scyphozoan development from other types. It is the cutting off of its oral disc by means of a constriction around the scyphistonia to form an ephyra larva. This process is known as strobilization and iii a well—fed scyphistoma may take place repeatedly until a dozen or fifteen cphyrae are formed from the one larva.


1‘i(. ‘)5 iSti‘obiliz.it1on of Auiclia amila (Rednivm from Claus) t, tentacles of strobila t..ie taeniolac, g fiist tiiuisx crsc giome, I, lobes of cphvi 1

The more usual condition is for each scyphistoma to produce two 01 three ephyrae. The constrictions appear piogressively later as they pass down the lawn, and in the well—fed individuals the appearance of a pile of saucers is ieadily suggested

The ephyra now continues rapidly its development and differentiation leading to the form of the adult jellyfish. The scyphistoma tentacles aie resorbed and in their place the characteristic lobes of the ephyra appear. The oral cone lengthens into the manubrium and other changes occur which result in the metamorphosis of the ephyra into the jellyfish.

III. THE PLATYHELMINTHES

Development in the flatworms presents many diverse aspects. Some eggs undergo no metamorphosis but pass directly into the adult condiMULLER’S LARVA 147

tion. Others reach their final development only after passing through

‘the most complicated life histories, involving (lifferent hosts, totally

different environmental conditions, and totally different types of organization. Since it is not the purpose of this chapter to follow through life histories, but merely to show the relations of types of larvae to embryos and adults to which they are related, only meager reference can be made to the group as a whole. One well-known form is Mul1er’s larva, the

S J ’ mo. 1 . p’ . (ix

‘ W ‘ M

s. ., _,4 . _,, < A r- *7 _ Irv-W ‘_ gr. , { * ' 1,1’; ~ ,. r.l. Q.” T‘. ls;-,’..\ (‘if :r Jicm « V’ 5, t'::7'\$\.«" ,‘ K3,,’ -* z ) ;,_ ‘ R» an, I ‘w 4 (' V 5.0. A B

ll(. ‘)0 \ smobilmd sn phisloxn L of Auului tlunla H uphv. 1 lll\ I. of Aurclirz mmta tftu lll)(‘I‘Iil()n (l{e(lrmn from ( lms)

gf Lttslrlt hl um ms mu nmnth rl, \ uious ruli ll lobes of H1111-lll\(‘ an! ‘I n m 11gm ll sense org ins

free-swimming larva of the polyelad Tuibellaiia named after its discoverer, Johannes Muller.

1. Mii1ler’s Larva

The development of the polyclads is known chiefly from an older study by Lang or Yungza and a later and more detailed investigation by Surface on the embryology of Planocera mquzlma. The cleavage is of the spiral type as found in such groups as gastropods and annelids‘. The cell lineage is similar in the early stages and the localization of formative substances surprisingly like that in the higher forms; the similarity is especially surprising when it is remembered that the Turbellaria agree closely with the etenophores in many points of structure Gastrulation is by the method characteristic of eggs with spiral 148 TYPES OF INVERTEBRATE LARVAE

cleavage, namely epiboly. An oval embryo with ciliated ectoderm and endoderm results. The stomodaeum opens into a rather broad gastral sac, in the wall of which are only small endoderm cells in place of the large endomeres of an earlier stage. Mcsodcrm, ectomesoderm, and ganglion cells are also present in the embryo of Planocera when it is ready for escape from the capsule. Eight ciliated lobes appear at this time just below the equator; these are the characteristic features of Mi'1ller’s larva.

Lang followed through the metamorphosis of Yungza in detail. The position of the mouth shifts from the pole to the ventral side of the


Fro 100 A, B, C, dorsal, ventral, and lateral view; of free-swimming larva of Yunma. (After Lang)

elongating larva. Symmetry is lost because of the inequality in the rate of growth of the two sides of the larva. Of the eight lobes one is dorsal, one ventral, and the others make up three pairs laterally placed, and all are connected by a continuous ciliated band. Growth in length with the gradual reduction of the lobes until the usual form of a flatworm is reached brings about the external changes. Among the internal changes involved are the development of eye-spots, the development of the parenchyma (which fills in the interior of the adult, and of which some cells differentiate into muscle cells), and the differentiation of the brain and genital organs. The most marked changes, however, are those MU LLER’ S LARVA 149

concerned with the development of the protusiblc pharynx. There is an invagination of the larval stomorlaeum, H] which the pharynx arises as a ridge-like thickening. The pharynx itself grows in length and the stomodaeum becomes everted to form the sheath of the pharynx. Surface records that the early cleavages as well as the maturation divisions require about one hour each. By forty—eight hours small ectodermal cells cover the entire embryo, which become ciliated, and during the third day rotation is set up in the capsule. Eye-spots appear about the fourth day. By the end of the fifth day the ciliated lobes appear, and


Tm 101 A, B, dorsal and xentrnl news of l‘lI‘\ are of Yungm aurrmtzaca. in process of metamorphosis (After Lang )

on the sixth the larva breaks from the egg membranes to become freeswimming. It swims for some time, eventually settling to the bottom and assuming the shape and habits of a typical polyclad.

Some of the turbellarian larvae, owing to disproportional development of some lobes, resemble fairly closely the pilidia of the nemerteans. There is resemblance between this larva in turn and the trochophore which Balfour thought was derived from it. Obviously, therefore, larval forms of this group are of importance in working out the ancestral history of invertebrate types, and by some the history is thought to run from the etenophores through the turbellarian forms to the pilidium and trochophore. 150 TYPES OF INVERTEBRATE LARVAE

2. Trematode Larvae

Trematodes are commonly divided into Monogenea and Digenea, depending upon whether one or more than one host is necessary for their development. Since only one host is necessary in the Monogenea, development is direct or nearly so, whereas in the Digenea there are often several intervening stages. In the sheep liver—fluke, which may be chosen as an example, the egg undergoes the early part of its development in a chitinous shell while it is passing through the alimentary canal of the


flo 102 A B, same as above but older

sheep. After it has been passed from the body of the host it at length escapes from the shell as a ciliated larva, the miracidium. This larva swims about in water or moves over damp vegetation until it comes in contact with a pond snail or perishes. It is said to be sensitive to the presence of the snails and to move toward them actively. At this time the larva is in many respects similar to a rhabdocoele turbellarian without gonads. It has nearly the shape of a slender cone with two eye-spots near the head end (the broader end). There is a brain, a pair of flame cells representing the excretory system, and an imperfect intestine. The rest of the body is filled with germ cells. After the miracidium has penetrated the body of the snail it loses its ciliated ectoderm, the enteron degenerates, and it elongates into a sporocyst, which is thus CESTODE LARVAE 151

merely a transformed miracidium.Within the sporocyst, germ balls* are budded ofl" and each begins a development similar to total cleavage to form a blastosphere which in its turn is converted into a gastrula. This passes then into the larval type known as the redia. The redia is usually looked upon as parthenogcnetically produced, and the alternation of generations thus involved differs from that seen in eoelenterates in that here a sexually developed sporocyst gives rise parthenogenetically to the redia. In the winter the rediae produce other rediae in a similar manner, but in summer they develop into another type of larvae, the cercaria. The rediae differ externally from miracidia in the absence of cilia, of eye-spots, and in the presence of a pharynx and a simple sac-like intestine, and their general shape is more cylindrical with a collar or circular ridge near the anterior end and short locomotor processes near the posterior. The cercariae have in an undeveloped condition all the organs which are found in the fluke and some other structures including a tail which are of brief duration and last only during larval life. The cercaria leaves the snail, encysts upon a blade of grass, and must be eaten by a sheep to continue its development. Its final metamorphosis consists in the loss of its tall, the rapid growth of the organs already present, and the development of its reproductive organs.

Variations from this case occur; in some forms stages are omitted and the cerearia may develop without a tail. The complication of two or more hosts and an intermediate larva which reproduces paedogenetically recalls the cases of polyembryony recorded in numbers of groups throughout the animal kingdom.

3. Cestode Larvae

Cestode larvae and life histories are only a little less complicated and involved than are those of the trematodes. The eggs of cestodes, like those of the trematodes, are surrounded in the uterus by a thin eggshell. In some forms there are also included “yolk cells” which contribute food to the developing embryo. Cleavage is irregular in type, although characteristic features are to be recognized. An outer layer of cells is formed from micromeres which separate from the larger cells early in cleavage. In most cases this layer of superficial cells gives rise to a chitinous coat which is thrown off ultimately. Only the central mass of cells which is enclosed by the superficial layer takes part in the formation of the embryo. This mass of cells develops a series of six hooks and becomes the hexacanth embryo. The development of the hexacanth

  • There is reason to doubt whether these germ balls are true germ cells involving

a reduction of chromosomes in their development. If these are not germ cells then the rediae are asexually produced and a true alternation of generations exists. 152 TYPES OF INVERTEBRATE LARVAE

embryo (onchosphere or proscolex) and the formation of the chitinoid coat with its inclusions of yolk material take place within the uterus of the posterior proglottids, and in this condition the embryo is passed to the outside; it must await its appropriate intermediate host for further development. .

If it is ingested by the proper animal (often along with the entire proglottid in which it was produced) the digestive juices soften the coat of the embryo, which is set free and at once begins boring its way through the intestinal wall and passes into liver, mesentery, peritoneum, brain, or other organ. Here it encysts but continues its development. If the intermediate host is an invertebrate the next stage is a cysticercoid; if a vertebrate, a cysticercus. The difference is chiefly in the large bladder or caudal vesicle of the latter. The cysticercoid has typically three parts: scolex (the tapeworm head), a body, and a caudal vesicle, the latter forming an enclosure for the other developing parts inside it. In the final host the scolex is pushed out, attaches with its hooks to the wall of the alimentary tract and begins to grow.

The cysticercus is attained from the hexacanth embryo in the following manner. The hexacanth embryo, having reached its place of encystment, enlarges markedly and its interior becomes filled with fluid or with loose spongy tissue. For this reason it is called the bladder worm stage. A small invagination into one side appears which deepens and develops into the scolex, but in an inverted condition. An elevation at its bottom becomes the rostellum, and the suckers appear on the inside of the lateral walls near their base. Metamorphosis of such a larval form takes place after transference to the final host by the eversion of the scolex and very active growth in the region just behind it to form proglottids.

In a few instances instead of a single scolex many are produced by the cysticercus by budding from its interior. This is the case in Taenia coenurus, which produces as invaginations from its wall many scolices that are later to be everted. In Taenia echinococcus this polyembryonic development may go even farther, the ingrowths from the wall becoming separated off to drop into the cavity as secondary bladders. Each of these goes on actively producing new crops of scolices.

IV. THE NEMERTINEA

Of the four groups of the nemertean worms only one so far is known which develops by metamorphosis. In this (Heteronemertini, Schizonemertini) there are two families and the characteristic and important larval form is the pilidium. In one of the families, however, there occurs a creeping form which is really a pilidium modified for creeping in keepTHE PILIDIUM 153

ing with the similar habit of the adults. This is known as the larva of Desor and is that of the genus Lineus. The nemerteans, while showing a distinct advance over forms already considered in acquiring a second opening to the alimentary tract, the anus, exhibit many primitive features which relate them to the flatworms and also to the ctenophorcs. The pilidium itself also is prophetic in certain of its features of the

trochophore larvae of higher groups. Cerebmtulus has been most studied in America as a type of nemertean development.

The Pilidium

The eggs of Cerebratulus cleave spirally and form blastulae and gastrulae in the manner typical for such eggs. The free-swimming pilidium is a helmet-shaped larva with a spike of long cilia arising from the apical plate of cells. The cilia elsewhere are uniform in size and distribution except at the margins where a ciliary wreath may be seen. This is the locomotor organ of the embryo, the prototroch. The sides of the umbrella-like portion are prolonged downward into hanging lobes or lappets. The pilidium is produced from the symmetrical gastrula by the unequal development of certain parts so that the blastopore opening becomes oval in shape and the invaginated enteron grows in length and bends

over to one side, the bent sac-like portion becoming the stomach and the open funnel the oesophagus.

From two large cells which pass into the blastocoele the mesenehyme is produced. It consists of a mass of stellate cells whose amoeboid movements may be seen through the transparent outer covering. The pseudopodia which are put out enable the cells to attach and some are converted into muscle fibres. The pilidium is completed in this condition and swims about for a considerable period, perhaps two weeks, feeding at the surface of the sea upon microscopic organisms.

The metamorphosis of the pilidium has proven elusive since it is not yet possible to rear the animals under laboratory conditions and only fragmentary information has been gleaned from the material collected from the sea. We have to do here with the first of these transformations, numerously observed in the invertebrate groups, in which only part of the larval structures are included in the adult animal. In this case the larval ectoderm, prototroch, lappets, and apical sense organ, as well as the fused outer parts of the amniotic invaginations about to be described, form a double bell-shaped structure which is left behind like a cap after the little worm is differentiated and has constricted itself away. This

larval rudiment swims about for a time, and then, unable to feed and exhausted, it dies. 154 TYPES OF INVERTEBRATE LARVAE

The formation of the worin's body from the larval pilidium begins with four eetodermal invaginations which appear on the flattened lower surface. These amniotic invaginations form, in their deeper portions, the imaginal discs which contribute largely to the definitive body of the worm. They are distinguished as right and left anterior, in front of the

fir: 103 A. pilidium larva of Cerebralulus lactus (Redrawn from M:icBri(le, after C‘ B Wilson) lap , lappet, oes , oesophagus, st , stom ieh, II|("a0ll , iiie-seneliyme cells a p . apical plate B, a. pilidium Just before metamorphosis (Redr l.Wll from Mac Bride, ziftei Metchnikofi ) 9, p , apical plate, a im , anterior imagimil disc oes , oesophagiis, pr , anlage of proboscis; pt. im., posterior imaginal disc

mouth, and right and left posterior behind it. They continue to deepen and broaden, growing up over the already formed alimentary canal until they finally meet and coalesce. Their outer walls form a temporary larval covering known as the amnion, a delicate envelope separating the body of the worm from the covering of the larva, and the inner fused portion is the skin of the future worm. The intestine of the pilidium is THE PILIDIUM 155

thus included in the body of the new worm and becomes the endodermal portion of the latter.

Rudiments of the other organs of the worm are developing meanwhile. The proboscis develops as an ectodermal invagination projecting into a mesodermal mass which is to become the proboscis sheath. The brain

fiG 104 l‘ullv dt-xcloped pllulinm uitli young Il(_‘l11(‘ll\ Ill sutlun its amniotic mu‘ (ltcdumn flolu lunschnlt and Hculu, after liutsrhli )

rm, iunnion (l , inushnc of pilidium lama surrounded bv worm, cc, cctodmm of \\o1m, in . mouth of piluliuin, n , l)Q;£1l\lllng()f ncnous svstem, r , probosus so excrcton organ

is of compound origin, arising as an cctodermal proliferation from the anterior imaginal discs. The formation of the anus and certain other organs has not been followed through because of the lack of material. However, from the cndodermal portion of the pilidium and the inner part of the amniotic invaginations comes the material from which all the later structures are derived. The outer part of the fused invagina— tions, such as the lining of a cap of which the larval walls are the chief 156 TYPES OF INVERTEBRATE LARVAE

parts, is cast off, and the young animal which it covered is the young worm ready for life upon the sea bottom.

V. THE ANN ELII)A AND MOLLUSCA 1. The Trochophore Larva

The trochophore larva is typical of annelids and molluscs. Other smaller groups, among which are the Polyzoa, Sipunculoidea, and Echiuroidea, also have trochophore larvae, and still other larval forms show relationships to the trochophore which are more or less close. In some larvae simple modifications are present and in others the relationships are harder to trace. It is unquestionably the most important invertebrate type of larva, viewe(l from a phylogenetic standpoint.

The trochophore larva in its simple condition is ovoid and possesses certain characteristic features, most conspicuous of which is the prototroch, a ciliated band about the equator. The prototroch is the chief organ of locomotion and participates in getting food. A group of cells known from its position as the apical organ functions as a sense organ, and from these sensory cells apical cilia grow out as a tuft. In some cases a metatroch, a secondary belt of cilia, is present posterior to the prototroch and a second tuft of cilia known as a tclotroch is present at the pole opposite to the apical tuft. Departures from the typical arrangement of cilia occur in various species. Larvae with the primary ciliated band only are spoken of as monotrochal. In some, called atrochal, the prototroch is not developed, but cilia are present all over; in others, without a prototroch, a mctatroch only is developed. Polytrochal larvae also occur, but these are later stages in which secondary bands of cilia are formed about the developing post-trochal region.

Internally a trochophore has a complete digestive tract with mouth, large, bulb-like stomach, short intestine, and an anus. The mouth of annelids is the old blastopore or an opening developed at the same place as the blastopore after a very temporary closure. The intestine meets an ectodermal invagination, the proctodaeum, with which it fuses. and an opening breaks through completing the alimentary tract. An archinephridium is present, running from the ocsophageal region diagonally to the end of the intestine. Each contains a flame cell, or solenocyte, with a cavity and a tuft of cilia, and an excretory tube leads from it. In some trochophores there is an eye-spot containing red pigment cells; it is sensitive to light. The mcsoblast cells, or teloblasts, derived from 4d, are present. (or their descendants) and later elongate into two strings of cells, the mesoderm bands. THE ANNELID TROCHOPHORE 157

A typical trochophore as described is derived from the gastrula by seine simple changes, the chief of which is the shift of the blastopore from the vegetative pole to the lateral position. In this process several factors take part. One is the increase in rate of development and in the actual number of cells of the dorsal posterior cells, particularly the descendants of the 3d cell. This inequality of growth tends to push the opening sideways. In some forms the blastopore also becomes oval in shape, then constricts in the middle, and the portion in the a-b quadrants is pushed anteriorly by the growing cells of the d quadrant. Of these two openings the anterior one becomes the mouth and the posterior one after temporary closure reopens to become the anus. This procedure is made much of by some authorities who reason that in this manner must have come the separation of the original ingestive opening into two, one of which is ingestivc and the other egcstivc.

In the fully grown trochophore larvae of all the groups in which it occurs are found the points of structure as described. Indeed, the homologies between the various groups are complete even to the details of trochophore development. When one considers the remarkable array of organisms which in spite of total absence of agreement in adult features have this type of larval structure, he must find the fact of their common method of origin very surprising and significant. Nemerteans, rotifers, annclids, molluscs (except cephalopods), and bryozoa, form a series which certainly presents a complete gamut of adult variation, yet all come from larval forms with features that are in general the same. It would, however, be even more surprising if there were not minor differences to be found in the trochophores. There are variations in the relation of the mesoderm mother cells to the gut wall, of the persistence of the protonephridia, the presence of the anal vesicle, of a prototroch, of the gastropod shell gland, and in other special organs which are the peculiarities of particular groups. It is notthese differences, however, which deserve emphasis, but the common features of development which find expression in the widespread trochophore type.

2. The Annelid Trochophore

The metamorphosis of the trochophore into an adult annelid may next be considered. It consists chiefly in the growth in length of the post—troehal region and in the differentiation of certain elements found there. The essential features of the metamorphosis are (a) the elongation of the post—troehal region to form the body of the worm (post-cephalic portion) and its consequent segmentation; (b) the apparent reduction (which is not real, but simply relative) of the troehal and preoral regions 158 TYPES OF INVERTEBRATE LARVAE

and their resulting changes to form the head of the worm; and (c) the disappearance of the ciliated bands. The processes are of course accomplished gradually, there being no moment at which the trochophore ends and the adult begins. The post-trochal region is one of active growth, differentiation, and cell multiplication. As an example of the metamorphosis of the annelid trochophore, Polygordzus has been often studied,

fiG. 105 Troehophorc of P(ll_Ij(]0rdLu8. (After Woltereck) An , .irch1ncphr1d1um

11 p . apical plate, mt. intestine, mtt, mctatroeh, 0 , mouth. pr t. prototroch st stomach, ti 1: . telotroch.

and no other is probably better known. It has been figured by Hatschek, Agassiz, and others, but is best known from the work of Woltereck. The elongation of the post-troehal region in Polygordzus involves especially the growth and division of the cells of the intestinal walls, the multiplication of ectoderm cells and the growth and differentiation of the cells of the mesoderm bands. The descendants of the 4d cell form the mesoderm bands, symmetrically placed on the two sides of the intestine The pole cells from which they came are known as teloblasts. The bands multiply not only in length but in thickness and in each a series of cavities THE ANN ELID TROCHOPHORE 159

gradually appears. These are the mesoblastie somites, and they are marked off from each other by constrictions which are traced on the surface by transverse grooves in the ectodermal covering. Their cavities grow progressively, and as they expand they fill up the surrounding space which was the remnant of the blastocoele. Ultimately they meet above and below the intestine, their walls fuse and break through, making a continuous pouch in each segmfint instead of a pair. Evidently in the growing worm, segments are not a in the same degree of advancement.

The origin of the excretory organs shows two stages in development in the annelids. The archinephridium by the addition of other cells from the third quartette and by increase in number of its own cells becomes a protonephridium, a rather complicated structure whose basis is flame cells. The origin of the permanent nephridia has been the cause of controversy among embryologists, particularly as to their derivation from ectoderm or mesoderm. These posterior or permanent ncphridia or metanephridia grow from strings of cells lying in the wall of the embryo and running posteriorly. These break up into loops and a lumen appears which later becomes the tubular nephridrum. In N crezs, Wilson described these as of eetodermal origin except for the funnelshaped opening which he hsaid lils meso- P115;-orfilfiy agljlgrdliisziiigwlirégvftgi dermal. Others consider t at t e entire ‘fiolmeck end is mesodermal and secondarily at- a_ anus? 1,. posterlor b(,,d(., 0; tached to the eetoderm. Still others think h:*:‘:o““1i:E:SDI1 v I>F0t0neDh“d1«* theentirestructureisectodermal.Although ' D ' the details in Polygordzus are not fully known, Woltereek holds to the ectoderrnal origin.

The nervous system begins with the mass of nerve cells that lies under the apical tuft. This is the cerebral ganglion and from it radiate eight nerves to the cells of the prototroeh. Two, the lateral nerves, continue across the prototroch around the oesophagus to form the ventral nerve cords.

These are the beginnings of the more important organ systems of the transformed trochophore. For the details of the metamorphosis and for 160 TYPES OF INVERTEBRATE LARVAE

the conditions as found in special forms reference should be made to the monographs and special articles dealing with these matters.

3. The Molluscan Trochophore

The metamorphosis of the molluscan trochophore is more complicated and involves the interposition of another larval stage, the veliger. While in the trochophore the characteristic larval organs are present, in the veliger there are also the rudimentary stages of the adult organs. There are three characteristic organs of this stage: the velum, the shell gland,


fiG. 107. Young trochophore of Patclla cocrula. (After Wilson.)

a.p., apical plate; 111., mesodermnl cell; m.b., beginning of mesodermal band; 1no., mouth; s.g., shell gland; st., stomach.

and the foot. The velum is derived from the prototroch of the trochophore and is in the form of a bilobed, much enlarged projection abundantly provided with cilia. It serves as the locomotor organ of the voliger and disappears with metamorphosis. The shell gland is at first a simple invagination opposite the month which may open out to form a flattened disc or actually evert. Its cells secrete a thin, horny cuticle which is the shell of the trochophore. In the case of the bivalve molluscs the rapid extension of this area forms the mantle and calcareous as well as horny material is secreted, thus forming the two valves of the shell THE MOLLUSCAN TILOCHOPIIORIQ 161

connected by a region known as the hinge. The variations in the shape of the mantle lobes and the shell secreted by it and in the length and proportions of the hinge correspond to the various systematic groups. The foot in the earliest stages is a thickening of the ectoderm cells just ventral to the mouth. In the cavity of the slight hollow forming behind this bulging foot are mesenehyme cells which contribute to the differentiation of the organ. Other organs make their appearance in the developing veliger, including a larval kidney which disappears as the foot grows out, the muscles, the ganglia, gills, coelome, liver, and secondary structures as crystalline sac and otocyst. The details of their development are beyond the scope of the present account.

The metamorphosis of the veliger into an adult-like form is not a process of long duration. The appearance of the organism is surprisingly


Fm. 108. A, embryo of a heteropod. (llcilmwu from Balfour after Fol.)

u.. arelienteron; 0., body r-avity; f., foot; mo., mouth; s.g., shell gland; v., velum. B, young veliger of I’l(mr0l2runL'hidium. (Redrxuvn from Balfour after Lancaster.) in., loop of intestine; y., residual yolk spheres; n.g.. nerve ganglion; ot., otoeyst.

changed largely because of the sloughing off of the cells which formed the velum; this process and some others coincident with it allow the organism to assume the external shape of a small adult. The larval muscles disintegrate, the anterior region with the mouth shrinks, drawing closer together the mouth and anterior adductor and advancing the front end of the foot. As a result the position of the developing gills is changed and the intestine is shifted and straightened. Although now the organism has the recognizable form of an adult, it is of course very immature and numerous internal changes have yet to be undergone. Labial palps and gill filaments in the bivalves, adult kidneys, pericardium, the final relations of the mantle cavity, development of the gonads and their ducts, all these and other minor processes of differentiation are still to be undergone before the final condition is reached. 162 TYPES or INVERTEBRATE LARVAE

VI. THE CRUSTACEA Nauplius Larva

O. F. Mjiller long ago studied some forms of copepods which we now know are larval,‘ but he thought them adults and gave them the name Nauplms. In this way originated the term that now represents a stage common to all Crustacea. In the lower forms it is usually a free~swimming larva and in many. of the higher ones it is simply a stage passed through in the egg, but it IS represented in the development of all Crustacea


Fm. 100. A, ventral View of gastrula stage of .l.staru.s flzwialflis. (Redrzmn {min MacBride, after Reichenbach.) e. l., cephalic lobe; th. ab., thoracic abdominal thickening.

B. nauplius stage of the same. an., anus; at‘, rudiment of first antenna; at‘~’, rudiment of second antenna; car.. ridge making the first trace of the carapace; e.l., cephalic lobe; lah.. lahrium; m.. mouth; mn., rudiment of mandible; pr. c., protocerebrum; th. ah., rudiment of thorax and abdomen.

Crustacean eggs show a great range of developmental types, and the various stages show no uniformity throughout the different groups. Cleavage may be superficial or it may be total and nearly equal. A cleavage cavity is usually lacking because of the large amount of yolk, but some species have it in more or less restricted condition. Gastrulation is usually by epiboly and ingression, but here again conditions vary. Cross fertilization is usual, but there are cases of self—fertilization, and parthenogenetic development may alternate with normal fertilization. There are some cases in which only parthenogenesis has so far been discovered. But in all cases a nauplius stage is at length reached.

The form named nauplius by Muller actually had four pairs of appendages, whereas the stage now known as the nauplius has only three NAUPLIUS LARVA

163

pairs. It was Claus in 1858 who named the three-appendage stage which is of such widespread occurrence throughout the Crustaeea. A nauplius


Pro 110 Continuation of I15: 10‘)

at‘

at’

nm

In A the rudiments of muxill K‘ have appearul

and the caudal fork is VlSll)l0 In B thoracic appendages are seen and the abdomen Ill

segmen tmg

larva, therefore, has three pairs of appendages, first and second antennal,

and mandlbular. But the degree of development toward independent existence in the nauplius stage is by no means uniform in the difieient Crustacea. There is in fact a series of larval stages in the C1 ustacea, the most important of which are nauplius, metanauplius, protozoaca, zoaea, mysis, all leading to the adult. There are, also, others less generally important, but more specialized for pai tieular groups. Of those mentioned a completed series occurs in the higher crustaceans only, in some forms of which all are represented. For every stage listed there is some group of higher crustaceans in which the larva hatches from the egg at the corresponding time. That is, hatching, or the breaking out of the free-living’ form from the


fiG 111

Nnuphus of Cyclops (After Claus)

an‘, first antenna; an’, second antenna. man , mandibular appendage. lab , labrmm, ex , exopodlte. en , endopodxte

egg membrane, is a variable process and some certain species may be 164 TYPES OF INVERTEBRATE LARVAE

found to illustrate each stage as a newly hatched larva. Evidently those which hatch in the more advanced stages (for example, the decapods) do not show the nauplius in a full functioning condition as do those in which the nauplius is a free-swimming larva, as in the barnacles. In the

fiG. 112. Zones. of Penaeus, ventral view. (After Claus.)

uni, first antenna; an“, second antenna; e., eye stalk; mn., mandible; mx‘, mx’. first and second maxilla; mxp*, mxp’, mxp3. first, second. and third muxillipeds; pl., beginning of pleopods; ur, uropod; e.f.. caudal fin.

crayfish, for example, the nauplius condition is shown by three pairs of mere thickenings or buds instead of developed appendages and there are in the embryo in addition only two cephalic lobes, two thoracico-abdominal rudiments, and the endodermal rudiment; this is far from a free-swimming embryo.

The nauplius of Cyclops is an elliptical form with no external sign of NAUPLIUS LARVA 165

segmentation, but with an enlarged labrum, openings of the alimentary tract, a single median eye, and the three pairs of appendages. The first antennal appendage shows no sign of a biramous character, but both the second antennal and the mandibular have at least partially developed both exopod and endopod. Examples of forms hatching in this condition are the copepods as well as Penaeus, and Balanus. In Balanus this stage is preceded by one in which three primary segments are recognizable. These become subdivided into eight lobes, which are the labrum, right and left first antennal from the first primary segment, the right and left second antennal from the second segment, and the right and left mandibular and the telson from the third. Future growth takes place between the mandibular lobes and the telson. From this stage the next changes lead to the metanauplius.


Fm 113 Mysis larva of the lobster. Ilomarua amcncanus. lateral view. (After Herrick ) Exopoditcs of the walking legs are to be noted (ex.).

The metanauplius condition is reached at the end of the first molt in those forms which hatch as nauplii, but occurs before hatching in such forms as Branchipus and Lucifer. Two additional pairs of appendages are present, the first and second maxillae, and segmentation is beginning.

In the protozoaea, illustrated by a newly hatched Squzlla, the first and second maxillipeds are present as well as the appendages of the earlier types, the abdomen is partially segmented, but not the thorax, and the compound eyes are making their appearance.

The zoaea, the stage in which the crab hatches, possesses third maxillipeds, some of the thoracic appendages, the number varying with different forms, compound eyes, an abdomen completely segmented, but the thorax showing as yet incomplete indications.

The mysis stage, characteristic of the genus of that name, has all 166 TYPES' OF INVERTEBRATE LARVAE

five pairs of walking legs with exopods, six pairs of pleopods (although in some they are hardly developed at hatching), and segmentation is complete. The lobster also hatches in an advanced mysis stage.

finally in the fresh-water shrimp, Crangon, the condition of the adult is reached so far as external features are concerned at the time of hatching.

Of the less important larval types of Crustacea, no mention will be made here.

VII. THE INSECTA

Among the insects development may involve the formation of very complex larvae and more or less complete metamorphosis, or may be direct. The structure and cleavage of typical insect eggs have already been described in the section on superficial cleavage. The cleavage of the centrolecithal egg results in the formation of a blastoderm which may be of uniform thickness in development or may have early shown a differentiation on the ventral side of an aggregation of cells which will become the primitive streak.

Even if the blastoderm is at first of uniform thickness, it gradually becomes thicker in the ventral region by the multiplication of the cells, and thus in this case too the primitive streak or germ band is formed. Mesoderm is formed by one of three methods. (1) Along the medial line of the germ band an invaginating groove is presently to be seen in many embryos of which those of the Coleoptera may be taken as an example. From the material of this invaginating groove comes the inner layer from which is derived the mesoderm and endoderm. (2) In certain other insects the formation of the mesoderm may be accomplished without the formation of a tube but rather from a middle plate which remains nearly flat and is overgrown at the edges by the lateral folds. It occurs in certain Lepidoptera and other forms.

(3) Still another type of mesoderm formation takes on the character of a proliferation and invagination of cells from a median ventral blastoderm region. This is characteristic of the Orthoptera. At the edges of the germ band the blastoderm begins a folding process and at length the two folds meet over the band in the middle region. Their union produces two membranes, the outer one, known simply as a serosa, and the inner one, the amnion. The germ band continues its own growth and the marks of segmentation become apparent shortly as transparent grooves. An anterior pocket growing dorsally from the ventral germ band is the beginning of the stomodaeum and the foregut, and a similar one at the posterior end forms the proctodaeum. A pair of large prc—eephalic lobes at the anterior end of the germ band develop in time into the lateral THE INSECTA 167

eyes, and antennae and mouth parts appear as rudiments in proper serial fashion. The appendages likewise are outpocketings of the ectodermal germ bands. It is evident of course that the variety of structures found among the insects means great variability in details by which these steps are accomplished. The general body form of the insect is

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Fm 114 Developing eggs of Bmchus quadnmaculatus (After Brauer )

A, tmrisverse section, showing completed blastoderm Dorsal side of egg toward top of page B, section of egg 9. little older than in A through anterior region Cells of veiitml blastoderm are crowded, but dorsal blastoderm is thin and flattened eh . chorion, v pl ventral plate.

completed by the growth of the margins of the germ band dorsally until they finally close over and form a dorsal wall. While this has been going on the progress and development of the internal structures has likewise been considerable and the embryo continues its development until finally ready to hatch into a larva.

During the larval stage the insect feeds, sometimes voraciously, storing up nutritive material for its subsequent development. In the more 168 TYPES OF INVERTEBRATE LARVAE

specialized insects this development is very complicated involving a complete metamorphosis with entire changes of form and often of function as well. The groups of insects which undergo this indirect type of development” or complete metamorphosis are spoken of as the Holometabola and include the Coleoptera, Strepsiptera, Neuroptera, Mecoptera, Trichoptera, Lepidoptera, Diptera, Siphonaptera, and Hymenoptera. The less specialized groups comprise the Heterometabola in which

fiG. 115. (‘ontinuation of 114.

A, Transverse section of egg after closure of gastral invagination. mes., mesoderm; am. ser.. amnio-serosal fold. B, Longitudinal section of an embryo of 32 hours. Am , amnion, ant. mes., anterior mesenteron anlage; caud. pl., caudal plate, mes., mesoderm; post. mes., posterior mesoderm anlage; ser., sorosa; st., stomodaeum.

development is direct and metamorphosis incomplete. These forms lack a true pupal period. They include Orthoptera, Dermaptera, Platyptera, Placoptera, Ephemeridae, Odonata, Thysanoptera, and Hemiptera. Since a distinction between larvae and pupae is lacking it is common to use the term nymph to apply to the young insects after hatching and several molts or ecdyses may be gone through among these forms. The terms, stages or stadia, are used to designate the intervals between the melts; and the term, instar, is frequently used to designate the insect at any particular stage. The Thysanura and the Colembola develop B 

92;-=.'saa‘5*.':. ".2 an

C D 3 ‘°.?g9;ooao%§g§$u°°°%


1,.,........'a.'.¢,=r u


F10. 116. Successive stages through the embryonic area. of Hydrophzlus. (From Korschelt and Hc-ider, after Helder)

A, Formation of invaginnted groove wluch 15 to produce the under layer B, Origin ol ammon. C. Amnion completed over embryonic area. Yolk has undergone cleavage D. Ongin of somxtes. E, Formatmn of tmchne F. Formatlon of coolome

Am.. amnion; c , coolomc, eat, octodcrm. end , ondodorm, mm, mesoderm. m ‘I. fit?!

m\I.4 hf mnundnum mu. m....\..n....u~. unvv\)Cn 4.. o...,.l.,... ..I .....l....I........ .. .... .,mo...,l 170 TYPES OF INVERTEBRATE LARVAE

without any metamorphosis and hence are often spoken of as the Ametabola.

Upon hatching, the larvae emerge with certain characteristics depending upon the group to which they belong; one is usually able to classify the insect into its order by mere reference to the type of larva. Common

65% 

‘

E

F I0. 117. Types of larvae. (From Folsom.)

A, B, Thysanum; C, thysanuriform nymph; E—I, eruciform larvae; A. Fampadea; B, Lep7.'.9ma,' C, perlid nymph (Placoptera); D, Libellula (0donata); E, Tenthredopsis (Hymenoptera); F, Lachnostema, (Coleoptera); G. Melanotus (Coleopteru); H. Bombus (Hymenoptera); I, Hypoderma (Diptera).

names are given to the larvae, such as the caterpillar of the Lepidoptera, the grub of the Coleoptera, and the maggot of the Diptera. The types of larvae are known to entomologists under several terms but they are fundamentally of two groups, the campodeiform and the eruciform. The campodeiform are also spoken of as the thysanuriform in reference to their generalized structure. They are flattened, have a long body, often THE INSECTA 171

with long legs and antennae, hard body plates, caudal cerci with welldeveloped mandibles and active habits. These are characteristics of the adult thysanurans, especially of the genus Campodea, but in the insects which undergo metamorphosis they are of transitory importance only. The eruciform larva is illustrated by the caterpillar or maggot with the cylindrical body which may grow to become more or less spindle shaped, weak integument, and with mouth parts, antennae, legs, and caudal cerei reduced, even to complete disappearance; correspondingly it leads


110 118 Successive stages in the de\ clopment of a pluteus of the Ophiuroidea and Echmoidea (After Leuckart )

ad e , adoral ciliated band, :11 , alimentary canal, an. anus, ar, arms, mo . mouth, per 0 c . porioral cllrated band

a very inactive life. Between these two types transitional forms are easily recognized, for instance, in the genus M antzspa of the Neuroptcra the larva which hatches from the egg is distinctly campodeiform and active but it enters the egg sac of a spider and becomes sedentary, loses use of its legs and completely changes its form, that is, becomes an cruciform larva. For the changes which occur during the growth of the larvae, the frequency of the melts, and the great variety of adaptive structures that are assumed in the various larvae of the insects, the reader must refer to treatises on entomology. Likewise the formation of the pupa is a subject which varies too much in detail to be discussed in this work. 172 TYPES OF INVERTEBRATE LARVAE

The internal changes which accompany the metamorphosis of insects are only incompletely understood. In those forms in which metamorphosis is incomplete certain organs are of larval significance only and their tissues must give way and provide the materials for other struc— tures characteristic of the imago. This destruction of larval tissue, or

int.

fiG. 119. Successive stages in the development of u. hrpmnaria of the asteroids. (After Leuckart.)

ad. c., adoral ciliated band, int., intestine. mo., mouth. oes . oesophagus; pr. 0. c., pre oral ciliated band; pt. o.c., post-oral ciliated band. histolysis, takes place commonly during the pupal period through the activity of phagocytes and is followed by a period of the construction of imaginal tissues or histogenesis. At the end of this constructive period the animal is ready for the final metamorphosis which converts it into an active adult or image.

VIII. THE ECHINODERMATA

In the phylum Echinodermata are to be found some of the most remarkable forms of larvae of any group in the animal kingdom, and THE ECHINOIJERMATA 173

in this group metamorphosis has a peculiar and unusual significance. The larval stages are preparatory for the changes which are to adapt the adult forms to a great variety of living conditions, and they bridge the gap from a rather simple ancestral form to the diverse conditions found among the five classes of living echinoderms. One has only to consider the different types of adults found among the asteroids, echinoids, ophiuroids, the holothurians and the crinoids to appreciate the problem which confronts the simple type of ancestral larval form. Such extensive metamorphoses as are found here have for their special function the adapting of the organism to the very changed conditions in which it finds itself. Since the larval condition is retained to the last possible moment in development, although internal changes of the most


Fm. 120. Successive stages in the development of an auricularia of the holothuroldi (After Leuckart ) Letters as in 118 and 119.

profound character are taking place, metamorphosis is of a typo sometimes spoken of as cataelysmal.

The gastrula of all the echinoderms develops into a form similar to what was probably the hypotheticalancestor of all the classes of the group; it is known as a. dipleurula. From this dipleurula it is conceived that the echinopluteus of the sea-urchin, the ophiopluteus of the brittlestar, the bipinnaria of the starfish, and the auricularia of the holothurian are derived. Of these four larval forms the first two are more closely related to each other than to the other group, in which also affinities are discoverable to the larvae of the crinoids. It is not feasible to undertake here a description of the development of the larvae and their metamorphoses in all these cases. For particular reasons and also because it is the form most commonly studied, we choose to follow through the development of the starfish larva, the bipinnaria, from its origin from the gastrula to its metamorphosis. 174 TYPES OF INVERTEBRATE LARVAE

1. The Bipinnaria

It is characteristic of echinoderm larvae that there should be a bilateral symmetry. Two important trends are noticeable as the transition from larva to’ adult takes place, namely the great development of the left side of the larva with the corresponding decrease of the right side, and the complete change of symmetry to a radial type whose axis is at right angles to the former larval axis. The egg of the starfish goes through a rapid and regular process of radial cleavage resulting in a blastula of about equal—sized cells. The cells become ciliated uniformly, the embryo bursts the egg membrane and, rising to the surface, begins its larval life. Gastrulation has in the meantime been going on, but the formation of mesenchyme is not completed until after the f ree—swimming stage is reached. The larva elongates, becomes somewhat flattened on the ventral side, the blastopore is metamorphosed into the anus, and the larval mouth breaks through anteriorly. The cilia disappear except for certain specialized ciliated _ bands which take on a shape characteristic of particular species. Gradually there appear as outgrowths certain special processes which as they grow carry out the ciliated bands to their borders


uc‘;:‘:)f‘;3O1‘;ngI‘l‘l‘l‘r°\fi:‘el and give the larva its bipinnatc form to which is of Asterms (Arm due the name “bipinnaria” given it by Sars. “3“““-) The earlier investigators were inclined to the al , alimentary - - _ ‘ mm mm” mouth; opinion that the starfish arose as a bud on the 1: ft

pr o 0., pre—oral Cllldtcd band; pt. o.c._ p 03 t- oral ciliated band.

side of the larva. It is now realized that this appearance is superficial only and that the larger part of the larval body is involved in the production of

the adult. The earliest trace of the adult body appears as a five-lobed structure in the left posterior portion of the larva. By the growth and dilferentiation of this structure and the loss of the larval mouth and oesophagus and the formation of the new opening, the metamorphosis into the little starfish is accomplished. In the case of the starfish a temporary fixed stage which is not found in all types of echinoderm is passed through. During this stage certain other larval arms and processes are developed and the larva is spoken of as a brachiolaria. It is now desirable to follow in more detail the changes which have been thus briefly sketched. THE DIPLEURULA 175

2. The Dipleurula

All echinoderm larvae agree, while showing much variation from each other on other points, in the possession of the following features: they are bilaterally symmetrical, have a locomotor organ in the form of a curved and bent longitudinal ciliated band with preoral and anal loops. They possess a V—shaped adoral ciliated band; the alimentary canal

fiG 122 A, Bipinnai-1.1 of Astcmas (Frontal view) B, Side view of an older bipinnaria. Median brarhioliirian process beginning to grow out at b (After Agassiz )

a , anus, a d a . anterior dorsal arm, ad e , adoral eiliated band, int , intestine. L eoel . left coelome,m d a, median dorsal arm,mo , mouth, oes. oesophagus. pt d a . posterodorsiil arm, pt 1 a . postero-lateral arm, pt 0 a , post~oral arm, pt 0 e . post-oral band of fllld, pr .1, pre—oral arm, pr 0 c. pre-oral band of cilia, r eoel , right coelomic sac, st, stomach

consists of the typical four parts, namely, the mouth parts, oesophagus, enlarged stomach and intestine. The coelome is budded off from the apex of the archenteron as a pouch which divides into two lateral pockets and has communication with the exterior by a ciliated canal opening on the dorsal surface to the left of the median line. This canal is the stone canal. Since these features are common to all the different groups of echinoderms it is believed that they must have been the characteristics of an ancestral type from which the different classes of 176 TYPES OF INVERTEBRATE LARVAE

the echinoderm existing today have been derived. This hypothetical ancestor is known as a dipleurula. To this larva the characteristic features of the ophiuroids most faithfully conform, and of all echinoderm types it is the most nearly bilaterally symmetrical, for which reason, along with ‘others, it is probably to be regarded as the most primitive. In addition to the features ascribed to the hypothetical dipleurula, it is assumed to possess right and left coelomes more or less divided into three parts, anterior, middle, and posterior. However, a departure from the characteristic dipleurulan condition is seen in Asterias in that the coelome is divided into only two parts (unless the stone canal and its connections are to be regarded as the homologues of the anterior coelome of the dipleurula and the anterior coelome of the starfish is homologous to the middle portion of the dipleurulan structure). The middle part of

m'p' s.c. rt.md.coel.


l.pt.coel.

fiG. 123. Diagrammatie reconstruction of ancestral dipleurula.

u.. anus; an. coel., anterior coelome; l. hyd.. left hydrocoelc; l.pt. coel., left posterior coelome; m.p.. madroporic pore; rt. md. coel., right middle coelome; r.pt. coel., right posterior coelome; s.c., stone canal.

the body of dipleurula has lobe-like processes extending outwards and covered with ciliated epithelium into which the middle coelome extends. These processes permit a comparison with the lip of the braehiopods and so-called lophophore which bears ciliated tentacles. In both cases the organs function to direct food-bearing currents of water to the mouth. Resemblances have also been pointed out between dipleurula and a simple ctenophore plan of structure, and upon the basis of these suppositions it has been concluded by some that there once existed a class of simple marine animals one member of which was of the general character of a dipleurula and another the ctenophore-like ancestor of the annelids and molluscs. These speculations seem also to give a basis for consideration of the similarities that exist between the trochophore type of larva and those of the echinoderm and at the same time of the very great differences that are to be seen in the early development of

these types. METAMORPHOSIS OF ASTERI AS 177

As an example of the development of an echinoderin, although it is hardly to be regarded as a type of the other classes, the embryology of Asterzas is now to be traced in detail.

3. Metamorphosis of Asterias

By the end of the first day after hatching the free-swimining blastula has been converted into a gastrula which is distinguished from the usual type of invaginate gastrula in that the archenteron occupies only a small portion of the inner space, leaving a large blastocoele still present. Into this space are early budded mesenchymc cells which send out processes and make a network in a gelatinous fluid filling the blastocoele. The gradual leiigthening of the gastrula to take on the form of a cylinder with round ends, the differentiation of the ciliated apical plate and especially of the longitudinal eiliated band, involving a thickening of the epithelial cells where it is to form,with a general increase in the number of cilia on them and a corresponding decrease of the cilia elsewhere on the larval body, are the next characteristic changes through which the young larva passes (fig. 122). In the meantime the coelomic sacs are budded off pm 124 Larva of Asmm from the apex of the arclienteron as in the *1‘ days Old. from dorsal surface case of dipleurula. The gut grows forward, (Alflgjeflgiwftu) I m. becomes constricted into the intestine, (left), persicscoiiixiniidigpiiiiéiiiirg, stomach,and oesophagus, and the oesophagus ;f"‘v’~:‘1‘,l‘:l"t‘;1(;”’§:::,“‘ ' ii: 2 2 v turns forward and ventrally to meet an in- post,-()r.),l aimed band, smm: vagination from the ectoderm, the stomo- "‘°“‘°d“““"‘- 5“ 5‘°“"‘°hv °°‘Sv

_ _ _ _ oesophagus. daeuin, with which it fuses. The anus is the

blastopore of the gastrula stage. With the formation of the arms the bipinnaria attains the completion of its outer features. The structure of these arms varies in the different species. In Asterzas vulgarzs, there are borne by the preoral band two larval arms called the preoral and a median dorsal one, while in A. glaczalzs, A. rubens, and A. berylmus (fig. 122), European species, there are also on this preoral band a median ventral arm and a. median dorsal one which are directed forward; there are also in both cases a pair of antero—dorsals, and a pair of postero-dorsals, a pair of postero-laterals, and a pair of post-oral arms. When the time for metamorphosis has been reached and the larva begins to take on its temporarily attached condition there grows out from its anterior part a series of processes known as brachiolas, a median and two 178 TYPES OF INVERTEBRATE LARVAE

dorsals, and the larva is termed a brachiolaria. Into these arms extensions of the coelome push out and in this particular they differ from the arms of the bipinnaria. These arms as listed include all the lobe-like outgrowths which are found in other starfish larvae.

The Coelomé. The development of the structures connected with the coelome form the most important contribution to the starfish body. After a period of slow enlargement near the oesophagus where they originated, the coelomic sacs begin a remarkable series of transformations. The right sac in some of the larvae grows to form a canal leading to the outside through the right madroporic pore, which soon closes up and is lost; and in other larvae it is never found. The left coelomie pouch, however, always makes a short vertical growth to the dorsal surface, forming the pore canal and uniting with an eetodermal depression to form the primary madroporic pore. Through the beating of its cilia water is passed into the coelome. These structures of the left side are significant for the future of the FM 135_ 1.~m,,m1V;Cw(,;u1;mchio1,.,;,. larvae, for it is the left side which

(3°m°“’h“t 3"“ AB*‘5Si”)- will develop to the greater part of a., anus; a.d.a., anterior dorsal arm; the adult Starfish, While the right

br.a., anterior median brachiolar arm; _ _ _ int., intestine;l.p.c.,left posterior coelome; contributes only a minimum. Never pt.l.a., posterior lateral arm; pt.o.a., post- ‘ oral arm; pr.o.a.. pre-oral arm; pt.d.a., thelebs’ anccstrally the larva‘ was

posterior dorsal arm; st., stomach. symmetrical and the two sides originally produced similar organs.

The sacs now grow in length and the right and left fuse together in the pre-oral lobe, although not elsewhere. A partial constriction of the left sac just behind the madroporic pore divides it into the left anterior and posterior coelomes. The hinder part of the left anterior coelome swells out to form a rather circular five-lobed outgrowth. This is the beginning of the water vascular system and is known as the hydrocoele. In some forms (Asterina) a right hydrocoele and the right anterior and posterior coelomes are also formed, but this is not the ease in Asterias. A madroporic vesicle is formed near the median line from the right anterior coelome. Its origin and position have been variously described, but the best opinion now seems to derive it from the right coelome. These developments complete the structure of the free-swimming biMETAMORPHOSIS OF ASTERI AS 179

pinnaria. It is now ready to settle down, become attached, grow into the brachiolaria and begin the metamorphosis which will produce the adult starfish. Between the bases of the brachiolar arms a region of fixation appears by means of which the larva becomes attached (fig. 126B). It is a thickening of the ectoderm, which becomes glandular, enabling it to fix the little animal to the substratum. The attachment takes place near the anterior end of the larva and gives to that portion

I.br.l.

pt.l.a.

l.pr.o.a. m.d.a.

r.pr.o.a.

r.br.l.

br.a.


Fm. 126. Lateral \ iews of bruoliiolnria ol'As(cr2as1uIgan~r in process of fixation. (Modified from Goto.)

A, Left side of earliest stage. temporary fixation bv the bruchioluriun arms; B, part of older brachiolaria corresponding to the base of A and showing the permanent fixation by means of the fixing disc, the pre—oral lob'e liming shrunk. 1-5, lobes of hydrocoelc growing out to corresponding enlargements of the body wall, I——V, the unlugen of the arms.

br.l., lateral braehiolar arm; fix, disc by which the larva attaches itself; 1.pr.o.a., left pro-oral arm; m.d.a., median dorsal arm; oes., oesophagus; p.d.u., posterior dorsal arm; p.l.a., posterior lateral arm; r.pr.o.a., right pre-oral arm; stom., stomodaeum.

of the body the function of a stalk for the enlarging posterior portion or disc. As development continues the stalk shortens and the disc grows. In the latter are the right and left coelomes, the hydroeocle, stomach, and intestine. In the former are the anterior coelomes, oesophagus, mouth, and madroporie vesicle.

While the larva is becoming attached and constrictions which divide both right and left coelomes into anterior and posterior parts are becom180 TYPES OF INVERTEBRATE LARVAE

ing more evident, the left posterior sends a process over to the right side around the gut. This at length fuses with the right anterior coelome, and as the left and right anteriors were already joined in the prc-oral lobe the entire co_1nplex presently becomes metamorphosed into the single anterior coelome. The right posterior coelome, however, is entirely c11t off from the right anterior and forms the epigastric coelome of the adult. During the time that the left anterior and posterior coelomes were divided from each other by a septum formed by their opposed portions, there appears a groove on the anterior side which is to form the stone canal, while one on the posterior side is the first sign of the perioral coelome. The stone canal becomes connected with the madroporic pore canal and runs down to the hydrocoele. The perioral coelome becomes a crescentic tube about a bud of the stomach which represents the adult stomach. The further development of the alimentary tract is as follows: The stomodaeum gradually disappears, having first become disconnected from the midgut. The oesophagus itself gradually shortens and atrophies as does the intestine, the larval anus having closed. It is stated, however, that a remnant of the intestine persists and from it the rectum of the adult arises. From the left side of the larval stomach the bud referred to above grows to form the cardiac stomach of the adult which may be cverted for the purposes of food getting. As it grows it is surrounded by the perioral coelome. At a point on the left side of the larva, which consequently is to be known as the oral side of the adult, the growing bud makes connections with the ectoderm and an opening appears forming the mouth. The rectum and adult anus do not appear until the body form of the young starfish is practically complete.

final Metamorphos1's. Since the left side of the larva becomes the oral side the right side is the future aboral and the first signs of the body form are seen as five thickened lobe-like elevations of the ectoderm which are the rudiments of the arms and indicate the position of the aboral disc. With the growth of the disc portion, the coelomes become displaced backward in the larva to occupy what will be their position in the new body region. The hydrocoele becomes entirely separated from the anterior coelome. It sends out lobes which are the ru(Iiments of the radial canals of the water vascular system and from which tube feet and outer parts of the system are later formed. The stalk portion, becoming less and less both in size and in importance owing to changes in the shape of its cells and to phagocytic action on some of the others, is reduced until it is included in the disc area and is covered by the oral disc. Only a small projection from the oral disc holds the larva fast to the substratum and at length it is broken as the little starfish completes its body form and wrenches itself free. The further changes which the ENTEROPNEUSTA l 81

organ system undergoes are gradually accomplished during the growth of the young animal. IX ENTEROPNEUSTA Tornarza of Balanoglossus. The modes of development in Balanoglossus and its ielated genera present a great deal of variation. In the genus

fiG 127 New England tornarm. from left side (After l\Iorgan )

a . anus, a d l , axitenor dorsal loop of the longitudinal r-iliated bind up . apical plate; up m , apical muscle band, 011 long longitudinal minted band (-001 H first, second, third. pairs of (oelomie ca\ mes g p, gill pouches mt , intestine o mouth oes , oesophagus per , penoardml sac, pl 1 , posterior lateral ll‘!!! of the lomzitudm 11 mliatod band. prol, pre—oral loop of the longitudinal cihated bind, st, atom l(‘h ttr telotroch, wp , water—pore.

Dolzchoglossus there is a large yolky egg which by a mueh—abridged series of stages reaches the adult without the intervention of any independent larval form. In several of the species of Balanoglossus a type of development which is probably more primitive is found, involving the presence of a special larva known as the tornaria. Originally when this larva was first found i_n towings it was assumed to belong to some genus of the Asteroidea, but the works of Bateson, Morgan, Ritter, and Heider have left no doubt as to its relations to Balanoglossus. Strangely enough C

fiG. 128. Metamorphosis of tornaria from Bahamas. (After Morgan.)

A, just before metamorphosis; B, during metamorphosis; C, young balanoglossid worm with three pairs of gill slits. ap . apical plate, cil. long., degenerating longitudinal ciliated band; col., collar region, col.p, collar-pore; ex., excretory tissue in posterior wall of proboscis coelom, gp., endodermic gill pouch, g.s., gill-slit; pr.p., proboscis-pore; tb ,

tongue-bar dividing the gill-slit; ttr.. telotroch; a.ttr., accessory telotroch characteristic of the Bahamas larva. ENTEROPNEUSTA 183

not all of the types of tornaria which have been described agree in all points, and several different methods for example of inesoderm formation and development of the coelomic cavities have been recorded for this larva. The work of Heider, although the most recent, is the only one which deals with the early stages. He was able to follow through the cleavage and development of the larva up to the tornaria. stage, but could keep his specimens alive only eight days. Morgan’s account from species taken at Woods Hole begins about where Heider’s specimens died so a fairly complete history is available. The structure of the tornaria larva superficially resembles that of the young bipinnaria and it is possible to apply the designations used on the bipinnaria to the longitudinal ciliated band and the posterior transverse ciliated band. This latter is also known as atelotroch, corresponding roughly to the same structure of the annelid trochophore. From the anterior end of the growing archenteron a vesicle is budded off which becomes the anterior coelome or the coelomc of the proboscis of the adult worm. From the posterior wall of the anterior coelome are developed rudiments of the pericardium and the peculiar dorsal heart of the Balanoglossus, as well as the rudiments of the head kidney. The more posterior part of the archenteron proliferates two groups of cells which are the begin- ‘ i

nings of the middle or collar coeloine and the posterior or trunk coeloine. At a level in c, anterior coelome; p.('., front of the collar coelome a constriction 9°” ““"“_1E “."p" ‘3"‘"°' *’°“"

, _ 0., mouth, 1., intestine.

appears which marks the separation of the

proboscis from the collar region of the adult. These two posterior coelomes are formed by different methods in the tornaria taken by Morgan at Woods Hole and those later studied by him in the Bahamas. In the former a solid outgrowth of cells from the gut wall is the rudiment of the coelome. In the latter the wall of the body cavity is formed by the aggregation of scattered mesenchyme cells, a procedure which is rarely witnessed in the animal kingdom. At the time of the constriction dividing the proboscis region from that posterior to it a dorsal strip of ectoderm remains unconstricted and becomes depressed beneath the surface in the form of a groove. This is the neural groove which is folded off and forms a neural tube in the fashion characteristic for vertebrate embryos. Below

it from the anterior part of the oesophagus a median dorsal pouch grows 184 TYPES OF INVERTEBRATE LARVAE

out to form the notochord. Gill pouches develop as several pairs of pockets from the sides of the oesophagus. The further development of the larva consists largely in the formation of the modifications of the coelome, the formation of the collar pores and of the genital organs. The metamorphosis is brought about by the development of a fold in the region between the collar and trunk coelomes and the general growth "in length of the trunk portion of the animal. No such complications of development and metamorphosis are found here as characterize the echino— derms, for the adult itself is of comparatively simple structure. Since the aim of this discussion is merely to show how the embryo is transformed into a young worm similar to the adult, it seems unnecessary to follow through further the details of the development of this very interesting animal.

BIBLXOGRAPHIC Nora

Among the more important accounts of the subjects contained in this chapter are the following: Schultze, Minchin, Maas, Metchnikoff, Géttc, MacBride, Brooks, Appelliif, Korschelt and Heider, Salensky, Lang, Surface, Woltereck, Balfour, Claus, Grave, Bury, field, Batcson, Morgan, Ritter, I-leider on Balanoglossus. These works are cited in full in the bibliography on page 406.


Chapter X Formation of the Mammalian Embryo

(NOTE: In developing a knowledge of comparative embryology especially as it applies to the vertebrate groups the most logical procedure at this stage (in which we have considered various invertebrate larval forms) would be the detailed study of various vertebrate embryos. It would be proper to consider in detail the embryology of amphioxus, the shark, a teleost fish, the frog, and the chick, as is so commonly done in courses dealing with this subject, and of course there are other forms also \vhich might be r-hosen.]

So much material is available upon these various forms that it has seemed Wiser not to devote space to a discussion of the embryology of any of them. Most textbooks of vertebrate embryology discuss at least some of these, and both brief and detailed expositions of the subject are easily available in English. Indeed the choice of forms difiers a great deal with instructors so that it would perhaps be necessary to include all of them to satisfy the selections that would be made in different institutions. In our own case it is our practice to ask the student to obtain a copy of Patton's “Embryology of the (‘hick” and to study the chick intensively in the laboratory. Because of the good accounts which are so generally available and because it is felt that nothing could be added in the present volume that is not easily available in other accounts, it has been decided not to ofier any special discussion of the groups mentioned.

On the other hand, the mammals present many embryological variations from the other vertebrate groups, the understanding of which is by no means so easy to obtain as the preceding cases. In the discussions in the chapters on cleavage, gastrul.-ition, etc., it has often been said that the conditions throughout the animal kingdom are as stated except for the mammals. For these reasons it has seemed best to include here an aiccount of the formation of the mammalian embryo and to leave other groups and the later history of the mammalian embryo for more detailed works.

Considered from the point of view of the embryological differences which are manifested in the class Mammalia, three distinct groups are found: the monotremes, the marsupials, and the higher mammals. In the monotremes, eggs containing a large amount of yolk are laid after the fashion of the reptilian groups, and the special features of the embryology of these forms hark back to the type of development as found in the reptiles more than they forecast conditions of the higher

mammals. A detailed discussion of the monotreme seems to be unnecessary.

I. MONOTREMES

The monotreme egg is the largest of all mammalian eggs since it contains yolk varying in diameter from 2.5 to 4.0 mm. The accounts as

given for Echidna and Ornithorhynchus do not all agree in the exact size 185 186 FORMATION OF THE MAMMALIAN EMBRYO

but variations are within the limits indicated. The egg is developed within a follicle consisting of only one or two layers of cells and when it is passed to the outside receives a covering of albumen and a shell. In Ornithorhynchus the shell is said to be calcified. _

Owing to the presence of a large amount of yolk, segmentation is discoidal, forming a blastoderm upon an unsegmented yolk mass. Semen failed to find yolk nuclei here as is the usual case in eggs with discoidal cleavage. The first two furrows are meridional while the third is parallel to the first and at right angles to the second. A many-layered blastederm is formed having the shape of a biconvex lens, the deeper-arched side of which is imbedded in the yolk.

The chief departure of the monotreme egg from other discoidal eggs comes in the rapid closure of the blastopore which takes place relatively early. The edges meet in a spot where yolk and upper and lower cell layers are continuous with each other, a condition which has given rise to some misconceptions as to the homologues of these structures with those of lower forms. The blastopore itself is the elongated primitive groove.

II. THE MARSUPIALS

The embryology of marsupials has been the subject of study during the last fifty years on the part of several investigators. The work of

Caldwell and Selenka in 1887 represents the first attempt at a study of the early stages of development, the subject of the former study being the Australian marsupial, Phascolarctus, and of the latter the North American opossum, Didelphys v2'rg1'm'anus. In 1910 Hill’s study of the Australian native cat, Dasyurus viverrinus, appeared, and this study in connection with the work of Hartman in 1916 and 1919 on the opossum gives us our best understanding of the embryology of this group. Other workers have been Minot, and Spurgeon and Brooks on the opossum, but the two mentioned are the chief source of our information.

The ovarian egg of Dasyurus, the largest mammalian egg known outside of the monotremes, measures 0.28 mm. according to Hill, while that of the opossum varies from 0.14 to 0.16 mm. The egg of the former is scantily supplied with albumen, whereas around the latter albumen islaid down in delicate concentric lamellae. The eggs of marsupials are richly supplied with yolk compared to other mammalian eggs but a strange phenomenon occurs by which yolk is extruded from the cells themselves into the space surrounding the blastomeres. In Dasyurus (fig. 130), according to Hill, extrusion takes place before cleavage begins in the form of a yolk body at the vegetative pole, but in Didelphys the yolk THE MARSUPIALS 187

is passed out during the first few cleavages and at no time forms a concentrated mass. It is thrown out from both ends or from all sides in greater or less amount during the early divisions. The greatest amount seems to be given off between 2- and 4-cell stages and since the yolk is distributed around the periphery of the egg no one point is the center of the extrusion. The orientation of the eggs likewise differs in these two genera. According to Hill the accumulation of the yolk marks the vegetative pole. The first three cleavages of Dasyurus are meridional but the fourth is horizontal and divides the eight blastomeres into an upper ring of eight small lighter-staining cells and a lower ring of larger more darkly staining blastomeres. The upper cells are regarded by Hill as formative or embryonic and the lower ones as non-formative giving rise to the outer layers of the embryos which are spoken of as trophoblastic. The embryonic portion is derived from the small cells of the 16—cell stage and therefore from the vegetative half of the egg as marked by the earlier extrusion of the yolk body. The larger cells from the animal region of the egg produce the trophoblastic portion. In Dzdelphys no such orientation can be found. Here the first cleavage wF)‘?mg2 ( flfgvage Smges Bugle :0‘ divides the egg into two blastomeres mrgtlnianus EAR; D 1,8 without any indication of polarity A. sectlon through 2-0811 stage. B.

... .. tth h4—llt PB,l or of qualitative differentiation. The f,e(:i;,°’nY 32$‘ ma°s:e:' ;“°P' zonapggf

Second cleavage plane is in general lueida, C, section through stage with about at right angles to the first, D’ mm" th'°"gh “age mm but a shift takes place by which two

opposite blastomeres come into contact with each other as is typical of many eutherian eggs. Thus no section can be cut through the centers of all four blastomeres.

From the 4-cell stage on, the cleavage of the opossum egg is irregular, it being possible to find stages of 6, 8, 10, 12, 15, cells and others. The space between the blastomeres represents a blastocyst cavity and even in the early stages the blastomeres tend to migrate to the wall of the “ovum” and arrange themselves in contact with it. Here they flatten and their outer surfaces take on the curvatures of the surrounding albumen layer. Thus the yolk is left within the cavity formed by the

dividing cells which are uniform in size and structure throughout. The 188

FORMATION OF THE MAMMALIAN EMBRYO

embryo is now spoken of as a blastocyst which is regarded as completed

by the 32—cel1 stage.


fiG. 131.


Drawings from models of the opossum egg. (After Hartman.)

A. 2-cell condition; B. 6-cell stage showing polarity and the fate of the two l’)lu.StUI1ll:I‘(“$ of the preceding stage; C, 16-cell stage; D, a blastocyst of 40 to 50 cells in which no e\ idence of polarity is seen. although it will shortly be reestablished with reappearance of

the endoderm.

The blastocyst of Dasyurus is formed in a different manner. Here the cells of each ring multiply rapidly but continue to occupy their hori



C

Sections through the (After

fiG. 132. blastocyst of the opossum. Hartman.)

A. section through the blastocyst of 70 cells but without endoderm, B, section through blastocyst of 82 cells showing six of the ten endoderm mother cells; C. little later blastocyst showing differentiation of the embryonic area and trophoblastic ectoderm.

zontal positions. Upon reaching the periphery they too become applied to the inner surface of the shell, the formative cells at one pole and the non-formative at the other. This constitutes a blastocyst of one layer of cells, a unilaminar blastocyst. Here too the yolk remains within the cavity. Presently the cells of the formative ectoderiii become differentiated and a little later endoderm formation begins. Individual cells (called endodermal mother cells) migrate in an amoeboid manner below the surface and there unite to form a second layer, the endoderm. This layer continues to proliferate and finally closes up to form a complete lining for the entire blastocyst, the primitive endoderm. This description of the formation of the endoderm by Hill seems to concern an entirely different method from that found elsewhere among the mammals.

Hartman also describes endoderm mother cells which detach themselves from their place in the blastocyst wall and behave in the manner THE MARSUPIALS 189

closely resembling that described for Dasyurus. The important difference here lies in the impossibility of distinguishing formative and nonformative cells among the early blastomeres a11d of relating such cells to the trophoblast and to the ectodcrm of the unilaminar blastocyst.

B

fiG. 133. Continuation of fig. 125. A. B, showing progressive differentiation of the endoderm and trophoblast.

Clearly there is no way by which the endoderm mother cells can be traced back in the opossum to the early cleavage stages and, as Hartman remarked, cleavage is entirely indeterminativc.

While the cleaving ovum of Dasyurus shows a greater degree of determination and much more marked polarity than is the case in Didelphys, 190 FORMATION OF THE MAMMALIAN EMBRYO

Hartman is in agreement with Hill on the general facts as to marsupial development. Even in the opossum egg a polarity of a sort is shown in the fact that the cells in one hemisphere divide more rapidly than those in the other and it may be assumed that the embryonic area is formed by the cells of the more rapidly dividing group and the trophoblast from those of the other. In discussing the formation of the embryo of Eutheria it will appear that the “inner cell mass” of the latter is homologous with the embryonic area of the marsupials and the trophoblast of both groups show a complete homology, a view in which both Hartman and Hill join. In the Eutheria, however, it is held that the trophoblast comes from one of the two blastomeres of the 2-cell stage and the inner cell mass from the other. Clearly the fate of the two blastomeres is different in these two groups for in the marsupials one half of each blastomere goes into the production of the embryonic area and the other half into the trophoblast.

Endoderm Formation

The embryonic area having become localized, a number of small cells undergo modification and become the endodermal mother cells previously referred to. This process begins to take place in blastocysts containing 50 to 60 cells. The cells increase in size, project into the blastocyst cavity, and undergo other recognizable changes. Presently they free themselves from the wall of the blastocyst and by putting out extended tips come in contact with each other so that a layer of endoderm is formed. Sometimes several divisions take place on the part of these cells before they have detached from the wall. The process of true endoderm formation in the opossum and in Dasyurus as well is thus one of the multiplication and migration of cells differentiated as endodermal mother cells from one pole of the blastocyst wall and in no case does it include more than one half of the entire blastocyst, the other half being made up of trophoblastic cells. It will prove interesting to compare this process with that of the placental mammals.

Hartman holds that the opossum egg is intermediate between that of Dasyurus and the placental mammals in its type of development. In size, in absence of polar differentiation in the unsegmented egg, in the crossed arrangement of blastomeres in the 4-cell stage, in indeterminate cleavage, and in early proliferation of endoderm it approaches the conditions of the Eutheria. But in the lack of a morula stage, of an inner cell mass as such (although the embryonic area is homologous with it), and in the method of endoderm formation it resembles Dasyurus. The large size of the latter as compared to other mammals, and the localization of the yolk mass in one portion of the egg (not far removed from ENDODERM FORMATION 191

the telolecithal condition), remind one of the derivation of these forms from a reptilian ancestry.

The blastocyst of the opossum during its later stages undergoes some important changes, most of which are concerned with its growth and enlargement. Its growth takes place by means of spreading and attenuation as well as by the more rapid multiplication of the trophoblastic


D

Fm. 134. Later blastoeysts of the opossum. (After Hartman.)

A. just completed bilaminar blastoeyst. B, a later blastocyst nearly ready for the uppeurance of the mesoderm; C, D, sections showing details of the trophohlast and of the embryonic eetoderm respectively.

emb. ec-t., embryonic ectoderm; tr. ect., trophoblastic ectoderm; s.m., shell membrane; alb., albumen. cells. finally a maximum size of 1.0 to 1.5 min. is reached and the trophoblastic region has come to occupy from four—fifths to five-sixths of the entire surface of the blastocyst. That is, the increase in size concerns the trophoblastic region mainly, the embryonic area growing very

slowly if at all. The cells of the embryonic area become much crowded and the endo derm attains a depth of three or four cells without taking on an epithelial character. The’ cells of necessity are irregular in size and shape. Then largely because of the migration of the endoderm cells they begin 192 FORMATION OF THE MAMMALIAN EMBRYO

to spread. While this migration is active on the part of the cells, no amoeboid movement has been detected by Hartman. With this process the blastocyst becomes biconvex in form, the flattening occurring in the direction of the egg axis with the formative area pressed against the shell membrane. The continuous growth of the trophoblastie area finally brings it also in contact with the shell membrane, thus effecting for the blastocyst a. return to the spherical shape and completing the formation of the blastoderm.

Meantime the endoderm continues its lateral migration until it has reached the trophoblastic pole of the egg, that is, until it has reached the point opposite its own place of origin, and thus a closed endodermal sac is formed within the ectoderm. During all this time the ectoderm has remained as a single layer of quite flat cells. N ow, however, these gradually thicken and become cuboidal. With this condition reached, the formation of the blastocyst of the opossum is completed. From the formative area, the embryo proper is developed in a manner quite comparable to that of the placental mammals; this phase of its embryology is not taken up here as a separate subject for discussion, since the formation of the embryo in the placental mammals is the subject matter of the next division of this chapter.

III. HIGHER MAMMALS

1. General Discussion

The third distinct embryological group of mammals is made up of the Eutheria or Placentalia. The eggs differ from all others in a number of characteristics, the first of which is the size, for all are microscopic. They range from 0.07 mm. in the mouse to 0.145 mm. in the dog and 0.13 to 0.14 mm. in man. (These figures are from Hartman’s calculations.) Even at this small size, however, the eggs are large in comparison to other cells of the body, for here as in other animals there is an accumulation of yolk within the egg. In the older works it was commonly said that the eggs of mammals are alecithal or yolkless. As already pointed out in an earlier chapter this is untrue, for although it is small in amount in the eggs of Eutheria some yolk is present in every sort of egg.

The term isolecithal or homoleeithal previously used in this work for such eggs as these is better applied here than alecithal and some writers use also the terms mieroleeithal, or small-yolked, to distinguish these eggs from the more usual and larger-yolked types which are spoken of as megaleeithal. Although more sparsely distributed than in other eggs, spherical yolk granules and often fat globules as well are to be found in the eggs of mammals. DEVELOPMENT UP TO THE BLASTOCYST 193

The lack of yolk in the eggs of placental mammals is one of the two major factors which are responsible for a very extensive modification found in the early embryology of these forms. Derived as they are from forms that are highly laden with yolk with an extremely discoidal type of development, it is not to be expected that the reduction in yolk would mean for the Placentalia a return to the simple methods of development which are found in the holoblastic regularly cleaving forms, as for example the echinoderms and amphioxus. The presence in all forms of Plaeentalia of a yolk sac, which is derived through the discoidal ancestry, is an evidence, although it contains no yolk, of the lack of simplicity in the development of these forms. The marsupials we saw constituted a step toward the reduction in yolk, for there the yolk was eliminated during the first cleavages. Not even the elimination takes place among the higher mammals for so little is present that it is easily used up during the early divisions. The lack of a yolk—filled hemisphere in the uneleaved mammalian egg very obviously means a most striking modification of the type of development, for in the discoidal monotreme only the animal half of the egg participates in the formation of the embryo. The fate of the yolkless vegetative half in the formation of the trophoblastic portion of the egg has already been foretold in the formation of the blastodise of the marsupials.

The second major factor in bringing about the modifications which are characteristic of higher mammals is also correlated with the yolkless condition. It is the (levelopment of an entirely different mechanism for supplying nourishment to the embryo and foetus before birth and takes the form of a placenta. The segmenting ovum becomes related to the uterine wall in a most intimate manner. This process is called placentation.

As a result of the factors mentioned the mammalian egg develops through a blastoeyst stage. Clearly it is difficult to work out the hon1ol— ogy between this type of embryo ‘formation and that of the forms described in previous chapters. Indeed some writers on mammalian embryology have positively denied the homologies that would be implied if we use the terms descriptive of the embryology of earlier forms for the conditions in the mammals. Such terms as formation of germ layers and primitive streak, ete., may lead to confusion and even contradiction

2. Development up to the Blastocyst

The ovarian egg of mammals exhibits certain characteristic features. It is formed within a follicle which consists morphologically of the same sort of germ cells as itself, but after one of them differentiates in an early embryological stage to become the ovum the remainder develop I 94 FOR M ATION 01*‘ THE M AM M ALIAN EM BR YO

only into follicle cells. The ovary of the mammal at the time of its biith is said to contain in an undifferentiated condition all of the oogonia. which are to be developed during its later life.* That is, the multipli—

‘I\\ ‘ lll ll \\\\§\\ ‘,2

l \§_u

J’

fiG 135. Section thioiigli ow an of ('4 dog (l min Kellicott, iiftcr \\ aldeyer)

0., ‘ Germinzil epithelium ', l) egg tubes c, suiiill ox anon follicles, d. older Uvflrldll follicles, c, ovum surrounded by discus proluzerus, f, semnd ovum in follicle with (- (Onlv rarely are two ov.i thus found in in single follicle) 3:, outer capsule of the follicle, h, inner capsule of the follicle. i, nieinbmmi granulosa, k, collapsed, degenerating follicle, 1, blood vessels. in. sections through tubes of the parovarium, y, iiivolutcd portion of superficial epithelium, z, tmiisitioii to p(‘l‘lt0l'|C"tl epithelium.

cation period is past at the tiuie of birth. Many of these cells are utilized only in the production of the follicle cells which surround each developing ovum. They multiply, become columnar, and form a follicular epitheliuin. On one side only of the follicle a definite accumulation of cells

  • In 8. recent paper, Hargitt (Jour Morphology and Physiology, Vol 50, 1930)

l’m1l((‘\ the claim that in the ovanes of some mammals the production of germ cells ifi continuous DEVELOPMENT UP TO THE BLASTOCYST 195

known as the discus proligerus surrounds the ovum while on the other side a cavity is left by the separation of the cells of the follicle from each other as the structure enlarges. This cavity becomes gradually larger, and is filled with a liquid, the liquor folliculi.

The fully grown follicle is known as a Graaflan follicle. The egg itself passes through its growth period in this follicle and becomes surrounded by definitely recognizable layers. The presence of the vitelline membrane, derived from the ovum, is a matter of dispute in various main Fru. 136. Fully grown human ooeyte just removed from the ovary. (From Kellieott. after Wuldeyer.)

Zena pellueida and follicular epithelium (corona radiata) outside the oot-yte. Nucleus in germinal vesicle stage.

mals. The secondary membrane derived from the follicle is present as a zona pellucida. Often this membrane is so perforated by tiny canals as to give the appearance of radiation in the membranes and hence is spoken of as the zona radiate. In some forms this is surrounded by a layer of regularly arranged follicle cells spoken of as the corona radiate.

The beginning of maturation occurs at the end of the growth period when the egg is ready to escape from the ovary. The first polar body is given off before the ovum has eserred. In the mouse this process is said to take place one-half hour before ovulation. Then the Graafian 196 FORMATION OF THE MAMMALIAN EMBRYO

follicle is ruptured, the ovum escapes into the periovarian space, and is carried into the fimbriated ostium of the oviduct which is in close proximity. The second polar spindle has already been formed and the second polar body is given off after fertilization in the upper part of the oviduct. Related to ‘the process of ovulation are changes in the follicle, which is converted into a corpus luteum, as well as physiological changes of great importance to the organism. However, the history of the embryo, which is the subject of this discussion, does not require the further consideration of these changes connected with the ovary itself, although they are of greatest physiological importance. The cleavage stages occur slowly as the egg passes down the oviduct. Twenty—four to forty-eight hours elapse before the completion of the first and second cleavages in the mouse. In the rabbit fourteen or fifteen hours are occupied by the first cleavage and a correspondingly longer time elapses before the ovum reaches the uterus. Eighty hours are required in the mouse for this passage through the oviduct, four days in the rabbit, eight to ten days in the dog and in certain ungulates it is said that the ovum remains over the winter in the oviduct. Cleavage is total and at first nearly equal, but rapidly becomes very irregular. figures are available for various animals showing cleavage stages consisting of almost any number of cells up to sixteen or twenty. Evidently it is impossible to determine for these eggs the orientation, polarity, and such facts of promoi-— phology as have been shown to apply to eggs of lower forms. Cleavage results in a mass of cells spoken of commonly as a morula. The cells at the outside become differentiated to form a subzonal layer lying next to the zona pellucida while those within the mass constitute the inner cell mass. The inner cell mass is in contact with the subzonal layer on one side but elsewhere a cavity is formed between it and the outer cells. The subzonal cells are also spoken of as a trophoblast or simply as the wall of the blastodisc vesicle, and their relation to the trophoblast of the marsupials is clear from the description already given for those

forms.

3. The Blastocyst

The homology of the inner cell mass with the embryonic or formative area of the marsupial as shown by both Hartman and Hill has also been mentioned. The view held by some that the trophoblast of the Eutheria comes from one of the two blastomeres of the 2-cell stage while the inner cell mass is derived from the other is based on evidence from some forms only and probably cannot be maintained with certainty for all mammalian types owing to the difficulties in determining the orientation. The cavity of the blastodermic vesicle or blastocyst becomes filled fiG. 137. Developing eggs of the rabbit. (After Van Beneden.) A, so-called metagastrula gtage preparatory to the formation of the blastocyst; B, beginning of znstrula cavity. the formation of the inner cell mass. 198 FORMATION OF THE MAMMALIAN EMBRYO

with a fluid which is supposed by some to represent the yolk of lower forms. The subsequent history of the blastocyst varies in different groups.

There are three important stages in connection with the early history of the formation of the embryo. The first is the growth of the blastodermic vesicle during which it takes on the form typical of the particular animal discussed. The second is the formation of the embryo body proper; this stage involves the subsequent history of the surrounding layers of cells. The third is the implantation of the blastocyst in the uterine wall and the formation of the placenta; this stage scarcely comes within the scope of this discussion and can be considered only in passing.

The growth of the blastocyst takes place in a manner similar to that described for the marsupial, the trophoblastic cells becoming extended and flattened and the cells increasing rapidly in number. Cell division at this stage takes place much more rapidly than in the earlier cleavage stages, for in three days after the embryo has reached the uterus in the rabbit it is ready for implantation. In other cases a somewhat longer period is necessary. The size of the vesicle at the end of its growth like the size of the mammals themselves is variable, as is also its shape. It is spherical in the mouse, ovoid in the rabbit, and in the ungulates is long and tapering, reaching a length of 20 cm. in the sheep of twelve days although the diameter remains nearly constant, a couple of millimeters. This growth, as in the opossum, is limited to the trophoblast, the inner cell mass remaining very small and restricted.

Up to the conclusion of the growth of the blastocyst no distinction as to ectoderm and endoderm has been possible among its cells. Formation of the endoderm now begins as described for the opossum from the differentiation of those cells of the inner cell mass which border the cavity of the blastocyst. Here these cells multiply rapidly and at the same time migrate so that they come to form a layer over the entire inner surface of the trophoblast which in this manner becomes twolayered and may be spoken of as a gastrula. Obviously this method of endoderm formation is more closely related to that of eggs cleaving discoidally than to that of the holoblastic types. In some mammals, notably the primates, the endodermal layer remains much smaller than the blastocyst itself, thus forming a double-layered vesicle whose outer layer is separated from the inner by reason of its more rapid growth. Thus of the inner cell mass the layer bordering the cavity becomes embryonic endoderm and the remainder is spoken of as the embryonic ectoderm. From this mass is to be differentiated the body proper of the embryo. It is formative in the strict sense, for all of the embryo is derived from it. The cavity of the blastocyst with its endodermal lining is now spoken of as the yolk sac and, although it contains no yolk, is reminiscent of the Fm. 138. Continuation of 130. A, B. growth stages in the formation of the blastula cavity and the transformation of the inner cell mass into a plate. 200 FORMATION OF THE MAMMALIAN EMBRYO

large-yolked reptilian forms. The inner cell mass minus the yolk sac endoderm which, though once part of it, has migrated away is now restricted to embryonic endoderm and embryonic ectoderm above it; by this time it should be spoken of as the embryonic knob. It is the history of the embryonic knob which especially concerns us.

fiG. 139. A. B, diagram showing the early formation of the blastocyst and the relation of the ectoderm, endoderm, and trophoblast; C, diagram of the development of the insectivore Tupaija from Hubrecht's observations showing the development of the cavity of the ectoderm which opens out to form the embryonic shield: I), development of hedgehog type, also after Hubrecht‘s observations. (Modified from Keibel.)

At about the time when the embryonic knob is distinctly recognizable, implantation takes place. That is, the blastocyst becomes attached by means of the trophoblast to the wall of the uterus and the placenta begins to form. Of implantation there are three types.

(a) Central, found in Carnivora and Ungulata, in some rodents including the rabbit in which it was first described and in the lower primates. In this type the blastodermic vesicle attaches directly to the uterine wall, projecting as it grows into the cavity of the uterus. THE BLASTOCYST 201

(b) Eccentric, as in the mouse and Inseetivora where a uterine fold forms in which the vesicle lies and is later enclosed as the edges of the fold come together.




I’-/7‘ 1.

Fro. 140. Series of diagrams to show development with entypy of the germ. A, the relations of the embryonic knob, the endoderm, and the trophoblast; B, later stage showing the cells of the embryonic knob arranging themselves to form an embryonic shield with the amniotic cavity and Rauber’s layer above it; C‘, later stage in its development. I), Still later stage showing inversion of germ layers. (Modified from Hubrecht’s observa tions on the hedgehog.)

(c) Interstitial, as in the guinea pig, most rodents, and in man. Here the vesicle makes its way into the mucous lining of the uterus and after becoming embedded therein is entirely covered over by the mucosa.

The time relations of the development of early stages in the mammals seems worthy of note, for a very much greater amount of time in 202 FORMATION OF THE MAMMALIAN EMBRYO

relation to the entire embryonic period is consumed by these earlier stages in the mammals than is the case in tlie Sauropsida or in other lower forms. Even the cleavage stages take place much more slowly. It has been suggested that the delay in the development of the embryonic shield (sce below) until after implantation has been accomplished

fiG. 141. A, B, diagram showing the rapid enlargement of the extraembryonic coelome and the cliorionic vesicle. (B, modified from Bailey and Miller.)

is due to the very meager nutrition of the embryo during the period in which it is free in the uterus. This view is perhaps borne out by the sudden rapid development which takes place immediately after implantation has been accomplished. Yet it is hard to understand why the cleavages should be slowed down to such an extent as we find to be the case if the factor of nutrition is the only one involved, for during the cleavage stages at least a small amount of yolk is always available. THE AMN ION 203

In the meantime the embryonic knob has continued its development and mesoderm has been formed. As the extraembryonic mesoderm grows, it pushes in between the trophoblast and the yolk sac endodcrm and the entire extraembryonic wall takes part in the formation of the socalled chorion, the serosa. Sometimes the trophoblast is spoken of as the chorionic ectoderm. The formation of the mesoderm in the mammal is a less conspicuous process than in some of the lower forms. It takes place entirely by delamination and migration of cells which are usually from the ectoderm. In some forms it is stated that the mesoderm is related to the endoderm but certainly the usual derivation is from the embryonic ectoderm. It will be noted that this separation of the mesodermal layer takes place before the formation of a primitive streak or any other elements of the body proper.

4. The Amnion

We may now return to the behavior of the embryonic knob as such. From this structure are derived not only the embryonic shield, which corresponds in a general way to the blastodermic disc of Sauropsida, but also the amnion and the structures connected with it. It is necessary to consider the formation of the amnion before taking up the origin of the embryonic shield. Mammals show two separate methods of the formation of the amnion depending apparently upon the relations of the trophoblast to the embryonic knob. In some forms the trophoblast comes to be interrupted over the embryonic knob which thereupon develops in a manner that is entirely different from the cases in which the trophoblast is continuous. In the latter case the trophoblast cells are said to constitute Rauber’s layer.

The details of the formation of the amnion under these two conditions vary in the different orders of the mammals and cannot be gone into here. The important features only can be pointed out. Taking up first the case in which the trophoblast is interrupted above the embryonic knob, we find two different methods by which the amnion is established although its subsequent history is quite alike in both cases. In the one which is illustrated by the inseetivore Tupaija studied by Hubrecht, the knob develops a cavity which opens to the outside as a groove. The edges of this groove make contact with the trophoblast adjoining them and later fold over to form the amnion itself. The bottom portion of the groove gradually flattens out and it is this area which becomes the embryonic shield and from which the body of the animal develops. In the other case as illustrated by the rabbit, the cells of the knob take on the form of a flat plate without the formation of a groove, but their edges are connected with the trophoblast and fold upward to form the amnion 204 FORMATION OF THE MAMMALIAN EMBRYO

as in the preceding case. There is here suggested a certain relation to the method of formation of the body of the embryo and the amnion in those forms having typical discoidal cleavage such as the birds and reptiles. The subsequent development of the embryonic shield in these forms also recalls that of the sauropsidan blastoderm. (figs. 139 and 140.)

flu. l42.—Sections through four stages in the early development of the insectivorc Tupaua javanica. (From Kellicott, after Hubrecht.)

A, blastodermic vesicle completely closed. endoderm still continuous with the embryonic ectodcrm. B, C, embryonic ectoderm split and folding out upon the surface of the vesicle. pushing away the trophohlnst cells: D, embryonic cctoderm forming a flat disc on the surface of the blastodcrmic vesicle.

E, inner cell mass ("ectodermal shield"); ec., embryonic ectoderm; en.. endoderm; tr., trophoblast.

The second method of formation of the amnion differs in many particulars from the first. The trophoblastic layer entirely covers the embryonic knob, a condition which is known to mammalian embryologists as entypy of the germ, and because of it the so-called inversion of the germ layers is brought about. It will be recalled that the embryonic C





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5.1. nu.


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fiG. 143. Sections through the blastodermic vesicle and blastocyst of the albino rat.

(After Huber) A, stage of 6 days 14 hours; B, 7 days; C, egg cylinder stage of 8 days. 206 FORMATION OF THE MAMMALIAN EMBRYO

knob may be likened to a hanging drop projecting within the cavity of the vesicle and that the lining of the cavity is endoderm, although this actually covers the outer or convex surface of the knob. Within the ectodermal portion of the knob where the cells are loosely arranged spaces now appear which gradually coalesce and they form the amniotic cavity. The ectodermal cells forming the roof of the cavity become the ectodermal layer of the amnion. The floor of the cavity on the other hand becomes the embryonic shield. The inner layer of the shield is thus ectodermal while the layer which for a time is actually the outer is endodermal. (fig. 143.)

In some cases, of which the guinea pig and the mouse are examples, the embryonic knob moves gradually to a position well down inside the blastocyst. This process carries with it the lengthening of the endodermal layer on the outside. Earlier students of these forms removed the outer layers of the blastocyst and came upon the embryonic knob which they properly regarded as the formative area. Because of the removal of the outer layers, however, they completely misinterpreted the method of development and were surprised to discover this covering layer to be of endoderm. Hence they spoke of the inversion of the germ layers in these forms and the phrase is still retained in the literature of mammalian embryology, although of course it has no real significance as will be seen from the future development of the body form.

In some forms it happens that the trophoblast layer covering the embryonic knob becomes thickened forming a trophoblastic knob above the embryonic knob proper. This is the Trdger of various writers on mammalian embryology. This may enlarge and in the forms just referred to accompanies the embryonic knob in its growth into the cavity of the vesicle. Within this trophoblastic knob a second cavity may occur called the false amniotic cavity. It has no relation to the true amnion, a completely closed vesicle, and presently disappears without further significance. In certain cases other spaces also develop as in the case of the interamniotic cavity between the cavities of the true and false amnions in the guinea pig. The false cavity may reach a relatively large size in the early stages while the true amniotic cavity remains quite small. Later on the relations are reversed.

5. Embryonic Shield

Regardless of the methods of formation of the amnion there arises in the development of all higher mammals a plate of cells from the lower cells of the embryonic knob in connection with the endoderm which lies just beneath it. This plate of cells is the embryonic shield and from its subsequent development the embryo proper is derived. Of EMBRYONIC SHIELD 207

the entire blastocyst and all the structures connected with it, it is the only true embryonic portion.

In many respects the embryonic shield of the mammal is comparable in its developmental processes to the blastoderm of the chick or other discoidal type. Its development has been studied in a great variety of mammals including the bat, dog, mouse, rabbit, guinea pig, mole, hedgehog, pig, and of course man.

As one looks down upon the shield after the trophoblast has been removed from above, the similarity to the chick is so striking that a very brief description will be sufficient to make clear the main point in development. It consists of a layer of embryonic ectoderm three or four


fiG. 144. Surface view of the embryonic shield of a dog. 13 to 15 days. (After Kellicott.) sh., embryonal shield; k.n., Henson's node; p.s., primitive streak.

cells thick under which is a single-celled layer of endoderm. This stage is reached during the seventh day in the rabbit and about the fourteenth in the dog. Then there occurs in the middle region of the disc a thickening and condensation of the cell layers to form Hens0n’s node or the primitive knot, and extending backward from this is a rather broad line which disappears in the thicker cells of the posterior margin of the shield. Henson’s node and this broad line are of course recognizable as the primitive streak, and shortly extending along its middle the primitive groove is to be discerned. In front of the node the mesoderm can be easily made out in sections appearing as a sheet between the ectoderm and the endoderm. This sheet early separates and, as has already been stated, its extension into the extraembryonic area participates in the formation of the serosa. It is supposed that the mesoderm takes 208 FORMATION OF THE MAMMALIAN EMBRYO

its origin from the region of Henson’s node. From the primitive streak stage on, the arrangement of the layers and parts of the blastoderm are not different in any fundamental particulars from that already noted for the Sauropsida. This is to be expected from the relations of the yolk sac, as already remarked, and shows that the conditions found in the mammals represent a modification of the type of development where a large mass of yolk is present. The development of the body cavity, embryonic and cxtraembryonic, of the splanchnic and somatic layers of the mesoderm, appearance of the head fold, and the other characteristic features of the sauropsidan type of development have their counterparts here, and as it is not the purpose of this chapter to discuss mammalian embryology after the body form has been established, it seems unnecessary to go into these matters. For a discussion of them the

reader is referred to the many available accounts particularly of human embryology.

BIBLIOGRAPHIC NOTE

Among the more important accounts of the subjects contained in this chapter are the following: Caldwell, Gatenby; Hill, Hartman; Assheton, Jenkinson, W. Heape, Heuser and Streeter, Huber, Hubrecht, Patterson, Minot, B. M. Patten,

Van Beneden, Wilson and Hill. These works are cited in full in the bibliography on page 406.

Chapter XI Egg and Embryonic Membranes

I. EGG MEMBRANES

The eggs of all animals are covered with one or more membranes and in these coverings there is a wide range of variation due largely to the environment and to the rate of development of the eggs. Those which are surrounded by water develop rapidly and are produced in great numbers, as are eggs of marine invertebrates, and are scantily provided with coverings. Those which take a long time for development,

as birds’ eggs, or those which are exposed to unfavorable conditions, as insect eggs, have more and thicker egg membranes.

Egg membranes are classified with reference to their origin. Primary egg membranes are formed by the egg itself, secondary by the follicle cells around the egg, and tertiary by the uterus or oviduct. All three types of membrane are sometimes found covering one egg, as in one of the cockroaches, Periplaneta.

If only one egg covering occurs, this can be secondary or tertiary, for example the egg of Distoma which is covered by a secretion from the oviduct. Only in exceptional cases are the egg membranes cellular as the zona radiata of Taenia, the spindle—like egg-shell of Echinorhynchus, the chitinous indented shell of Hydra, and the layers covering the ascidian egg. These membranes are really embryonic membranes. In the case of Hydra there are two membranes which are formed after cleavage from the ectodermal cells.of the developing embryo.

The eggs of some animals have been described as naked. Although they may possess none of the three membranes described above as primary, secondary, or tertiary, still they are not actually naked. We now know that all eggs possess a cortical layer, the outer part of which has been called a plasma membrane. This structure is really a delicate surface layer of cytoplasm which cannot be distinguished from that which underlies it but which is physically different from it. The presence of the layer has been demonstrated by micro-dissection experiments (Chambers and others) which show that the surface of the egg is firm and somewhat elastic, offering resistance to mechanical injury. Plas molysis experiments have shown that this layer is a semi-permeable membrane and that it plays an important role in regulating the exchange which takes place between the cell and its surroundings.

In the animal kingdom as a whole there is an astonishing variability in the manner in which egg coverings appear. In sponges, the development of the egg within the adult body makes membranes unnecessary. They are lacking also in Hydrozoa, Siphonophora, and Anthozoa, although some coelenterates do have them. In some of the lamellibranchs, as Drezssensza, no membranes are present, and the eggs of some others, as M ytilus, have them in the beginning of their development and later


fiG 145 Cross section of egg of Hydra arzsea (Redmwn from Korsehelt and Heidor, after Ehrenberg and Brauer )

cc, ectoderm, en. endoderm with volk granules, im , inner membrane, om. outer membrane

throw them off. In some animals, as echinoderms, the eggs are without membranes when shed into the water but the fertilization membrane is formed as soon as the sperm enters the egg.

A. PRIMARY MEMBRANES

Vitellme Membrane. In many and perhaps in all eggs, there is a vitelline or fertilization membrane. This membrane is the most constant of the primary membranes, though it is often difficult to see before fertilization. Early workers had thought that the fertilization membrane was formed at the moment of fertilization, for, in many eggs, as for example in those of echinoderms, it separates from the egg immediately after fertilization. The presence of this membrane, often some distance from the egg, is an index of fertilization. Its origin is not clearly known. PRIMARY MEMBRANES 211

It has been thought by some to represent a precipitation reaction, by others to be merely the outer layer of

the egg which has been lifted away, or to be a substance produced at the time of fertilization. The separation of the vitelline membrane may be due to several causes, as follows: the egg itself may lose water and shrink, the membrane may swell, or the substance between the egg and membrane may absorb water. The space so formed between the egg and its fertilization membrane is the perivitelline space. (See fig. 7 ) Its size varies considerably in different species.

In some eggs the vitelline membrane is apparently lacking and the egg is covered directly by a chorion or secondary membrane as in the cephalopods. In many eggs it is present before the sperm touches the egg, though the evidence that all eggs possess it is not conclusive. There are many vertebrates in which it has not been recognized, although for some representatives of nearly all classes of vertebrates it has been described. In these animals it is frequently termed the zona pellucida or, if it is traversed by pores, the zona radiata. It is possible that the vitelline membrane of the ripe vertebrate egg may be the result of the fusion of the primary and secondary membranes of an earlier stage.

Amphioxus is described as having a thin vitelline membrane formed near the end of the growth period. When the egg is shed into the water, another membrane, the perivitelline, is formed inside the first, a space intervening fie 146 Successive stages in the

between the two. ‘But immediately c,l,,e.:/ne,l?f:,l,'::":,,°fC31:‘:la:““(:'}:r"'§‘$$.‘f

upon the entrance of the sperm, the facher.) 212 EGG AND EMBRYONIC MEMBRANES

inner membrane hardens and the two fuse. Thus is formed the fertilization membrane which is separated from the egg by the perivitelline space.

The vitelline membrane is usually structureless, transparent, and devoid of canals. It is found throughout all the animal phyla, although, it may be, ndt universally. Often it forms very quickly at the moment of fertilization as just mentioned, but there are cases in which it appears more gradually. In the latter instance, as in Cycles, the attachment of the egg to the ovarian wall remains as the micropyle. A micropyle is not always present in the vitelline membrane, for sometimes it is unnecessary, since in some eggs fertilization may take place before its formation and in others it is porous and easily penetrable by the sperm. There are, however, some invertebrates, as cephalopods, in which the vitelline membrane is lacking.

The true vitelline membrane is a part of the egg itself, but it proves difficult in some eggs to determine whether the membrane which has been designated the vitelline is really primary or secondary. Confusion also seems to exist regarding the origin of the zona radiata, the membrane which lies next to the vitelline membrane. In some eggs, as in selachians and in Petromyzon, the zona radiata lies inside it, and in others, as in the teleosts, the zona radiata lies outside it. This membrane derives its name from the radiations which are seen in cross section and which in the vertebrates at least are due to fine canals.

To classify properly the vitelline membrane and zona radiata of a particular form as belonging to the primary membranes we must know their origin, and this may be very difficult to ascertain. A review of the text—books will show that these names have been given to diverse coverings in many cases without any knowledge of their origin. Hence it will be clear that the membranes as so named are not homologous in all forms. The question is not of great importance, but is considered only because of confusion in the terminology.

It is obvious that the egg itself, if not surrounded by follicle cells, must secrete its own membrane. However, if follicle cells are present they take a greater or less part in forming the coverings of the egg.

Zona Radiata. The zona radiata occurs in some echinoderms, worms, and molluscs, but there is much doubt as to its origin in these forms. In some cases it is evident that the membrane is a product of the egg itself.

Lillie has shown that the zona radiata in the Nereis egg is not a membrane at all but merely the outer layer of the egg protoplasm, and that it consists of closely crowded alveoli. “The zona radiata,” he says, “is in fact a coarse emulsion or foam structure. The jelly is formed by the extrusion or the diffusion of the alveolar contents of the cortical PRIMARY MEMBRANES 213 layer through the vitelline membrane.” The zona radiata of Nereis thus secretes the jelly which surrounds the egg. The structures which seem to be radiations are the collapsed walls of the alveoli. The socalled zona radiata of Nereis is thus not homologous to the membrane of that name in other forms.

The zona radiata has a wide distribution among vertebrate eggs and is found in all classes. It is in many cases doubtful whether this layer is formed from the outer part of the egg or from the follicle epithelium. In cases where there are two or more egg coverings it probably arises from the egg itself. When the zona radiata arises later than the egg membrane outside it, it must be formed from the egg, as Eigenmann has shown for Fundulus.

The purpose of the zona radiata in many vertebrates is clear. Through the delicate canals of this layer, protoplasmic processes of the follicle cells _ penetrate. Nutrient substances from these cells are 5-f



passed through the processes to the egg. The pur— fe pose of the zona radiata is thus that of a nourishing ' I membrane. In the vertebrates it is of considerable v.m. — thickness during the development of the egg. After y the growth of the egg the layer often diminishes B

greatly in size. Fro 147. A portion

In the shark’s egg (Balfour, Giacomina) the zona radiata develops inside the vitelline membrane which is here a true primary membrane, being formed before the follicle cells themselves. The zona in this form is a provisional egg covering for the development of the egg in the ovary. When the egg development is complete, it becomes a thin membrane.

Contrasted with the provisional zona radiata of the selachians is the permanent layer of that name

of the egg follicle and surface layer of the egg of Scyllmm cam'cula. (Redrawn from Korschelt and Hcider, after Balfour.)

f.e., follicular epithelium; s.f., secondary follicular epithelium; v.m., vitelline membrane; y., yolk; z.r., zona radiata.

of cyclostomes, teleosts, and ganoids. In these fishes the zona radiata is often divided into two layers or at least there are two radially striped layers which have the same origin. In some of the fishes as Perca there is a. gelatinous layer outside of it through which run cell processes that connect it with the follicle cells. This and other similar structures frequently present on the surface of the teleost egg would seem to be ehorionic membranes. However, Eigenmann has shown that in Fundulus they are derived from the egg itself.

Although the origin of the zona radiata from the egg has been determined for the selachians and for Fundulus, more work must be done 214 EGG AND EMBRYONIC MEMBRANES

to ascertain what part the follicle cells may have in the formation of this layer in other fishes.

In the bony fishes, since the egg membrane, which is often sticky, is present before fertilization, the micropyle must be formed in a different manner from‘ that mentioned above for many of the invertebrates.

Eigenmann has described its formation

in Pygosteus in which each micropyle ' is due to a long process of one of the follicle cells that reaches to the egg and passes through the zona radiata.

The eggs of amphibians and reptiles have a vitelline membrane which later forms a zona radiata. The formation of this layer has been clearly described by Rctzius for one of the lizards, Lacerta


fiG 148 Section through the fol- _ _ _ hole and outer layers of the egg of vzmdzs. In this form the early follicle 1S

fi:'l§:rfi)“”“”l” (‘Um K°“’°h°” and one—layered. In it cells of two sizes may

fc’ follicular eI,,the1,um, L gala. be distinguished, large cells, the centers tmous layer. ov. ovarml epithelium: of which are filled with round nuclei, §f,‘,,‘,;,,‘§{°°“‘°“‘°“"" ' ’°"" ' ' ' ‘°““ and smaller cells with oval nuclei. The egg itself has a delicate surface layer, the first anlage of the zona radiata. This membrane, as in the selachians and Fundulus, is formed from the egg itself. During the growth of the egg the zona radiata grows thicker, the large follicle cells become pear shaped and send processes to the egg. Some of the cells remain round and lodge between the stalks of the pear-shaped cells. The small cells take up a more distal position, and meanwhile the processes of the larger ones become branched to penetrate the plasma of the egg. The follicle now thickens and the zona takes on its characteristic radiate structure. finally the follicle cells diminish in size and the follicle itself is thinner. , fiG 149 Mwropyle formation The nuclei of the large cells lose much of mus “mamas their chromatin as the cells are stretched fc , follicular epithelium, t r , more closely over the egg. The zona ‘h°°”' ‘°““’““’ Y’ y°‘‘‘' “' 2°“ _ _ radiata. radiata, in which two layers can now be distinguished, is likewise thinner. The nourishing function of the follicle is thus clear, for it is evident that substances are passed to the egg through the long processes of the follicle cells which penetrate the zona radiata. It is seldom that the ormation of the membrane is as clear as

in this form. (fig. 150.) !'-?«"?3"-:'o' fiG. 150. The origin of the egg membranes of Lacerta viridis. (Redmwn from Buchner. pfter Retzius.) For description, see text. 216 EGG AND EMBRYONIC MEMBRANES

In the bird’s egg the primordial follicle contains the ovum surrounded by a one—ce1led layer of cubical follicle cells, the granulosa. The zona radiata is later formed between the ovum and the follicle cells and there has been considerable discussion as to its origin. Bartelmez thinks that it is formed from the follicle cells; at any rate it has a function similar to that described for the reptiles. The follicular cells are connected to the ovum by delicate strands of protoplasm which pass through Fm_151_ Primordialoggfollicle the zonaradiata.Nutrimentdiffusesthrough from ovary of hen. (Redrawn from these protoplasmic bridges, there being no Lime’ after H°u') evidence of the passage of solid food particles. In the bird the primary vitelline membrane formed immediately


Fro. 152. Section through an ovarian egg and follicle of the egg of a pigeon. (Redrawn from Lillie.)

ex.. theca externa; g.. granulosa; g.v., germinal vesicle; in., theca interns; p., peripheral protoplasm; s~s, stalk of the follicle; z.r.. zona radiate. SECONDARY MEMBRANES 217

over the egg as in other animals is a structureless membrane usually considered as from the egg itself, though some workers have thought it to be a product of the follicle cells. It is very diflicult to differentiate the vitelline membrane from the zona radiata and the former may be in part the anlage of the latter, as in the case of Lacerta which we have just described.

In mammals, the origin of the vitelline membrane is uncertain. Some authors say that there is no true vitelline membrane; the transparent zona pellucida next the egg is thus referred to by others. However, if



’ ,lusaUu\‘\n.vn , Ilralnm gunulocum

zona Plxl.\L€.\a.I.



co uldul ' \ i..'.3.i.i1u..i.' vilclluicb \\,g,qg. ‘mime: uunm a nun In unlrun mam rune

fiG 153 An ovarian follicle approaching maturity (From Patten )

this layer is secreted by the follicle cells, as some workers believe, it is of course a secondary membrane. The zona pellucida may be fairly thick, and in the mole, pig, rabbit, and sheep it takes on a radiate appearance and hence becomes a zona radiata.

The term zona radiata is unfortunate in the mammals, for outside this structure is a cellular layer of radially elongated follicle cells called the corona radiata and confusion is apt to exist between these two.

B. SECONDARY MEMBRANES

Secondary membranes are formed by the follicle cells which surround the ovum and are therefore the product of maternal tissue. These membranes, which are truly chorionic in nature, may take on a variety of 218 EGG AND EMBRYONIC MEMBRANES

forms, depending upon the activity of the follicle cells. The distribution of the chorion is more restricted than that of the vitelline membrane, but some eggs which lack the latter possess a chorion. It may arise as a cuticular secretion of the follicle cells forming a delicate membrane which later thickens to assume the character of a chitinous-like shell, as in the insect egg. On the other hand, it may be formed by direct transformation of the follicle cells themselves. Its substance is, according to Tichomirow, chemically like keratin


F 154 A t 1' th fll l - - - . epitlieelium WltlIlJ0tll1;Ol:lh?)r)0: oof lDc‘:ct8': and much “Cher In nitrogen than 15

ms bwolor (Redrawn from Korschelt chitin,

and Heme’) Both primary and secondary mem branes are often present before fertilization takes place, and since they are usually impenetrable to the sperm they are perforated by one or more micropyles situated at or near one of the poles of the egg. In nemerteans and in most molluscs the micropyle is near the lower pole, but in cephalopods and also in echinoderms, insects, and fishes, it is near the upper pole. In the Orthoptera it may be either at the lower pole or at the side of the egg, and in Oedzpoda there is a circle of 30 to 40 micropyles at the lower pole.

The chorion of insect eggs is very different in different species. In the simplest cases it is smooth, one-layered, and structureless. Its surface may have elevations or may be divided into polygonal areas so that it looks like an epithelium. In certain forms, as in the locust, the follicle cells send out processes to these polygonal areas of the chorion around which a shell is secreted. After formation of the shell, the cell processes are withdrawn.

Porous canals through which the egg obtains air often .. _ penetrate the chorion. In Ranatra and N epa, water fiG 155 An scorpions, in which the eggs are sunken into plant iii stalks, the chorion is drawn out at the end of the seven processes

. . . h h egg into delicate processes which serve to aereate the §{,b‘§, s‘(’R':d:::,l,:

egg_ from Korschelt

The micropyle is formed in a characteristic manner and Held”) in insects as has been described in the locust M econema vamans. One of the follicle cells sends a long conical process down to the egg. This process remains during the secretion of the chorion and then is drawn back into the follicle. The chorionic pores referred to are formed in the same way. Also the micropyle of the bony fishes is formed in a SECONDARY MEMBRANES 219

similar manner, but as has been earlier mentioned, the membrane perforated in this case is a zona radiata and not a chorion. (See fig. 191.)

In Octopus the chorion is drawn out into a stalk which becomes twisted and serves to anchor the eggs. Among the chitons there are different types of chorions. Some of the eggs have a knobbed surface

and some are covered with needle-like processes. Many actinian eggs also have sharp processes.


Fro. 156. The egg membranes of Meconema varians. (From Korschelt and Heider.) ch., chorion; f., follicular epithelium; m., micropyle.

The myxinoids have a characteristic shell. At each pole of the egg are attached stiff anchoring filaments which end in lobed umbrella-like expansions. At the germinal pole of the egg the shell is marked by a furrow-like ring so that a lid is formed which the animal pushes off at the time of hatching. There is considerable disagreement about the


fiG. 157. The upper part of the egg of Bdellostama stouti. (Rcdrawn from Ziegler, after Doflein.)

A, section showing nucleus and above it the micropyle between the bases of the processes. B. Opereulum and processes.

origin of this shell. Cunningham says that it is the product of the egg itself, and Doflein derives it from the follicle cells. The membrane is usually considered as a true chorion.

In Petromyzon the inner egg membrane is covered with a mucous layer which causes the egg to hang onto stones. This membrane is formed through transformation of the follicle cells themselves. In some 220 EGG AND EMBRYONIC MEMBRANES

of the ganoids also there is a similar adhesive membrane formed from the follicle cells. Under this layer are two membranes, the chorion and the vitelline membrane.

The follicle cells of the ascidians show a special type of modification. five envelopes are formed by these cells and thus we have a unique example of an egg covered by five secondary membranes. When the ascidian egg is still young it is surrounded by a primary follicular epithelium derived from undifferentiated ovarian cells. Beneath this epithelium is a band of structureless membrane. These flat epithelial cells multiply and become cubical. Some of them find their way inside the epithelium and form an inner layer called the test—cell layer while certain of them wander into the egg. The cells of this layer do not give rise to the test of the adult ascidian as was formerly supposed to be the case. As the egg matures, these test cells degenerate and later are found in a gelatinous mass over the egg.

In the solitary ascidians the follicle layer of the egg takes on a special character. These cells, instead of remaining cubical, increase in size and become highly vacuolated, resembling a foam structure. They also develop processes which support the egg and enable it to float.

In addition to the follicular membrane and the test-cell layer, two other membranes are formed around the ascidian egg. Beneath the two layers already described, the follicle cells secrete a structureless membrane called the chorion. Still another membrane is formed between the basement membrane and the follicle cells. This is the external pavement epithelium and it may be regarded as another layer of follicle cells. There are thus five membranes over the ripe ascidian egg. Next the egg is the gelatinous layer of test cells, and over this are the following layers, the chorion, the foam-like follicle epithelium, the external pavement epithelium, and the basal, follicle membrane. Since all these membranes are derived from the follicle cells they are secondary membranes.

In the Dipnoi the primary membranes are covered by the gelatinous tertiary membranes, and secondary membranes are absent. In the frog’s egg there is a thin but tough membrane around the vitelline membrane and this is secreted by the follicle cells. Over this is the jelly formed by the oviduct, so the frog egg has all three types of membranes. In the urodeles this secondary membrane appears to be lacking. In reptiles and birds the chorion seems to be entirely lacking, for the egg white and shell are tertiary membranes.

From the descriptions just given it will be seen that the chorion has a variety of forms and that its special characteristics are adaptations to the needs of the different species.

Comparable to the chorion in a certain sense is the mammalian SECONDARY MEMBRANES 221

follicle which is here described in some detail. Although of course it cannot be considered as a membrane, still it is formed by the follicle cells. As described in an earlier chapter, the mammalian ovum is highly specialized because of the intra-uterine development of the embryo. There is only a very small amount of yolk present in the egg as contrasted with the large amount in the eggs of birds and reptiles. Secondary and tertiary membranes are entirely lacking, but the Graafian follicle

Fm 158 The developing ovum and follicle cells of the cat (Redrawn from Buchner) See text for description.

which surrounds the egg is a product of the follicle cells. (fig. 153.) In earlier times mammals had eggs similar to those of reptiles and birds, for the monotremes, the simplest mammals, possess an egg with shell and egg albumen. In the entire animal kingdom the Graafian follicle is probably the most specialized structure produced as a modification of the follicle cells. In the middle of the follicle is a cavity filled with liquid, known as the liquor folliculi. The ovum itself, surrounded by the zona pellucida and the zona radiata, is attached to the Wall of the Graafian follicle by a group of cells known as the discus proligerus. The cells of the discus 222 EGG AND EMBRYONIC MEMBRANES

are continued into the cells of the follicle wall known as the membrana granulosa, which consists of many layers. Outside the membrana granulosa the ovarian connective tissue is differentiated into two investing layers, the theca folliculi. The outer of these is densely fibrous, and the inner cellular, penetrated by small blood vessels. Buehner describes the growth of the Graafian follicle in the cat (fig. 158), where it begins as a simple follicle in which the ovum is surrounded by a cellular layer, the granulosa. The cells about the ovum multiply rapidly, and part of them lose their connection with the upper surface of the egg to wander out to form a second loose ring around it. The rings separate sharply from each other and each becomes many-layered, while a cavity known as the antrum appears between them. This cavity becomes filled with a liquid which is secreted into it and quickly enlarges. The outer ring of follicle cells is crowded to the periphery and forms the stratum granulosum. The ovum itself at first bulges slightly into the cavity of the follicle, and later as its surrounding cells are undercut protrudes farther into it, its attachment to the follicle being new a delicate stalk of cells, the discus proligerus. When the egg is ready to escape, me. 159. Follicle and portion of cyto- this narrow sta‘k is broken, and plasm and nucleus of ovum of a rabbit. (Re the follicle ruptures, the egg passes drawn from Buchner.) _ through the tube into the uterus. The follicle now undergoes a transformation and becomes the corpus luteum. Sometimes the follicle cells immediately around the egg are found clinging to it after its discharge.

The mammalian ovum and its surrounding follicle are thus seen to be highly specialized. The presence of only a very small amount of yolk and the preparation for the attachment of the ovum to the uterus are all adjustments to the intra-uterine development of the embryo. The role of the follicle cells as a nourishing membrane has been definitely determined in the dog by experiment. The follicle cells are filled with mitochondria. When lecithin is injected into a dog these mitochondria increase in number. However, if the dog is allowed to become hungry, the mitochondria decrease. They seem to act as store houses for the TERTIARY MEMBRANES 223

developing egg. The identification of lecithin or of a similar substance has been observed by Russo in the protoplasmic bridges which penetrate the zona radiata.

C. TERTIARY MEMBRANES

Tertiary membranes, unlike primary and secondary, are formed after the egg has left the ovary. They are secreted by the oviduct or uterus or by special glands connected with them. Tertiary membranes are of various kinds, gelatinous, horny and chitinous, or cocoon-like. The type of membrane shows adaptive correlation to the needs of the developing embryo. The gelatinous type of covering is frequently seen in fishes and in amphibians and also in many invertebrates, as Geryonia, and Sagitta. Chitinous shells cover the eggs of the phylopods, Apus and Branchipus, and a horny capsule covers the shark’s egg. Under the tertiary membranes there may be a primary or secondary membrane or both for in some eggs all three types are present.

In the cephalopods the tertiary membranes show different modifications. The egg of Sepia and its surrounding albumen is covered by a black leathery capsule, but in Loligo the eggs, each in a firm envelope, are arranged in a gelatinous mass known as “dead men’s fingers.” The flatworms have cocoons which are formed in the ovary. There are various kinds. Branchiobdella has a stalked capsule containing one egg. The rhabdocoele turbellarian cocoon contains several eggs. In this capsule and in that of the trielad Dendrocoelum there are a great number of yolk cells included beside the egg and these serve to nourish it. The trematode capsule contains one egg and is either stalked or provided with a lid or both may be present. The polyelad capsule is similar to that of the trematode but there are several eggs in one cell.

Coeoons are sometimes formed by special skin glands. Thus in the lumbricids and in the Hirudinea the cocoon which has a ring-like form is secreted by a special skin gland and drawn off over the anterior end of the worm. In it is deposited albumen for the nourishment of the embryo.

In the gastropods the cocoon is large though the eggs themselves are small, for they are surrounded by albumen. In Limax, Helix, and Paludina there is only one egg in a cocoon. In some gastropods only one egg is deposited but in other cases there are a number, all but one of which are utilized to contribute to the growth of the embryo formed from that one. (This is the phenomenon called by some “cannibalism.”) Some insects also have cocoons which are tertiary membranes as contrasted with the larval cocoon formed for the pupa of the butterfly. Periplaneta has a cocoon which is carried by the female attached to the 224 EGG AND EMBRYONIC MEMBRANES

posterior end of the abdomen. In this cocoon the eggs are laid each enclosed in the vitelline membrane and the chorion. H ydrophilus, the water beetle, has a round cocoon in the form of a web. The female places the cocoon on the under side of a leaf to which it is attached by a stalk. There are fofty-five to fifty eggs in palisade-like arrangement within the cocoon nourished from the substance of the web.

The selachians, when not viviparous, have tough egg membranes. The albumen and the horny capsule are deposited about the egg while it is in the oviduct. The capsule differs in different species. In the sharks its four corners are drawn out into fibers which permit the egg to cling to water plants. Occasionally several eggs are found in one capsule.

Water-living animals frequently have eggs with gelatinous coverings. They are laid singly in the urodeles and in Ceratodus. In many other animals, however, the eggs are laid in gelatinous masses of varying sizes which may be irregular (cephalopods and frogs), plate-like (some polyclads, gastropods and insects), or rope-like (some nemerteans and annelids).

A gelatinous covering over the egg is typical of the amphibia. In many of the amphibia there are special modifications of these tertiary envelopes. An interesting example of this kind is that of a tropical anuran. At the time of egg laying the oviducal secretion which surrounds the eggs is beaten up by the hind legs of the parents into a fine foam containing many air bubbles. This foam is sometimes placed on the surface of the pond and floats about or it may also be placed in a wet hollow on the ground. Some of the frogs deposit the eggs in a mass of jelly on one or more leaves. Sometimes the single leaf is bent by the copulating frogs into a funnel which retains its shape by means of the adhesive jelly around the eggs. Some of the Dipnoi (Ceradotus and Lepidosiren) have a gelatinous tertiary envelope similar to that of the amphibians. In Lepz'dosz'ren this layer may be very thin or very well developed.

In birds there are a series of tertiary membranes. The hen’s egg may be described as typical. Immediately around the yolk is deposited a spirally wound layer of egg albumen, the edges of which are twisted into the chalazae, stretching from the yolk to the poles of the egg. About this layer is deposited another layer of egg albumen and over the entire mass the shell is formed. The shell membrane is double and the two layers are separated at the blunt end of the egg to form an air chamber. The shell membrane lies immediately below the shell, which is porous and brittle and impregnated by calcium salts, even to the extent of 98 per cent of the substance. The tertiary membranes of birds are in general like those of the hen’s egg, the differences which occur being due to INVERTEBRATES 225

size, shape, and color of the shell. The egg that is relatively largest is that of Apteryz, for in this species it weighs one-fourth of the body weight of the parent.

The eggs of reptiles are much like those of birds, but the chalazae are lacking. In some forms, as in the lizards and snakes, the shells are more like parchment, little calcareous matter being deposited. The egg-shells of crocodiles and of some turtles are hard like those of birds.

Tertiary membranes are entirely lacking in the mammals with the exception of the primitive monotremes. The egg of Echidna is much like a bird’s egg but the egg—shell is formed of keratin and not of calcareous salts. The mammals have adapted themselves to a terrestrial life by the development of a series of embryonic membranes, as the birds and reptiles have done with egg membranes, but in the higher group it has been found necessary to forsake entirely the devices which were adequate for the lower forms. The membranes of the embryos are considered in the second part of this chapter.

II. EMBRYONIC MEMBRANES

A. INVERTEBRATES

In addition to the membranes which properly are classed with the egg itself the animal kingdom possesses numerous cases of accessory membranes which are developed by the embryo. These are in the nature of cellular sheets which by various invaginations, foldings, outpushings, etc., cover the embryo or parts of it. They are especially well developed in the vertebrates and to that group most of the attention is paid by embryologists. Nevertheless, among the invertebrates there are a good many illustrations of the development of different embryonic membranes. Most common are the amnion and the membrane which is formed in connection with it, the serosa. But there is also an invertebrate yolk sac, surrounded by a yolk membrane, and even a placenta occurs in a prevertebrate group, the ascidians of the family Salpidae. Of course this latter structure is very rudimentary. It is really nothing but a tubercle or knob of rather specialized maternal tissue which becomes richly vascular and to which the zooid already budded off attaches itself for nourishment.

Of the invertebrates proper certain molluscs show the development of the yolk sac. The amnion occurs more or less developed in the pilidium larva of the nemerteans, in the developing Polygordius, in the echinopluteus when it is undergoing a metamorphosis, in the larva of insects and of the scorpions. Some of these groups also show the possession of 8. serosa in connection with the amnion. 226 EGG AND EMBRYONIC MEMBRANES

The Yolk Sac

The true yolk sac can occur only in forms having an extreme telolecithal type of egg structure. Among the invertebrates the cephalopods

fiG. 160. Various stages in the development of 0. squid, showing the relations of the yolk sac. (Modified from Harmon and Gardiner.)

B and C. dorsal views; D, sagittal section. a., arm rudiment; {., funnel; m., mouth; o.c., optic cup; y.ex., external yolk; y.in., internal yolk.

are the only forms which show a well-developed yolk sac. As is described in Chapter V, the cleavage of the protoplasmic cap of the cephalopod THE AMNION 227

egg results in the formation of a series of blastoccnes arranged about a germinal area consisting of blastomeres. These blastocones separate entirely from the blastoderm and rapidly extend themselves over the surface of the yolk underneath the growing blastoderm. They constitute a yolk membrane enclosing the large mass of yolk. Over them the blastoderm gradually extends and when the embryo proper is formed it becomes marked off by a groove from the yolk sac, as it may now be properly called. The yolk sac takes on the appearance of an appendage which it maintains until the development of the embryo is far advanced. Actually the yolk mass becomes divided into two portions, one of which is contained within the body of the embryo and constitutes the internal yolk sac in contrast with the external one which has just been mentioned. The yolk masses of the two are joined at all times, however. The further growth of the embryo results in proportionate decrease in the size of the external yolk sac which is gradually included within the body of the young animal. Morphologically this structure represents a precocious median development of the mass of tissue which produces the arms of the squid and is comparable to the developing foot of other molluscs. Strictly speaking it is not merely an embryonic appendage, for all of it is finally withdrawn into the body of the growing animal. A somewhat similar ventral protrusion from the foot of the snail, Helzlr, was described by Lankester and while not a true yolk sac it is indicative of the tendency so markedly illustrated by the squid.

The Amnion

The first structure in the animal kingdom which may be designated as an amnion is seen in the metamorphosis of the pilidium larva of the nemerteans which is described on page 153 (figs. 103 and 104). On the flattened under surface of the helmet-like pilidium, four amniotic invaginations form. They consist of 'ciliated ectoderm and other deeper parts and are known as the imaginal discs. Their continued inward growth upward and over the alimentary tract finally results in their fusion. The inner parts, or the imaginal discs, form the outer covering of the little worms while the remaining portions of the coalesced invagination make up the amnion which is a temporary covering entirely lost with metamorphosis.

The second appearance of the amnion is seen in the metamorphosis of the annelid, Polygordius. This structure superficially resembles that of the pilidium, for here also four invaginations appear arising from a circular groove which is known as the amniotic fold. It serves as a covering for the folded portion of the worm which remains in this con228 EGG AND EMBRYONIC MEMBRANES

dition until the time of metamorphosis when, by severe contraction, the worm becomes straightened out and the amnion has no further function.

An amniotic invagination is described in the metamorphosis of the echinopluteus of the sea-urchin. It occurs on the left side of the larva as a pit which deepens and broadens until it comes in contact with the wall of the hydrocoele. The tissue which lies between the amniotic in


fiG. 161. Transverse sections of embryos of Clytia. (Redrawn from Folsom after Lecaillon.)

A, through germ band at gastrulation; B, through germ layers and amniotic folds; C, stage later than B; D, through germ layers. a., amnion; a.c., amniotic cavity; c., coelome sac; e.. ectodcrm; i., inner layer; g., germ bond; n., neuroblasts (primitive nervous cells); 59., serosa.

vagination and the hydrocoele undergoes important changes and is involved in the formation of the so-called echinus rudiment. Into the amniotic cavity this rudiment and especially the tube feet develop.

In the scorpion, according to Brauer, an amnion is formed shortly after the two-layered stage shown in fig. 39. At the edge of the blastederm a sheet of cells arises and grows backward and presently a second layer is formed over the first. The outer is the serosa and the inner the amnion. Underneath these the embryo develops.

The amnion of invertebrates reaches its highest development among the insects, and of these the Coleoptera show it most clearly. There are THE AMNION 229

really two types of development with respect to the relations of formative area. and of yolk shown in the insects. In the one type, called by

some “overgrown,” the germ band retains its original position in the blastoderm and the folds of the amnion and serosa arise at its sides and

fiG. 162. Diagrammntie sagittal sections of Calopteryx. (From Folsom, after Brandt.)

A-D, illustrate invaginution of germ band; E-F, illustrate rex olution of embryo. a., anterior pole; a.c., amniotic cavity; am., amnion; z1iit., antenna; b. blastodcrm, d., dorsal; g.. germ band; h., head end of germ band; 1., laliriuin, l‘-l“, thoracic legs; m., mandible; mx., maxilla; p., posterior pole; 5., sorosa; v., ventral; y , yolk.

grow over it. This occurs in the Coleoptera, and it is for this reason that the formation of the amnion is most clearly shown there. In the other type, called “invaginated,” the germ band invaginates at one end of the egg, and is finally carried into a cavity formed within the yolk mass; after the closure of the opening of the invagination the formative portion develops entirely within the egg. Due to this invagination the ventral 230 EGG AND EMBRYONIC MEMBRANES

surface of the developing embryo comes to face the dorsal side of the egg and a subsequent process of revolution is necessary before the embryo at length resumes its original orientation. This type occurs in the Odonata. The relations of the folds of the amnion are shown in fig. 116, which illustrates the development of Hydrophilus, and also in fig. 161, which shows the formation of the amnion in the beetle Clytra. Folds of the blastoderm arise at the side of the germ band and continue their growth until they meet above it and fuse. The membrane thus formed directly above the germ band is the amnion, and the outer one, the serosa. The formation of the amnion and serosa in Calopterya: is shown in fig. 162.

Students of the embryology of the insects are not entirely in agreement in regard to the morphological relations of the embryonic membranes found throughout the group and several types of classification have been proposed. It hardly seems necessary to consider the various classifications or the points upon which they have been based. Serosa and amnion occur together in the Coleoptera, Lepidoptera, Diptera, Dcrmoptera, Isoptera, and Odonata. An amnion only is found in Xenos, a strepsipteran parasite, and even it is vestigial in such forms as M usca and Drosophila. A serosa only is formed in a few of the Hymenoptera including the honey bee, wasps, and ants.

B. VERTEBRATES EXCEPT MAMMALS

Embryonic membranes are especially well developed in the vertebrates where they serve for protection, nutrition, and respiration. These are the yolk sac, amnion,serosa or chcrion,allantois, and its derivative, the placenta. Since the name “chorion” is also correctly used for the secondary membrane secreted by the follicle cells, it is confusing to use this term for an embryonic membrane of different origin. We shall therefore always designate this embryonic membrane as serosa although it is quite customary among mammalian embryologists to use “chorion” in both senses. A

For an introduction to the nature of the embryonic membranes of the vertebrates and of the parts they play, the conditions as found in the chick may be taken as a type. Of course these conditions apply particularly to the Sauropsida; however, they may be looked upon as providing a point of departure for the entire study. They have often been described, so a brief reference here is all that is necessary. The first membrane to appear in the chick is the yolk sac. As the blastoderm grows over the yolk its lower edge consists after gastrulation of primary ectoderm. At an early stage the endoderm and later the mesoderm may be seen back of the edge gradually making their way over the yolk. The VERTEBRATES EXCEPT MAMMALS 231

mesoderm divides into two layers, and the investments of the yolk are first the splanchnopleure (endoderm and mesoderm), then the extra Fra 163 Diagrams of the extraemhryomc membranes of the chick (From Duv9.l’s Atlas)

A, 2-day embryo, B, 3-day embryo a , air space, of , ammotlc fold, a c , amniotic cavity, all , allantois, alb , albumen, e , embryo e e c , extruembryomc eoelome, ect , ectoderm, end , endoderm, In , mesoderm, ser. serosn; s , shell, sm . shell membrane, so. soma.topleure. sp , splanchnopleure, v , vltellmo membrane, y , yolk, y s . yolk sac

embryonic coelome, and last the somatopleure (mesoderm and ectoderm). The anterior and posterior parts of the gut are the first to develop 232 EGG AND EMBRYONIC MEMBRANES

a cellular floor. The midgut remains open to the yolk for some time. As the embryo becomes constricted off from the yolk the two ends of the gut enlarge further, and the extent of the opening of the midgut is decreased. finally, the latter is connected to the yolk only by a narrow

a1l.c.

flu 164 (‘ontmuation of fig 163 A, 5—day embryo, B, 14-day embryo

am , amnion, all e . allantoie cavity, all s , allantolc stalk, u , umbilical stalk neck called the yolk stalk. At the yolk stalk the inner and the extraembryonic splanchnopleure are continuous. The absorption of yolk material through the yolk stalk probably does not occur directly but is brought about by the vitelline circulation. Deep yolk sac septa which are folds of the splanchnopleure grow down into the yolk, and glandular VERTEBRATES EXCEPT MAMMAIS 233

absorbing cells aid in its digestion and in passing it to the vitelline circulation. The yolk mass decreases toward the end of the incubation period, and finally the entire structure is drawn into the body.

During the early growth of the blastoderm over the yolk the amnion and the serosa are being formed. The amnion arises by folds of the extraembryonic somatopleure near the anterior region of the embryo. first to form is the head fold of ectoderm and endoderm, for the mesoderm has not yet reached this region, and this is joined by lateral folds of somatopleure so that the entire region is covered. Later a similar tail fold covers that region and is continued forward until it meets the anterior lateral folds. The fusion of these folds encloses the embryo in an ectodermal cavity, the amniotic cavity. The union of its two folds has caused the somatopleure to double back on itself and thus to enclose the embryo in two membranes of similar nature although of inverted order. The inner membrane or amnion consists of ectoderm continuous with that ‘over the embryo and of somatic mesoderm. The outer membrane or serosa consists of somatic mesoderm and of ectoderm continuous with the outer covering of the yolk. Between the amnion and the serosa is the extraembryonic coelome which is connected with the body cavity of the embryo. The serosa is merely a continuation of the somatopleure which has made its way nearly around the yolk. It also covers the allantois which later develops within the extraembryonic coelome. Thus it comes to line the shell and covers the embryo and the other three membranes.

The allantois arises as a diverticulum from the hind gut within the body of the embryo. As development proceeds it extends out into the extraembryonic coelome, its connection with the gut being designated as the allantoic stalk. Since it arises from the gut, it has necessarily a lining of endoderm and an outer layer of mesoderm, that is, it is an extension of the splanchnopleure. It grows very rapidly and unites with the serosa so that there is now a double layer of mesoderm in its outer wall, splanchnic on the inside and somatic from the serosa on the outside, and over all is the ectoderm of the serosa. The rapid growth of the allantois carries it first over the amnion, with which it fuses, and then over the yolk sac. finally, pushing the serosa before it, it extends even over the albumen, which has become dense from loss of water, forming an albumen sac which is lined by the ectoderm of the serosa. The allantois has a rich blood supply in a network lying close to the porous shell, through which the exchange of gases is made easy. The chief function of the allantois is respiratory but it also serves as a receptacle for the excretory wastes from the kidney of the embryo. Shortly before the chick hatches, its beak breaks through into the air space of 234 EGG AND EMBRYONIC MEMBRANES

the egg, pulmonary respiration begins, and the circulation of the allantois becomes slower and slower, until at hatching time the dried allantois remains inside the shell.

With conditions as found in the chick as a starting point, the development of the various vertebrate membranes may be appropriately taken up.

The Yolk Sac

The yolk sac is the only accessory structure which may be looked upon as of general occurrence among the vertebrates. It will be recalled that all vertebrate eggs show a distinction between yolk pole and animal


fiG. 165. Embryo of toad fish showing large yolk sac attached.

pole. (See Chapters IV and V.) The eggs are markedly telolecithal whether the cleavage is holoblastic or meroblastic. The relation between discoidal and holoblastic eggs is discussed and illustrated earlier (fig. 51) where it is shown that the condition of the large yolk-laden endoderm cells of the bilateral type is gradually converted into the yolk mass of the discoidal type. The latter is incapable of segmentation, yet the homology between them is complete. The yo1k—laden endoderm cells which make up the ventral portion of the enteron and serve as a source of food supply for the growing embryo may be regarded as the antecedent of the yolk sac of the meroblastic vertebrates. They do not constitute a true yolk sac, but the mass of cells is the equivalent of an internal one and corresponds in a general way to the outer sac of fishes, reptiles, birds, and mammals. For all of these it is an important nutritive structure.

In myxinoids, elasmobranchs, and teleosts, in all of which the eggs are extremely telolccithal, a well-developed yolk sac is characteristic. THE AMNION 235

Before the blastoderm spreads over the yolk the embryo has formed and has become folded 0E. The yolk sac, therefore, is formed by the extraembryonic blastoderm which grows over the yolk and it is attached to the embryonic body by a stalk, narrow in elasmobranchs but wide in teleosts. The yolk sac has an area vasculosa that is rich in blood vessels by which the food material of the yolk is brought to the embryo.

Although it is an outgrowth of the gut the connection of the yolk sac with that structure may be interrupted early in development as is found among the teleosts (for example the salmonids), in which case the absorption of the yolk is brought about exclusively by the vitelline vessels. In addition to its nutritive function, the yolk sac often acts as a respiratory organ. It functions in this manner in the lower vertebrates whcre an exchange of gases takes place between the blood vessels of the yolk sac and the surrounding water and also in the early stages of higher vertebrates where the exchange takes place between its blood vessels and the medium surrounding the egg. Even in mammals the yolk sac may have a respiratory function. In the mono- ‘ tremes it still retains its yolk and hence its nutritive function. In the placental mammals, however, it is devoid of yolk but may still be functional in early stages when it is quite vascular and helps to absorb fiG 166 Embryo of Torpedo nourishment from the maternal tissues. §l;?,Y,‘“§sb?:“:f0r,;°:

Structurally the yolk sac is developed in from the posterior part of the about the same manner throughout the embm’ (After zlegler’) lower classes of vertebrates. A distinction is to be observed in the appearance of the mesoderm of the elasmobranchs, as Torpedo, and in teleosts, as the salmon. In the former the mesoderm is an undivided layer which grows out peripherally from the posterior portion of the embryo and then anteriorly about the edge of the blastodisc. In the latter case the mesoderm splits into somatic and splanchnic layers which grow laterally from the embryonic area and carry the body cavity as the extraembryonic coelome out over the yolk.

The Amnion

In the Sauropsida (reptiles and birds), we have the first appearance of the amnion, serosa, and allantois. This group and the mammals make up the Amniota, which possess the amnion and are contrasted with the Anamnia which lack it. Since most of these latter lay their eggs in a 236 EGG AND EMBRYONIC MEMBRANES

fluid medium, usually water, the developing embryos are not subjected to injury through violent motion or through changes in temperature or in humidity, and thus no special covering of the embryo is necessary. All the higher vertebrates either lay their eggs in a shell or hold them in the mother’s body during the embryonic period and some kind of protection is heeded to prevent the embryo from drying or from pressure or stress that might reach it. Therefore these embryos are protected by two membranes, the amnion and the serosa. When fully formed the amnion has always an inner layer of ectoderm and an outer layer of mesoderm.

Of the Amniota the reptiles are the most primitive. It is interesting to note that in them the amnion develops earlier than in the birds at a time before the head has become prominent and before the mesoderm


fiG 167 Diagrammatxe transverse section through a (‘helonian embryo (Cl€m"l1I8)(Redrawn from Kerr. based on a figure of Mitsukuri.)

has split into its two layers. In the Chelonia the amnion is at flrst formed of ectoderm and endoderm, the mid-dorsal part being of solid ectoderm. Later after the mesoderm has split it is drawn up into the amniotic folds and the endoderm takes no further part in the formation of the amnion. This is different from the condition in the chick in which the amnion is formed from the somatopleure except in the proamnion region where there is no mesoderm. (A proamnion region is characteristic of reptiles in general.) The broad ectodermal band in the roof of the amnion in the Chelonia has its counterpart in a small area known as the scro-amniotic isthmus in the amniotic roof of the chick. This latter may be considered as the remains of the broader layer of the reptiles. The amniotic fold in the Chelonia begins at the head end and proceeds backward until the whole embryo is covered. By the backward growth of this flap there is formed a long tunnel-like cavity covering the embryo and extending posterior to it. Later this posterior extension becomes partly obliterated and the cavity is closed. This again is quite THE AMN ION 237

different from the formation of the amnion in birds in which a head fold, lateral fold, and a tail fold take part. In some reptiles, however, as the chameleons, amnion formation is similar to that of birds, from lateral folds around the embryo, and is not due to the elongation of one an 5 fiG 168 A and B Chelonnn blastodorms showing stages in the formation of the amnion A, Cheli/dra, B, Clemmys (Redrawn from Kerr after Mitsukuri)

a . amnion showing neural groove beneath it, a f , edge of amniotic fold, a t . amniotic tunnel.

terior fold. Since the amnion appears earlier in the reptiles than in birds, and its cavity is formed before the embryo is marked off from the yolk, there is no need for the amniotic folds to grow upward as in the chick. The development of the amnion in the birds as a group offers nothing different in principle from the type already described, that is, from this conditions in the chick. The amnion of the mammals presents new features, however. Their character has already been discussed in the chapter on the formation of the mammalian embryo, Chapter X, to which the student is referred, and the chief facts regarding it are again mentioned a little later in this chapter under the head of the membranes of the mammalian embryo.

The Allantois

The allantois appears first in reptiles and is developed in all amniota. It always originates as an outgrowth of the hind gut and has therefore an endodermal lining and an outer layer of mesoderm. In amphibians it is represented by the urinary bladder. In reptiles the outgrowth has been described as solid, but it has also been maintained that the contracted space in which it develops causes it to be collapsed and so to take on the appearance of a solid structure. In birds it has a three-fold function. It increases in size, probably on account of the large amount of excretory Wastes collected during the embryonic life in the shell. Its large size and its position next to the air space in the end of the egg and just inside the shell are correlated with its new use as a respiratory organ. Also, pushing the serosa before it, it forms a double-layered sac over the albumen. This sac is thus lined with ectoderm. Since it absorbs the albumen, the allantois thus has a nutritive function, although of course this is of less importance than the similar function of the yolk sac.

The allantois of mammals acquires no further function. It aids the trophoblast in the formation of the placenta which is for the mammal an embryonic organ of nutrition, respiration, and the removal of excretion. It thus becomes the most important embryonic membrane of mammals, for through the participation of its blood vessels it has the chief part in the formation of the placenta.

Viviparity among the vertebrates is especially related to the functions of the allantois and the adaptations which it makes, but other embryonic membranes are also employed in bringing about this mode of caring for the embryo. Viviparity occurs in all the vertebrate groups, beginning with the fishes, except the ganoids, lung fishes, and birds. It is possible that it may have been characteristic of some fossil ganoids, but probably the birds because of their habit of flight have never been able to develop this method of caring for their young. There are many parallel methods of relating the embryo to the maternal tissues, and functional placentae are not confined to the mammals. In all forms below the mammals the embryo is chiefly nourished by the yolk sac even though other structural modifications supply additional sources of food. Development within the body of the mother always serves the same function, protection in THE ALLANTOIS 239

the struggle for existence. Among the elasmobranchs there are several genera in which there is intra—uterine development. In Acanthias the typical egg membranes are formed but the horny egg-shell is thin and disappears in later stages. The uterine wall contributes to the nourishment of the embryo by supplying the albuminous fluid which is enclosed in the egg-shell. In this form the lining of the uterus during later stages of development is thrown into folds which are brought into contact with the yolk sac. In Torpedo the folds are prolonged in trophonemata, nutritive threads which reach the pharynx of the embryo through its spiracles. In M ustelus laevis the folds of the uterus fit into grooves in


Fm. 169. Yolk sac placenta of Muslclus lacvis. (Rcdmwn from Corning after Joh. Muller.)

u., wall of uterus; y.o., yolk sue.

the yolk sac and, as both are highly vascular, they form a functional yolk sac placenta. A placenta used in this broad sense means any structure which brings about, by means of an abundant vascular supply, an intimate relation between maternal and embryonic tissue, for the purpose of conveying nourishment from the one to the other. Here the yolk sac functions in this manner, but in the Amniota it is usually the allantois.

The teleosts include a number of viviparous forms. In some the eggs are developed in the ovary itself where vascular processes on the surface contain the eggs and act as placentae. In others the embryos develop in the enlarged oviduct _or uterus. Sometimes (Scorpaenidae) the maternal body merely holds the embryo which obtains its food supply entirely 240 EGG AND EMBRYONIC MEMBRANES

from the yolk. In other cases (Anableps) the yolk sac sends out villi to the uterine wall.

Viviparity is uncommon among the amphibia. In one of the salamanders (Salamandra atra), however, development takes place in the oviduct but usually only one of the eggs reaches maturity for the others break up and are absorbed by the outer gills of the developing embryo. The embryo has additional nourishment from the blood which escapes from the uterine wall.


fiG 170 Embryo of (‘hulcides tndactylus (Redrawn from Kerr after Giaconiine)

A, 7-mm embryo, B, 15-16-mm embryo seen from apical pole all, allantois, pl, allantoic placenta (foetal portion) . y s , yolk sac

The reptiles include a number of viviparous forms. In some, the blind worm and the viper, there is a thin shell and the embryo is simply held in the uterus, the lining of which remains unchanged. In the lizard, Chalczdes ocellatus, the shell breaks and finally disappears, the uterine wall becomes vascularized, and 1S thrown into folds which fit other folds on the yolk sac. Both the allantois and the uterus adjoining it are highly vascularized but the placenta-like folds develop only on the yolk sac. A type of placenta more nearly approaching that of the mammals is found in still another lizard, Chalczdes trzdactylus. The condition of its allantois and yolk sac may be regarded as transitional from that typical of the Sauropsida to that of the mammals, for both function as placenta and projections from both vascularized sacs interlock with MAMMAIS 241

similar projections from the uterus. But of the two the allantoic placenta is the more highly developed. Thus the true allantoic placentae are not limited to the mammals but appear also among the reptiles.

Evidently the problem of relating the embryo to the maternal tissues has been solved in similar ways, although employing different structures in the different groups of the vertebrates. In the mammals the wall of the uterus is highly developed as a special adaptation of the maternal tissue to accomplish this function. In other forms the oviduct sometimes takes care of the need so far as the mother is concerned, and even the ovary may serve in this capacity. On the part of the embryo, the yolk sac of lower forms often carries on the function, while in the higher forms it is taken over by the allantois.

C. MAMMALS

Of the embryonic membranes of mammals the greatest interest is in connection with the allantois and the placenta which it helps to form. The yolk sac and amnion are also present, however, and show features which are new. In the entire early development of mammals there is a rather general lack of structural homology with that of other classes of vertebrates, and although similar results are reached convergently so far as the structure of the embryonic membranes is concerned, their methods of origin in some forms is very different.

There are two great types of development found in the mammals. The monotremes are unlike all the others in that their eggs are large and yolk-laden and their cleavage discoidal. The animals are oviparous, the development of the embryo taking place within the egg-shell, as in the case of the Sauropsida. Cleavage, germ-layer formation, and the development of the embryonic membranes is comparable to these processes in that group. The membranes are of the same kind and are probably formed in the same manner.

The marsupials are the lowest mammals which have intra—uterine development. The young are born in an immature condition, and are placed in the abdominal pouch where they become attached to the teats of the mammary glands, Here the immature period is completed. Since at birth the young are so miniature, the allantois, which in the higher vertebrates functions as a medium for obtaining nourishment from the uterus, is usually small. The yolk sac contains no yolk, though it is large and well developed. Its wall opposite the embryo contains only endoderm, and the extraembryonic coelome is absent in this part of the blastoderm. During uterine life there is usually a yolk sac placenta.

The marsupials include a number of forms which taken together make up a series similar to that described for the lower vertebrates and illus242 EGG AND EMBRYONIC MEMBRANES

trate the change from a yolk sac placenta to an allantoic placenta. The first of the series is the opossum, Didelphys, in which the yolk sac has 9, nutritive function. This membrane makes connection by means of folds




. on: 077777;!‘ 6


Fm. 171. A, diagram of a section through monotremo embryo; B. diagram of a. section through marsupial embryo. Ectodcrm, solid line; mesoderm, dotted line; endoderm, dashed line.

a., amnion; a.c., amniotic cavity; 3.11., allantois; e., embryo; e.e.c.. extraembryonic coelome; sen, serosa; y.s., yolk sac.

with the uterine wall. The latter secretes a nourishing fluid which is absorbed by the trophoblast and the endoderm of the yolk sac, and thus is transported to the embryo. In Dasyurus we have a further step THE YOLK SAC 243

in the series. The allantois is still small and the yolk sac large. The trophoblast forms a syncytium with pseudopodial processes which attack the uterine wall and engulf uterine blood vessels. The nourishment is passed on to the yolk sac which may be correctly called a yolk sac placenta, for the connection between the uterine wall and the yolk sac is very close. Parameles illustrates the last step in the series. In this form the yolk sac is large and probably has some function in absorbing nourishment. The allantois, however, grows larger, develops a richer blood supply, and reaches the trophoblast. The uterine wall, at the place where the trophoblast touches it, develops a syneytium and becomes vascular. The trophoblast disappears and the blood vessels of the allantois and the uterus come into close contact. There are no true villi as in the higher mammals. This is the first case we have met of a true allantoic placenta and the only one known for the marsupials. It differs from all others in that the syncytium is entirely of uterine origin and does not develop from the trophoblast as it does in those mammals having a discoidal, deciduate placenta.

The development of the eggs of the true placental mammals involves the formation of a blastocyst with differentiated trophoblast and inner cell mass as is described in Chapter X. The embryo resembles a hollow vesicle with a drop hanging from one spot on its inner surface. The inner cell mass is the formative or embryonic portion. The trophoblast is non-formative and produces only ectoderm of the serosa. After this stage the inner cell mass or embryonic knob differentiates into two portions, an upper eetodermal layer from which will be derived the ectoderm and amnion of the embryo and a lower endodermal layer from which will be derived the enteric canal, the yolk sac, and the allantois. The embryo proper at this stage is called the embryonic shield and consists of a layer of ectoderm covering a layer of endoderm. (See fig. 144.)

Jenkinson has offered an interesting suggestion about the significance of the early development of the mammal. He compares the blastocyst stage with the later stage of the reptile or bird in which the yolk sac has become completely covered and the serosa contains the embryo in the amnion with its yolk sac and allantois attached. In the mammals also there is a stage of a closed sac, the blastocyst, which contains in the inner cell mass all the material for the embryo and its membranes. J enkinson regards this as a precocious separation of the materials of the mammalian embryo due to the loss of the yolk on the part of the ovum.

The Yolk Sac

The yolk sac has the same layers as that of the lower forms, but in the placental mammals it arises in a different way and is functional 244 EGG AND EMBRYONIC MEMBRANES

only in early stages, if at all. The endodermal layer is formed from the innermost layer of the inner cell mass. These cells proliferate and spread around the inside of the trophoblast until they form a closed sac just as would have happened had a central yolk mass been present and they had grown around it. Sometimes the cavity is very small and the yolk sac correspondingly restricted, as in man, when it forms a very small vesicle owing to its slow growth. In other cases the endoderm is quite closely applied to the inner side of the trophoblast and a large yolk sac is thus formed. In no case, however, does it contain yolk. It is therefore an insignificant structure and the function which it serves in the lower


Fro. 172. Diagram of a. section of rodent embryo. p., placenta; other letters as in fig. 171.

forms is presently taken over by the allantois. The completion of the yolk sac comes only when in later stages the mesoderm is formed between the endoderm and the trophoblast.

The formation of the mesoderm begins in the embryonic area and some time elapses after its separation into its two layers before it grows out into the space between the endoderm and the trophoblast of the vesicle; but at length it pushes out from the embryonic area and grows between these two layers. An early split in this mesodermal layer completes the yolk sac which thus consists of endoderm and splanchnic mesoderm. The vitelline circulation develops to provide the usual vascular supply.

In many of the higher forms it is merely a vestige of the membrane through which the embryos of simpler forms obtain their food. In some cases, however, it retains something of its earlier function in that in THE YOLK SAC 245

early stages it absorbs nutrirnent from the uterus. In these cases it becomes a yolk sac placenta. When this occurs, as in the ungulates, camivores, and rodents, the yolk sac is large and its blood supply is rich and comparable to that of the chick. In marsupials, in which the uterine development is of short duration, the yolk sac placenta often functions until birth.

In rodents the yolk sac is always large and invagination of its upper wall by the embryo gives apparent inversion of the germ layers. This may take place early in development as in the mouse and guinea pig, or

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later as in the rabbit and squirrel. In some cases the lower wall of the yolk sac is never formed. In others it disappears along with the trophoblast, and the cavity of the yolk sac is in communication with the cavity of the uterus. The upper wall of the yolk sac absorbs the material secreted by the uterus and its supply of blood vessels carries this to the embryo. Thus the yolk sac acts as an accessory placenta.

In the rabbit the yolk sac, which contains a nourishing fluid, is very large and in early stages practically fills the blastodermic vesicle. A rich supply of blood vessels develops in the side of the yolk sac which is toward the embryo. The opposite side contains no mesoderm and fuses with the trophoblast. Later the yolk sac shrivels and since its outer wall is fused with the trophoblast it remains as a mushroom-shaped 246 EGG AND EMBRYONIC MEMBRANES

membrane. The two walls of the shrunken vesicle thus come close together and later they fuse. Since the inner wall of the yolk sac was highly vascularized its blood vessels continue to supply a large part of the blastoderm. The rest of the blastoderm is fed by blood vessels of the allantois which help form the placenta. The yolk sac of the rabbit is probably a more important nutritive organ than the allantois. The vitelline artery ends in the sinus terminalis and the blood is returned to the heart by the vitelline veins.

In the Insectivora the yolk sac is often large in early stages and its blood vessels may begin to form a yolk sac placenta as in Tupaija. In




'1 0 ', I 2 0"


,-0"0-o.....ooo° ,_-_-_;J

Fm. 174. Diagram of 11 section of embryo of insectivore. u., wall of uterus; other letters as in fig. 171.

some insectivores the mesoderm never covers the lower wall of the yolk sac (Sores: and Talpa). This organ is unimportant in later stages.

The yolk sac circulation in most mammals is of importance in early stages only, while the allantois is being formed. Later, when the allantois has established its relation to the uterine wall, there is a retrogression of the yolk sac. This is true of man, in which the yolk sac becomes a solid strand of cells extending; out into the body stalk or umbilical cord. In some forms, as the insectivores, the yolk sac remains until birth.

The Amnion

The formation of the amnion is due to the development of the upper portion of the inner cell mass. It is accomplished by one of the two THE PLACENTA 247

methods described in Chapter X. In the one case, there may be a fold or a series of folds of the extraembryonic somatopleure similar to those of the chick, as in most ungulates and some insectivores. In the other case, the cavity may arise in situ in the embryonic knob or between it and the trophoblast, and thus may never open into any other cavity, as in the mouse, guinea pig, bat, other insectivores, and many primates, including man.

The Allantois

The allantois arises as a diverticulum from the gut in the same manner as in the chick. In the rabbit this diverticulum extends out into the extraembryonic eoelome and soon comes into relation with the trophoblast. In many rodents, as the mouse and guinea pig, it is often small and its endoderm may not grow beyond the body of the embryo. In Tarsius and in man the vesicle never extends freely into the extraembryonic eoelome but is enclosed as a vestigial structure in the body stalk. This latter is an enlargement of the primitive connection between the embryo and the trophoblast, a connection which is never lost. It is regarded as the equivalent of the allantoic stalk of other forms.

The allantois of lower mammals assumes the function of nutrition but retains its cavity which may serve as a receptacle for urinary wastes. The size of the cavity is progressively reduced until in some forms it disappears completely with the inner endodermal layer and only its mesodermal portion remains. This part becomes highly vascularized and, together with the trophoblast, forms the embryonic part of the placenta, a structure which comes into relation with the circulatory system of the mother and so takes care of the functions of respiration, nutrition, and excretion. Thus the mesodermal portion of the allantois accomplishes the function which in lower forms the entire structure serves.

The Placenta

A placenta is any organ which brings about an intimate relation and vascular connection between maternal and foetal tissues. The formation of a yolk sac placenta has been described for some of the fishes and reptiles and is again found among the marsupial mammals. Among the higher mammals, however, it is always the allantois which brings about this relation between the embryo and the mother. In these forms, the actual contact is made by the trophoblast, as part or all of it comes into relation with the uterine walls. It is the allantoic vessels, however, which, through contact with the trophoblast, furnish the foetal part of the

placental circulation. _ The placenta is necessarily a compound structure. Its embryonic 248 EGG AND EMBRYONIC MEMBRANES

parts are trophoblast (sometimes lined with mesoderm) and the allantois with its blood vessels. Its maternal part is the vascular uterine wall. The foetal and maternal parts may be merely in apposition or they may be in such close relation that they are actually fused. In both cases an intimate physiological relation results. The blood vessels of the allantois (umbilical arteries and veins) are brought close to those of the uterus, making possible an exchange of substance by diffusion. The embryo is thus able to obtain oxygen and food materials and also to dispose of its waste products. There is never any direct connection between foetal and maternal blood vessels.

The placentae of mammals are of two general types, deciduate and non—deciduate. The non—deciduate placenta is sometimes called a semiplacenta. The name deciduate was given to indicate the loss, at birth, of the lining of the uterus. Although this loss is not significant in all socalled deciduate forms, the name has still been retained. The following brief classification of types of placentae of the Placentalia is partly based on the conception of Jenkinson. The types are closely related to the method of implantation of the ovum in the uterine wall. Of implantation there are three types, central, eccentric, and interstitial, as mentioned in Chapter X. Implantation is central if the embryo becomes attached superficially to the uterine wall; eccentric if it is enclosed by folds of the uterus; or it is interstitial if the embryo burrows down into the uterine wall. The classes of placentae are as follows:

The non—deciduate type is that in which the surface of the trophoblast develops villi which fit into crypts or depressions in the uterine wall. In the simplest cases, the uterine epithelium persists in these crypts and at birth the villi are drawn out without damage to the uterus. In other cases, the uterine epithelium is destroyed and there is a closer union between foetal and maternal tissues. This type of placenta is characteristic of the ungulates, but is also found in the Cetacea, Edentata, Sirenia, and Lemuroidea except Tarsius.

The second type is the deciduate in which the uterine epithelium is always destroyed by the trophoblast. Foetal and maternal blood are in close relation. There are two subdivisions of this type as follows:

(a) Zonary deciduate placenta. The maternal blood circulates in capillaries of the uterus. The placenta, which is zonary or band shaped, is composed of foetal and maternal tissue in very close relation. At birth part of the wall of the uterus is destroyed and there is a true decidua. This type of placenta is characteristic of the Carnivora. (b) Discoidal deciduate placenta. The trophoblast destroys not only the uterine epithelium but also the subepithelial tissue. The maternal blood circulates in lacunae or spaces in the trophoblastic wall. These spaces NON-DECIDUATE PLACENTA 249

represent maternal blood vessels which have been engulfed by the trophoblast and they are the chief part of the placenta contributed by uterus. Blood is the principal maternal tissue lost at birth, and the deciduae are thin and more or less degenerate. The portion of the trophoblast which is involved in the placenta is disc-shaped. Placentae of this type are found among rodents, insectivores, bats, in Tarsius, monkeys, and man. These three types of placentae require a more detailed description.

Non—decz'duate Placenta. The non—deciduate placenta may be illustrated by that of the ungulates. In these forms the allantois enlarges rapidly and occupies the length of the trophoblast. The surface of the trophoblast forms villi into which extend the mesoderm and blood vessels of the allantois. These may be single or branched. They may be scattered over the surface of the trophoblast (diffuse placenta, as pig);


Fm. 175. Diagram of embryo of ungulate contained in uterus. Wall of semen has been cut, showing embryo in section. c.. cotyledon; ed., edge of cut in serosa.

they may be situated in groups or cotyledons (cotyledonary placenta) when they are also branched (ruminants), or there may be a combination of the two types, both cotyledons and simple villi being interspersed (intermediate placenta). Also the cotyledons may be grouped in a band around the trophoblast.

The trophoblastic villi fit into crypts or corresponding depressions in the uterine wall. When the villi are in groups or cotyledons, the corresponding groups of crypts on the maternal side are called maternal cotyledons. These latter are in some cases stalked and the foetal cotyledons are then concave.

In the difiuse placenta, the uterine epithelium persists as the lining of the crypts and at birth the villi are withdrawn with no injury to the uterus. In the cotyledonous placenta the uterine epithelium, except that of the glands, degenerates and there is a much closer union of maternal and foetal tissues. Consequently the two portions of a placenta of this type separate with some difficulty.

In the diffuse placenta the uterine and trophoblastic epithelia are in contact, but in the cotylcdonary placenta the contact of the tropho250 EGG AND EMBRYONIC MEMBRANES

blastic epithelium is with a highly modified and vascular subepithelial connective tissue. In the latter case, however, there is no true fusion of foetal and maternal tissue as is true of the deciduate placentae. The maternal connective tissue and trophoblastic villi are both rich in capillaries. Nourishment is obtained by the trophoblast in two Ways. Both the villi and the trophoblastic cells at their base absorb nourishment (“uterine milk”) from the maternal tissues, and extravasted blood and

u 9 a

QC 5:".

F10. 176. Cross sections of placentae. A, pig; B, cow; C, out. (Modified from Grosser.)

d.. degenerating uterine epithelium; 0., embryonic capillary; m., maternal capillary; mes., mesoderm of serosa; s., epithelium of serosa; u., uterine epithelium; v., villus.

cell débris from the crypt walls are ingested by pseudopodia from the cells of the trophoblast. Absorption and respiration also are brought about by diffusion between the maternal and foetal capillaries. The blood in these vessels is separated by very thin layers of tissue only. The placental layer consists, on the foetal side, of the capillary walls, connective tissue, and trophoblast, and on the maternal side of connective tissue, eapillary walls and, in the diffuse placentae, of uterine epithelium also. Thus diffusion between foetal and maternal blood vessels is easily carried on. DECIDUATE PLACENTA 251

In the allantoic fluid of ungulates are found bodies of queer shapes called hippomanes. These are formed as accumulations of coagulable material from the uterine milk and become saturated with calcium oxalate crystals. They push, pocket-like, into the trophoblastic wall between the cotyledons and later are pinched off into the cavity of the allantois, surrounded by trophoblast and allantoic wall.

Fm. 177. Embryo of sheep enclosed in embryonic membranes and showing cotyledonous placenta characteristic of many ungulates. (Redrawn from Corning after 0. Schultze.)

a., amnion; c., cotyledon; e., atrophied end of blastodermie vesicle; u., umbilical cord.

Deciduate Placenta. In deciduate placentae the union of maternal and foetal tissues is closer than in placentae of the non-deciduate type. In deciduate placentae, part or all of the trophoblast, called the trophoderm, becomes specialized and, by the aid of enzymes, erodes the uterine wall. At birth the lining of the uterus is removed as part of the placenta. In the zonary deciduate type, this lining or decidua is in close union with the foetal blood vessels, so that maternal and foetal tissues are removed together. In the discoidal deciduate type, however, the 252 EGG AND EMBRYONIC MEMBRANES

maternal blood, which circulates in spaces in the trophoblast, is the chief tissue lost from the uterus, for the deciduae are thin and degenerate.

The placenta of the zonary deciduate type occurs only in the Carnivora. This placenta may in some respects be considered as intermediate between the naon-deciduate and the discoidal deciduate types. In the Carnivora, the trophoblast destroys the uterine epithelium (but not the subepithelium) and eats its way into the wall of the uterus. Here trophoblastic villi invade the connective tissue of the uterus and come in contact with the maternal capillaries which are much richer than in the nondeciduate placenta. Foetal capillaries grow into the villi and foetal and maternal blood are thus brought close together. This placenta is therefore formed by fusion of foetal and maternal tissues. The trophoblast, connective tissue, and the capillaries of the allantois contribute the embryonic part, and the capillaries and connective tissue of the uterus contribute the maternal part. The maternal blood is separated from the foetal blood only by these structures. The placenta is at first thin, but becomes thicker owing to the elongation and branching of the villi and the growth of the connective tissue. When birth takes place the blood vessels and connective tissue of the uterus are removed along with the foetal vessels and the connective tissue. It is possible that this placenta may have originated from the non-deciduate type by a closer association of the maternal and

pm 173_ Embm, 0f dog foetal tissues after the erosion of the uterine

showing band-shaped placenta wall_ 11 te ' t' fth ' . . . . ((:R:iui*(:a.wrtisfil'(dxl)1 Co:§ill.:.1)vorcs The placenta of the dzscozdal deczduate type

differs from the carnivorous placenta in that the cavities in which the maternal blood circulates are not maternal

capillaries but broad laeunar spaces which have formed in the walls of the trophoblast itself. The tissue of the placenta is almost entirely of foetal origin. The placenta of the mouse may be taken as typical of this type. In this form the trophoblast erodes the uterine epithelium and attaches itself to the subepithelial tissues of the uterus. It then develops lacunar spaces in its wall. Later after the allantois has developed and has reached the somatopleure its capillaries DECIDUATE PLACENTA 253

grow in between the lacunae of the trophoblast. Further growth of the placenta is brought about by the thickening of this wall. Maternal blood from ruptured vessels of the eroded uterine wall circulates in the lacunae. The maternal and foetal blood, however, are separated from each other only by the walls of the trophoblastic lacunae, a small amount of connective tissue, and the walls of the capillaries themselves. As these lacunae are in such close relation to the allantoic capillaries, diffusion is easily possible between them. The placenta of the mouse is typical of the deciduate placentae of the discoidal type. Since maternal blood


fiG. 179. Diz1.gr:un of embryo of carnivore enclosed in uterus. Band—shuped placenta IS represented as if transparent, showing embryo in section below. Letters as in fig. 171.

circulates in lacunar spaces in the trophoblast one can readily understand why the uterus loses only blood and a slight amount of connective tissue at birth.

The discoidal deciduate placenta of the Anthropoidea is similar to that of the rodents.

When a human trophoblast reaches the uterus it bores its way into the wall and implantation is thus interstitial. The trophoblast becomes differentiated into two layers, plasmotrophoblast, which is a plasmodial covering without cell walls but containing many nuclei, and an inner cytotrophoblast or layer of Langhans, which consists of distinct cubical cells. The plasrnotrophoblast at its place of attachment to the uterus erodes the uterine epithelium and dissolves the wall. The outer trophoblast has a spongy character and the spaces become filled with maternal 254 EGG AND EMBRYONIC MEMBRANES

blood from the eroded uterine wall. Later the spongy network is transformed into villi which are surrounded by the trophoblastic spaces that now have the character of lacunae. These villi are at first solid, with the syncytial layer on the outside and cells within except in late stages when the cellular layer disappears. Some of the villi branch freely into the lacunar spaces, but others anchor the trophoblast to the uterine wall. The lacunae are lined everywhere, even on the maternal side, by a syncytial layer. Later the mesoderm of the serosa wanders into the villi which are now branched and which become vascularized by the allantoie blood vessels. These so—called villi are very different from the


Fro. 180. Diagram of human embryo 1n utero. d.r., decidua reflcxa; c.u., cavity of uterus, um., umbilical cord.

villi of ungulates, which are projections from the wall of the trophoblast. They are not villi at all in this sense but are more like the foetal capillaries of rodents which are covered by the trophoblast into which they have pushed. They are merely the irregular walls of the lacunae of the trophoblast.

The villi are at first over the whole surface of the trophoblast (diffuse placenta), but later, those nearest to the cavity of the uterus degenerate so that here the surface is smooth. The villi of the other side remain giving rise to a diseoidal-shaped placenta.

The uterine covering over the trophoblast is known as the decidua reflexa or decidua capsularis. The part of the uterus where the embryo is attached is known as the decidua basalis or serotina, and the opposite wall the decidua Vera. In man the decidua capsularis comes in contact with the decidua vera in the fifth month and the uterine cavity is obliterated. Later the capsularis becomes non-vascular and gradually DECIDUATE PLACENTA 255

disappears so that the trophoblast is in contact with the decidua Vera. This in turn, becomes degenerate, as only the inner portion of the uterine lining remains. The decidua basalis, on the other hand, takes an important part in the formation of the placenta. The uterine capillaries increase and maternal blood from this region supplies the placenta. In late stages, the basalis is reduced to a very thin membrane.

When birth takes place the amnion is ruptured, the amniotic fluid escapes and contractions of the uterus expel the embryo, the break taking place across the degenerate deciduae. Later, there is discharged an afterbirth, which consists of the placenta with the thin layer of decidua basalis and the attached membrane composed of fused amnion, serosa, and deciduae capsularis and vera. It is thus evident that the


fiG. 181. e.h., capillary of the decidua basalis; e.v., capillary of a villus; i, inter-villous cavity

filled with maternal blood; L., Langhan's cells (cytotrophoblast); m., mesoderm of the serosa; s., syncitial layer (plasmotrophoblast); v.f.. fixation or anchoring villus.

only maternal tissue which is lost is uterine blood and a small amount of connective tissue representing the thin layer of the degenerate lining of the uterus. The largest part of the placenta is of foetal origin, but maternal blood accompanies it.

In some of the monkeys, the placenta is double. There is, of course, only one umbilical cord, but the two placentae are connected by blood vessels. In the orang and gibbon there is a single placenta. The lower monkeys have no decidua reflexa.

The following outline lists the characteristics of the embryonic membranes and placentae in the different orders of mammals. In many cases the embryology of only a few forms has been investigated. It is probable that further investigation may show that some animals do not follow in all respects the usual types found in their orders. Indeed, it may be found that some show quite aberrant types, as is true of the lemur, Tarsius. EMBRYONIC MEMBRANES OF MAMMALS


Monotremata

Marsupialia

Artiodactyla

Yon: SAC

Like bird, contains yolk on left side of embryo

Large well-developed, but

contains no yolk No extraembryonic coelome in blastoderm opposite embryo During uterine life there is yolk sac placenta with exception of Pera— melee

Small functional only in

early stages, when it is vascular

Aiimion

Has sero—amniotic connection and is probably formed :13 in Sauropeida

Probably formed by folds

Inner cell mass moves upward pushing trophoblast away The folds from edge of embryonic shield form amnion

Penssiodactyla

Cetacea

Sirenia

Proboscidea

As in artiodactyls

As in artiodact) ls

Large amnion of Orca obIiteratc-s exttaembry onic cavity

Amnion obliterates extra embryonic coelome in Elephas

ALLANTOIB

Well-developed. on right side of embryo

Small, since young are born immature

Large, occupying most of uterus Goat embryo 2 inches long has allantoia 2 feet long Hippomanea in allantoic fluid

As in artiodactyls

In Halicore is large. as in 8|’tl0d8.Cl.\lS Hippomanea in allantoic fluid

PLACENTA

None

Found only in Peramelas Trophoblaat not involved in its production, uterine wall develops vascular ayncytium

Rnimnxs

Oviparoifa egga with hard shell Young fed milky secretion from primitive abdominal mammary glands

Series of forms through Dtdelphys. Dan/uriia, and Perameles showing transfer of placental function from yolk sac and allantoia

.\on—deciduate Most ruminants cotyledonary Pig diffuse unbranched villi Deer hippopotamus earrel, girafle intermediate

l\on-deciduate placenta Hfirse branched difiused V] l

l\on-deciduate placenta With diffuse, branched villi

‘Ion-deciduate W itli branched difiuae villi arranged in band around tropboblast (Really zonary non-deciduate )

fuse villi \ot classified yet as to deciduate or nondeciduate but villi seem to be like those of articdactyls

Central implantation

Membranes incompletely described

Zonary placenta Vlltll dif Embryology not Sufi ciently investigated

256

EGG AND EMBRYONIC MEMBRANES‘ Carnivora

Edentata

Rodentia

Chiroptera

Insectivora

Primates Lemuroidea

Anthropoidea

Large yolk sac probably functional in early stages

Disappears

Large Invagination of upper wall gives apparent inversion of germ layers

Lpper wall acts as accessory placenta That of rabbits is more important nutn tive organ than allant ois

Functional onl stage Repla tois

in early by allian Large Yolk sac placenta formed in Tupaija Mesoderm restricted to upper wall in Talpa and Sore: Persists until birth

Rabbit amniotic posterior

Formed from series of folds

Large amniotic cavity oblitcrating extraembryonic coelomc

folds formed after embryonic shield has taken superficial place on blastoderm \/louse, rat giunea pig closed sac inside inner cell mass

Vespertillw confluence of irregular spaces in embryonic knob forms amnion

Extremely large Grown between 5 olk sac and trophoblast completely lining serosa

Small

Often small and endoderm does not grow out beyond body as in mouse and giinea pig

Replaces yolk sac

Hedgehog forms a closed Groves out prominently cavity in embryonic knob dwarfing yolk sac

Talpa Sore: Tupaua formed by folds

Small yolk sac early disappears (Tarnus small vascular)

Small yolk sac with cavity and vascular in early stages

Tarsms formed by folds

Amniotic cavity formed in inner cell mass

Very large fills extraembryonic space Tarsms small outgrowth of gut remains in base of umbilical cord

Small contained in stalk of umbilical cord


Zonary deciduate

May be zonary oval bellshaped or difluse Marius non-decidiiate with simple diffuse villi Tatusm modfied discoidal deciduate

Discoidal deciduate

Discoidaldeciduate saucer

shaped or bell shaped

Discoidal deciduate usuallv concave In hedgehog is decidua reflexa like that of man but formed differently In mole acontradeciduate condition (allantoic capillaries separated at birth from placental trophoblast which is absorbed by uterine walls)

Non-deciduate diffuse (Tarsius discoidal deciduate)

Deciduate. discoidal

Central implantation

Little known about mem branes of edentates Central implantation in Ta!usm

Implantation is central in rabbit eccentric in mouse. interstitial in guinea pig and gopher

Implantation eccentric (in some forms)


Implantation central

Implantation interstitial


MEMBRANES OF MAMMALS 257 258

APPENDIX TO PART ONE

THE FMBRYOLOGICAL CONDITIONS OF ANIMALS FOUND IN THE VARIOUS PHYLA ‘


Germ 1' or- Types of ma— Cleavage

Typra of Blaatulae

Mesoderm

Ty pea of Formation

Gaatrulation

i

«Xe =Occutrence in the Phylum

X =0ccurrence in Smaller Divisions of Phyla

Larval Forms

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Porifera . . . . . . . . . . . . ‘%

Coelenterata . . . . . . . :2 age Ctenophora‘ . . . . X Hydrozoa . . . . . . . X X SC)’ hozoa . . . . . .. X Ant ozoa . . . . . . . . . . X 3X

Platyhelminthes . . . . . .

, Amphiblastula and Parent.-hymula — — — - -

améx as X Hé xx |# X x1 as x H6 x><>< He >< Hex

afiéjé xx _T Hex

awe 1 He X aiéx

awe ><><>< He x x__

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. -— * lak fie s ' I l\Iu1ler 5, Sporocyst, l\I1nc1d:um, Cysticel- ‘ cug. Pilzajum, Redia. Cercaria. Larva of Depot

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T1-ochelminthes . . . Rotifera. . . . . . .

Molluscoidea . . . . . . . . Phoronida , . . . . Brachiopoda . . . . Bryozoa.

X X X X

aaex 3:e>< x x if->_<3%>< ate

Supposed to be nrochophore

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1* "»'e" I 1% Dgrect development X ‘ X I Dlrc-ct development

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Uphxupluteus, Bipinnaria, Echmopluwua. Aunculana

2

Annelida. . . . . . . . . . . . %% Polychaeta . . . . . . . . X Oligochaeta . . . . . . . .

Echinodermata..... 9%! i

Asteroidea . . . . . . . Echinoidea . . . . . . Ophiuroidea. . . _ Holothuroidea . . . . . .

Mollusca . . . . . . . . . . . Amphineura. . . . Pelecypoda . . . . . . Gaateropoda . . . Cephalopoda . . . . . . .

Arthxopoda . . . . . . . . . .

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Nauplxus, .\Iet.anaup1xu5. Zoaea, Megalapa. and others

9% ae 1%

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Cruatacea_ . . . . . . . . . Bx-anchnopoda. . . . Ostracoda . . . Copepoda . . . . . . Eucopepoda. . . . . Cimpedia . . . . Amphipodn. . . . Schizopoda .. Decapoda . . . . . .

Myriapoda. .

Insecta . . . . . . . . . . Coleoptcra . . .

Arachmda . . . .. Ax-aneida . Scorpionida. . . .

Chordata . . . . . . . . . . fié Enteropncusta Tumcata . . . Cephalochordata X Vercebrata .. .....

Cyclostomata Petromyzontm Myxinoidea .

Elaamobranchii. . .

Ganoidea. . . .. .

Teleoatei . . . . . .

Amphibia . . . . . .

Reptilia . . . . . .

Aves . . .

Mammalia . . X X

XX X

x# X xxxxxx xxxxx x

Larva. pupa, and others

xxxxxxx x x x x

xxxx xxx % xxxxxxxxxxxxxxx x x


tr”

X Tomnria. Tadpole and others

  1. xx fixxxxxxxxxx
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X. 260

APPENDIX TO PART ONE

TABLE OF ANIMAL CLASSIfiCATION INCLUDING EXAMPLES OF

EMBRYOLOGICAL SIGNIfiCANCE

(None: This table does not include the forms listed in certain chapters in Part Two, in which the systematic position is given in the text.)

Phylum Porif’era

Class 1. Calcarea Order 1. Homocoela. Leucosolenia Order 2. Heterocoela, Grantia, Sycandra Class 2. Hexactinellida Euplectella

Class 3. Demospongia

Order 1. Tetraxonida Geodia, Cliona

Order 2. Monaxonida Spongella

Order 3. Keratosa Euspongia

Phylum Coelenterata

Type 1. Cnidaris. Class 1. Hydrozoa

Order 1. Anthomedusae (Tubularia) Hydra, Hydractimea, Pennaria, Bougainvillia, Clava, Clavellina, Turritopsis, Eudendrium, Tubularia, Margelis, Nemopsis, Sarsia, Podocoryne, Protohydra, M icrohydra, Pol:/podium

Order 2. Leptomedusae Obelia, Campanularia, Plumularia, Sertularia, Clytia, Cory/morpha M onocaudis, Gcmothyrca, Tima, Aequoria

Order 3. Trachymedusae Campanella, Geryonia, Trachynema, Persa, Liriope, Aeginopsis, Gombmmus, Haleremita

Order 4. Narcomedusae Cunina, Cunocantha, Aegina

Order 5. Hydrocorallinae M illepora, Stylaster

Order 6. Siphonophors. Physophom, Nanomia, Diphyes, Physalia, Porpita, Velella, Halistemma

Class 2. Scyphozoa.

Order 1. Stauromedusae Tessara, Lucemaria

Order 2. Peromedusae Pericolpa, Periphylla ANIMAL CLASSIfiCATION 261

Order 3. Cubomedusae Charybdea

Order 4. Discomcdusae Aurelia, Pelagia, Cassiopea, Cg/anea, Ulmaria, Stomolophus, Polyclonia

Class 3. Anthozoa (Actinozoa) Subclass 1. Alcyoniaria

Order 1. Stolonifera (Tubiporidae) Tubipom

Order 2. Alcyonacea Alcyonium

Order 3. Gorgonacea Corallium

Order 4. Pennatulacea Pennalula, Ifenilla

Subclass 2. Zoantharia (Hexacoralla)

Order 1. Edwardsiidae

' Edwardsia

Order 2. Actinaria Metridium, Halcampa, Paranemonia, Bunodes, Sagartia, Tealia, Bicidium, Epizoanthus

Order 3. Madreporaria Sclerophylla, Oculi/La, Aslrangirc, Aslrca, Faira, Fungia, Madrepora, Porites, Astroides, Mcandrina

Order 4. Antipatharia Antipathes, Gerardia

Order 5. Zoanthidea

Order 6. Cerianthidea Cerirmlhus

Type 2. Ctenophora Class 1. Tenmculata Cullianira, Plcurobrachia, IIrmm'phora, Mnemiopsis, Bolina, Cestus Class 2. Nuda Bertie, I dyia Phylum Platyhelminthes Subphylum 1. Platoda Class 1. Turbellaria Order 1. Rhabdocoelida M icrostoma, Vortex, M onosceles, M onops, Stenostoma

Order 2. Tricladida Poly/scelis, Planaria, Dendrocoelzmz, Bipalizzm, I2’(.’elloum, Gunda, Poly chaerus, Syncoelidium, Phagocata Order 3. Polycladida Leptoplana, Stylochus, Thysanozoon, Discocoelis, Planocera, Yungia Class 2. Trematoda. Order 1. Monogenea (Polystomea, Heterocotylea) 262 APPENDIX TO PART ONE

Polystomum, Sphyranura, Epibdella, Gyrodactylus, Diplozoon, Tristoma, Microcotyle Order 2. Digenea (Distomeae)

Distomum (Fasciolaria), Monostomum, Bilharzia, Clonorchis, Paragonimus

Class 3. Cestoda. Caryophyllaeus, Archigetes, Ligula, Tetrarhynchus, Echinobothrium, Acanthobothrium, Bothriocephalus, Taenia, Anoplocephala, M oniezia, Dipylidium

Subphylum 2. Nemertinea Class 1. Nemertea Order 1. Protonemertini Carmella Order 2. Mesonemertini Cephalathrix Order 3. Metanemertini Geomzmertes, Tetmstemma, Amphiporus, Malacobdella, Nectonemertes Order 4. Heteronemertini (Schizonemcrtini) Lineus, M icrura, Cerebratulus, Zygeupolia Phylum Nemathelminthes

Class 1. Nematoda Ascaris, Ancylostoma, Trichinella, filaria

Class 2. Gordiacea Gordius

Class 3. Acanthoccphala Echinorhync/zus

Phylum Trochelminthes

Class 1. Rotifera

Philodina, H ydatina Phylum Molluseoidea Subphylum 1. Podaxonia

Class 1. Phoronida Phoronis, Echiurus, Bonellia

Class 2. Gephyrea Sipunculus

Subphylum 2. Polyzoa

Class 1. Entoprocta. Urnatella, Pedicellina, Loxosoma

Class 2. Ectoprocta

Order 1. Gymnolaemata Gemmellaria, Bugula, flustra, flustrella, Eschara, Crisia, Tubulipora, Alcyanidium, Valkeria, Paludicella Order 2. Phylactolaemata. Plumatella, Pectinatella, Cristatella Subphylum 3. Brachiopoda

Terebratula, Terebratulina, Lingula, Waldheimia, Rhynchonella ANIMAL CLASSIfiCATION 263

Supplementary group of uncertain position, showing some relations to Entero pneusta:

Pterobranchia Cephalodiscus, Rhabdopleura Phylum Chaetognatha Sagitta, Spadella Phylum Annelida Class 1. Archiannelida Polygordius Class 2. Chaetopoda Subclass 1. Polychaeta Order 1. Phanerocephala Nereis, Podarke, Aphrodite, Lepidonotus, Autolytus, Polymie, Diopatra, N othria, Eunice, Syllis, Trypanosyllis Order 2. Cryptocephala Eupomatus, Hydroides, Spiroides, Arenicola, Amphitrite, Terebella, Sqbella Subclass 2. Oligochaeta Order 1. Microdrili (Limicola) Tulnfex, Dcro, Nais, Sparganophilus, Lumbriculus, Ctenodrilus, Branchiobdclla Order 2. Macrodrili (Terricola) Lumbricus, Allolobophora, Diplocardia Class 3. Hirudinea Order 1. Gnathobdellidae Ilirudo, Jllacrobdella Order 2. Rhynchobdollidae Clepsine, Pontobdella, Piscicola Phylum Echinodcrmata Class 1. Asteroidea Asterias, Asterina, Astropecten, Heliaster, Pythonaster, Asteriscus, Culcita, H ippasteria, Ctenodiscus Class 2. Ophiuroidea. Ophiura, Ophiothrzlt, Ophiopholis, Amphiura, Astrophyton Class 3. Echinoidea Cidaris, Arbacia, Toxapneustes, Strcmgylocentrotus, Coelopleurus, Spawngus, Echinocardium, Brissus, Echinarachnius, Clypeasler, M ellita Class 4. Holothuroidea Holothuria, Cucumaria, Psolus, Thyone, Caudina, M olpadia, Synapta Class 5. Crinoidea Rhizocrinws, Pentacrinus, Comatula, Antedon Phylum Mollusca Class 1. Amphineura Order 1. Placophora (Chitonida) A Amicula, Trachydermon, Chiton, I schnochiton, Cryptochiton 264 APPENDIX TO PART ONE

Order 2. Aplacophora (Solonogastres) Proneomenia, Conchoderma, C/Laetoderma, Dondersia Class 2. Scaphopoda Dentalium Class 3. Pelecypoda (Lamellibranchiata, Acephala)

Order 1. Protobranchia N ucula, Leda, Yoldia, Solenomya

Order 2. filibranchia Arca, M ytilus, M odiola, Anemia, Trigonia

Order 3. Pseudolamellibranchia Pecten, Ostrea, M eleagrina, Lima, Pinna

Order 4. Eulamellibranchia Anodonta, Unio, Pisidium, Cg/clas, Cardium, Astarte, Mg/a, Pholas, Teredo, Aspergillum, Venus, M actra, Tellina, Salem, Dreissensia

Order 5. Septibranchia. Silenia, Cuspidaria, Poromya

Class 4. Gasteropoda. Order 1. Prosobranchia. Suborder 1. Aspidobranchia Acmaea, Palella, Haliotis, Margarita, Trochus Suborder 2. Pectinibranchia

Littorina, Strombus, Sycotypus, Busycon (Fulgur), Crepidula, Urosalpinx, Murex, Paludina, Carinaria, Pleurobranchidimn

Order 2. Opisthobranchia

Suborder 1. Tectibranchia Bulla, Philine, Aplysia, Haminea, Umbrella Suborder 2. Pteropoda Cymbiliopsis, H yalaea, Clione Suborder 3. N udibranchia

Doris, Asolidia, fiona, Staurodoris

Order 3. Pulmonata Helix, Bulimus, Limax, Lymnaea, Physa, Planorbis

Class 5. Cephalopoda

Order 1. Tetrabranchia Nautilus

Order 2. Dibranchia

Suborder 1. Decapodn. Spimla, Ommastrephes, Architeuthis, Loligo, Sepia Suborder 2. Octopoda. Octopus, Allopasus Phylum Arthropoda Class 1. Crustacea.

Subclass 1. Entomostraca

Order 1. Phyllopoda Suborder 1. Branchiopoda Branchipus, Artemia, Apus ANIMAL CLASSIfiCATION 265

Suborder 2. Cladocera

Daphnia, Simocephalus, Leptodora, Polyplwmus

Order 2. Ostracoda Cypris

Order 3. Copepoda.

Suborder 1. Eucopepoda. Cyclops, Lemaea Suborder 2. Branchiura.

Argulus

Order 4. Cirrepedia

Suborder 1. Eucirripedia Balanus, Lepas Suborder 2. Rhizocephala. Sacculina Subclass 2. Malacostraca Superorder 1. Leptostraca

Order 1. Phyllocarida

Nebalia Superorder 2. Arthrostraca

Order 1. Amphipoda Gammarus, Caprella

Order 2. Isopoda Asellus, Porcellio

Superorder 3. Thoracostraca

Order 1. Cumacea. Diastylis

Order 2. Stomatopoda. Squilla

Order 3. Schizopoda. M ysis

Order 4. Decapoda

Suborder 1. Macrura Palaemonetes, Crangon, Penaeus, Lucifer, Astacus, Homarus Suborder 2. Brachyura Dromia, Cancer Class 2. Onychophora. Peripatus Class 3. Myriapodu

Order 1. Pauropoda. Pauropus

Order 2. Diplopoda. J ulus

Order 3. Chilopoda. Lithobius, Scutigera, Scolopendra

Order 4. Symphyla Scutigerella 266 APPENDIX TO PART ONE

Class 4. Insecta. Macrotoma, 9. thysanuran; Hydrophilus, the water beetle; M iastor, the fly; Leptinotarsa, the potato beetle; Copidosoma, parasitic hvmenoptera Class 5. Arachnida Order 1. Araneida , Epeira

Order 2. Scorpionidea Buthus, Euscorpius

Order 3. Phalangidea Phalangium

Order 4. Acarina Lepas, Izodes

Order 5. Pedipalpi Tarantula

Order 6. Palpigradi Kaenenia

Order 7. Solpugida Eremobates

Order 8. Pseudoscorpionida Chelifer

Order 9. Xiphosura Limulus

Order 10. Eurypterida Eurypterus

Supplementary Arachnid groups of doubtful relationship Pantapocla, Tardigradn, Pentastomidea (Linguatulina) Phylum Chordata Subphylum 1. Enteropneusta Balanoglossus, Dol2'choglossu.s, Ilarrimania Subphylum 2. Tunicata Cynthia, (Hana, Molgula, Appcndicularia, Distaplia, Botryllus, Salpa, Pyrosoma, Doliolum Subphylum 3. Cephalochordata Amphioxus, Branchiostoma Subphylum 4. Vertebrate. Series 1. Anamnia Class 1. Cyclostomata Order 1. Myxinoidea M yzine, Bdellostoma Order 2. Petromyzontia Petromyzon, Lampetra Class 2. Pisces Subclass 1. Elasmobranchii Superorder 1. Selachii Squalus, M ustelus, Galeus, Raia, Acanthias, Scyllium, Carcharias, Cestracion, H exanchus, N otodanus, Pristiurus, Torpedo ANIMAL CLASSIfiCATION 267

Superordcr 2. Holocephali

Chimaera Subclass 2. Ganoidea Amia, Acipemer, Lepisosteus (Lepidosteus) Subclass 3. Teleostei Serranus, Ctenolabrus, Bclonc, Salmo, Fundulus, Perca Subclass 4. Dipnoi Cemtodus, I’rotopterus, Lcpidosiren, Class 3. Amphibia. Subclass 1. Stegooephalia Subclass 2. Lissamphibia

Order 1. Apoda ((iym11ophiona.) Dermo]2Izis, Coocilia

Order 2. Urodela

Fam. 1. Proteidae N ecturus, Proteus, Typhlomolge Farm. 2. Sironidac Siren, Pseudobmnchus Farm. 3. Amphiumidac Amphiuma, Cryptobranchus Farm. 4. Salmnandridac

Ambystoma (Amblystoma, Siredon), Diemyctylus, Salamandra, Triton, Plcthmlon, Eurycea (Hpelerpes), Desmognathus

Order 3. Anura Bufo, Rana, Pseudacris (Chorophilus), Ilyla, Pipa, Alytes

Series 2. Amniota Division 1. Sauropsida. Class 4. Reptilia

Order 1. Rhynchocephalia. Sphcnodon

Order 2. Squamata.

Suborder 1. Sauria (Lacertilia) Gecko, Draco, Anolis, Lacerta, Varamts, Iguana Suborder 2. Serpontis (Ophidia)

Python, Boa, T/zamnophis, H ydroplzis, Elaps, Vipera

Order 3. Loricata (Crocodilia) Alligator, Crocodilus, Gavialis

Order 4. Testudinata (Chelnnizi) Testudo, Cizrysemys, Clemmys, Chelone

Class 5. Birds Division 2. Mammalia Subclass 1. Prototheria.

Order 1. Monotremata.

Echidna, Ornithorhynchus Subclass 2. Eutheria Division 1. Didelphia. 268 APPENDIX TO PART ONE

Order 1. Marsupialia Didelphys, Perameles, Dasyurus, M acropus, Phascolomys, Phascolarctus Division 2. Monodelphia (Placentalia) Section A. Unguiculata (Clawed Mammals) ' Order 1. Insectivora Sorex, Talpa, Erinaceus, Tupaija Order 2. Dermoptera Galeopithecus Order 3. Chiroptera Vespertilio, Pteropus, Desmodus, M yotis Order 4. Carnivore. Suborder 1. fissipedia. Canis, Hyaemz, Procyon, Felis Suborder 2. Pinnipedia. Odobalnus Order 5. Rodentis. Lepus, Sciurus, Mus, Camla Order 6. Edentata, Bradypus, Dasypus, Tatusia Order 7. Pholidota. (Lepidota) Manis Order 8. Tubulidentata Org/cteropus Section B. Primates Order 9. Primates Suborder 1. Lemuroidea Lemur, Tarsius Suborder 2. Anthropoidea. Cebus, Ateles, Simia, Gorilla, Cynocephalus, Homo Section C. Ungulata (Hoofed Mammals) Order 10. Artiodactyla Bos, Camelus, Sus, Dicotyles, Hippopotamus, Corvus Order 11. Perissodactyla Equus, Tapirus, Rhinoceros Order 12. Proboscidea. Elephas, Loxodonta Order 13. Sirenia M anatus, Halicore Order 14. Hyracoidra. Procavia (Hyrax) Section D. Cetacea Order 15. Odontoceti Dolphin, Delphinus, Phocaena, Grampus Order 16. Mystacoceti Balaena

Part Two Embryological Problems

CHAPTER I THE ORIGIN AND DEVELOPMENT OF GERM CELLS

A problem of very considerable embryologieal interest is that of the origin and subsequent history of the germ cells. This is a matter of great theoretical interest because of its bearing on the Weismannian doctrine of the continuity of the germ plasm, and one which has been the cause of much controversy, at least as regards certain of its aspects. There are really three important phases of the problem; the place of origin of the germ cells, the path of their migration to the definitive gonads, and the subsequent history after reaching the germ glands.

A. VERTEBRATES

In Vertebrates the gonads arise from the genital ridges which develop on the dorsal side of the body cavity between the mesentery and the beginning kidney. This ridge is covered by the epithelium of the coelome or peritoneum, which is known as “germinal epithelium.” From the differentiation of this germinal epithelium in the four-day chick embryo Waldeyer (1870) first described the beginning of the sex cells or germ cells. Waldeyer’s view was accepted by the workers of his time as an adequate explanation of the origin of the germ cells and has been given as the only explanation in all of the text-books until quite recently. It is, moreover, supported by the observations of a school of investigators

of the present day. It is, of course, true that with the formation of the '

gonad the germ cells are to be found in that organ and they appear to have arisen from its epithelial covering.

In 1880 Nussbaum, as a result of his observations on the development of the trout and the frog, reached the conclusion that the germ cells were of blastomeric origin, being segregated in the early stages of deVelopment in a region outside that which will see the formation of the embryonic body. They actively migrate or else are carried into the body proper and into the germ gland by the growth forces which operate to give the organism its body form. Since Nussbaum’s time the evidence has steadily accumulated that in many vertebrates, as in well-known cases among the invertebrates, the germ cells are early set apart from the somatic cells and develop independently from them. Their history may be traced backward from their appearance in the germ gland to

211 272 THE ORIGIN AND DEVELOPMENT OF GERM CELLS

very early stages and the path of their migration clearly made out in many cases. Many careful investigations (Hoffmann, 1892; Eigenmann, 1892; Beard, 1900; Woods, 1902; Allen, 1906, 1907, 1911; Dodds, 1910; Swift, 1914, 1915, 1916; Jordan, 1917; Okkelberg, 1921; Richards and Thompson, 1921; Swingle, 1926; Hahn, 1927) have failed to reveal any conditions not in accord with Nussbaum’s theory. It has been demonstrated that the primordial germ cells arise widely scattered in the


In. 125.2 Tr.ms\ erse section through .1 4 mm land of the bowhn Anna uzlza (After Allen )

Gut end . gut cudodorm roof end , roof endoderm, penph end, peripheral ondodcrm, Wolff cl . Wolfhan duct, s c . sex cells, lat mes , lateral mesoderm

endodeun or in the-splanchnic mesoblast in the extraembryonic area. From this point of origin they pass with progressive development to the region of the body axis. This movement has been accounted for in three ways; it is usually thought that the cells actively migrate in an amoeboid manner, passing up the mesentery and into the region of the gonad. Swift found that the primordial germ cells of the chick are carried in the blood stream, and in Fundulus it has been shown that the forces which are responsible for the formation of the embryo body carry the germ cells to their place. The movement of the cells of the germ ring by confluence and the other normal processes which lead to VERTEBRATES 273

the formation of the axial region of the body brings about the translocation of the germ cells as well as the somatic cells. Along the path of migration there is no difficulty in recognizing the germ cells for they have clearly marked characteristics. On these points there is rather general agreement.

The subsequent history of these cells appears to be an uncertain prob1em———one much involved at the present time in controversy. Some investigators claim that some of these. cells never find their way into the gonad, but undergo degeneration in various parts of the body. Some (firket, von Berenberg—Gossler, Ilargitt, and others) claim also that the primordial cells which may have arrived in the gonad by


flu. 183. 'l‘rans\'(-rse section through the hind gut of l).l—mm. larva of Amid crzlva. (After Allen.)

coel., coelomie cavity; gut end., gut endodorm; mes., mesentery; s.e., sex cells; Wolfi’.d.. Wolffian duct.

migration in the manner indicated _do not actually give rise to the definitive germ cells, for they find degeneration of these cells along with proliferation of a second group of germ cells derived directly from the genital epithelium. These latter, or even in certain cases a third proliferation, are the source of the definitive germ cells. The primordial germ cells in these cases may pass far through their cycle before degenerating, as shown by Kingery for the mouse and Swinglc for the tadpole, in both of which the maturation cycle is practically completed before the degeneration occurs.

In a recent account Swingle has reviewed the progress of the investigations on the Anura, He has shown from embryological studies that there are in various parts of the United States “local races which differ 274 THE ORIGIN AND DEVELOPMENT OF GERM CELLS

markedly in regard to the time of occurrence and character of the developmental processes involved in the formation of the definitive testes.” He is convinced that the sex cells appear first in the endoderm, and give origin to those cells which produce ripe sex products. Every stage from the origin of the primordial sex cells to the fully developed spermatozoa has now been traced in the bull frog, and no doubt now remains as to the continuity of the germ line in this form. On the other hand Hargitt and others have claimed that the germ cells arise in urocleles from differentiated mesoderm, the peritoneum. Swingle sug— gests that the discrepancy is due to an origin and segregation earlier than their appearance in the peritoneum, and that after their segregation they wait in the layer where they are later seen for an appropriate time for development. This is in agreement with his finding that local races differ in the time of development of the sex cells. In the urodeles they are incorporated in the mesoderm in an early stage whereas in the Anura they are in the endoderm, but it is not necessary to assume their origin in either layer because of the fact that later they appear in the one or the other.

It is to be noted that none of the writers who find degeneration have satisfactorily proven that all the primordial germ cells degenerate or that none of them are left to produce definitive germ cells. It is also noteworthy that recently certain evidence has been found which indicates that in an ordinary course of events the definitive germ cells are derived from the primordial cells. However, owing to the power of regulation which animals possess under the stress of unusual and harmful circumstances which bring about the degeneration of the primordial cells, secondary sex cells may be proliferated from the germinal epithelium and produce the definite sperms or ova. At the present time the safest interpretation seems to be that as a rule the primordial germ cells thus early segregated in the vertebrates give rise to the definitive germ cells, but that in exceptional cases, where the regular events are interrupted and the primordial cells so disturbed as to cause their degeneration, the organism responds by proliferating from the germinal epithelium new cells which take their place. It must never be forgotten that the chief characteristic of protoplasm, especially embryonic protoplasm, is its plasticity, its power of regulation and of adaptation to new conditions. “Life is a constant adjustment of internal and external conditions.”

Although the matter is still involved in controversy, some important theoretical conclusions have already resulted from the investigations. first of all, it is an obvious fact of major importance that heredity is a matter of germ cells, and that the germ cells contain organized material THE INVERTEBRATES 275

through which the continuity from generation to generation is carried on. The germ cell mechanism is the mechanism of inheritance. Not only is there continuity of germ cells but of the organized system (germ plasm) which they convey. Secondly, the distinction between germ cells and somatic cells is often more or less artificial and has in many cases been emphasized unduly. Weismann himself spoke with less certainty about the continuity of germ plasm than many of his followers have done, although he without doubt was expressing a fundamental truth. Yet there still remained a theoretical question which his formulation of his doctrine did not fully state, namely, the possibility of the soma contributing to or becoming part of the germ plasm. Various views on this point have already been given.

It is the author’s opinion that with the possible exception of the mammals no group has as yet presented evidence of positive character that contradicts the view that germ cells as well as germinal material are distinct from the somatic from a very early period. In the mammals the situation is 11ot yet clear. It is worthy of note that the cases in which uncertainty or confusion exists are exactly those which have proven least satisfactory for cytological and accurate embryological studies. When favorable material is available there is general conformity to the expectations of those who would emphasize the importance of the germ plasm. These include cases of determinative cleavage where the germ—cell cycle has been followed in case after case, and also those which have yielded clear figures for chromosome studies.

If in addition the recent view be accepted that the chromatin of all cells represents the germ plasm and the cytoplasm the soma, as is now held by numbers of students, the history of the germ cells becomes a study of the specialization of chromatin and nuclei and that of the soma one of cytoplasmic specialization. The general problem of the germ-cell cycle is thus given its proper place as one of embryology, where it is of great interest, and it is no longer one of theoretical significance to geneticists.

B. THE INVERTEBRATES

In the invertebrates there are many forms in which no suchMuncertainty prevails as in the case of the vertebrates. There are two chief methods by which germ path is recognizable: 1.e., chromatin diminution and germ-cell determinants. There are of course many cases in which nothing is known of the development of the germ cells, but there are in several groups of the invertebrates cases in which the germ path (Keimbahn) has been-worked out in practical completeness. In the coelenterates primordial germ cells were found by Weismann, Kleinen276 THE ORIGIN AND DEVELOPMENT OF GERM CELLS

berg, and others in a wandering condition early in the development of hydroids. The details of Weismann’s observations have been disputed by Hargitt, but his main contention is borne out that the germ cells are recognizable long before the sexual individuals appear. The case

fiG. 184. The dexelopment of the germ cells of Sagilta. (After Elpatiewsky.)

A, fertilized egg showimz the “germ cell determinant,” B, 2-cell stage, germ cell determinant in one blastomere only; (‘, H—cell stage; D, szastrula with two primordial germ cells. '

t 2., germ cell determinant; p.b.. polar bodies; p.g.c.. primm'diul germ cells.

which has been of greatest interest from the standpoint of the history of the germ cells is that of Ascaris megalocephala as brilliantly worked out in great detail by Boveri. In Ascaris (see Chapter IV, Section 3) the first cleavage division results in two blastomeres, one of which is purely a somatic cell while the other is a stem cell. The history of each 'rm«: INVERTEBRATES 277

fiG 185 Early stages In the development of Cyclops fuscus (After Amma)

A, first cleavage nucleus, 13, (laughter nuelex reconstructed with the ectosomes or germ cell determrnants 1n one blastomere only, 0, second elenvage dnmon wrth the germ cell determmants agmn l1m1ted to one blmtomere, D, l()-cell stage All the blustomeres m the

restmg condltmn except the stem cell, E, gastrula In whlch two pnmordral germ cells are to be dlstmgulshed from the endoderm cells. 278 THE ORIGIN AND DEVELOPMENT OF GERM CELLS

of these cells has been fully described by Boveri. They are distinguishable by means of a process known as chromatin diminution, part of the chromatin (the thick ends of the chromosomes) of the somatic cell being cast from the nucleus into the cytoplasm, because of which process the

1

fiG. 186 A, longitudinal section through an oocyte of M iastor americami. (After Hegncr )

n c , nurse chamber, g v . germinal vesicle, p Pl , pole plusm, f ep , follicular epithelium B, later stage of same in which somatic cells are beginning to form and blastoderm and the two pl'll‘flB.!’y germ cells containing the pole plasm are already cut of?

somatic nuclei in subsequent cell generations are both lighter in color and smaller than the germ cells. All the chromatin of the stem cell is retained in this second division, but of the daughter blastomeres produced from it, one undergoes the diminution process while the other divides directly in the regular manner and becomes again a stem cell. Of the products of its division the same relation holds, for the process THE INVERTEBRATES 279

is repeated four times. Thus, at the end of the fourth cleavage there are fifteen somatic cells (which will give rise only to somatic cells ordinarily) and one cell which is the primoridal germ cell and the ancestor of all the germ cells. At the next division this divides again

Fm. 187. Continuation of fig. 186. A, similar stage of eight germ cells, blastoderm complete; B, sagittal section through embryo with eight germ cells near the end of the tail fold.

and the two cells thus produced give rise later on in the interior of the embryo to all its sex cells.

In Sagitta, Elpatiewsky recognized in the fertilized egg a structure, called a “germ-cell determinant,” which does not divide with the egg. (fig. 184.) The blastomere containing it becomes a stem cell. In the fifth division the stem cell produces a somatic cell and a primordial germ cell. 280 THE ORIGIN AND DEVELOPMENT OF GERM CELLS

In an early gastrula four cells have resulted from two divisions of the primordial cell. The subsequent divisions of the four are responsible for the formation of both male and female germ cells (for the animal is hermaphroditic). It is said that the two anterior give rise to the ovary and the two posterior to the testes.

Among the arthropods there are many cases of the early segregation of germ cells, and their recognition is possible either through cytoplasinic inclusions (germ-cell determinants) or by distinctive characteristics, particularly chromatin diminution. In the Entomostraea are two outstanding cases, M oina (Grobben) and Cyclops (Haecker, Amma). Here the stem cells are distinguished from the first cleavage onwards. In the unsegmented egg of (71/claps (fig. 185) certain granules (ectosomes) are to be found accumulating at one pole of the spindle as the cleavage mitosis advances. These granules are thus segregated into one of the blastomeres which becomes the stem cell. This process continues through the fourth division and results in the segregation of the primordial germ cells.

In the insects a germ path is recognizable in several orders. In the Diptera (Mzestor, Kahle, 1908, Hegner, 1914, Chironomus, Hasper, 1911, and in other cases) the germ cells appear at the

Fm. 188.

Longitudinal section through ovarian egg of ( hpixlosoma. almost ready to be laid. (After Hegner.)

The germ cell determinant (k) lies near the posterior end of the egg.


posterior end of the egg as pole cells and can be traced into the larval gonads. Here polar granules, germ-cell determinants, or pole plasm, as the mass is variously called, are present in the uncleaved egg and enter the pole cells. In addition to this in M iastor (figs. 186, 187) the pole cells are provided with two nuelei from the third cleavage which have not undergone chromatin diminution as distinguished from the other six. In the Hymenoptera. (fig. 188) an “oosome” is present in

fiG. 189. Longitudinal section through the egg of Leptinotarsa drmlvnlirieata. (After Hegner.) The'posterior end was killed with :1. hot needle just after the egg was laid. The egg was then allowed to develop for 24 hours. bl., blastoderm; g.c.d., germ cell determinants; k.. portion of the egg killed. THE INVERTEBRATES 281

the unscgmented egg which in the 4—eell stage becomes associated at the posterior end with the forming primordial germ cells. finally, in the chrysomelid beetles (fig. 189), Hegner found a “polar disc” composed of germ-cell determinants which participate in the formation of the primordial germ cells. This relationship was made more certain by an experiment which he performed. With a hot needle he killed the posterior end of the egg, l)ut allowed the remainder of the egg to develop. A blastoderm was formed which was normal in every particular (up to a certain stage) except that it was entirely lacking in germ cells.

These cases prove conclusively that among many invertebrates we may regard the early segregation of the germ cells as satisfactorily established. In addition to these there are many cases of cell lineage in which there is no question but that the germ cells arise from blastomeres segregated at a quite early stage. It is to be noted also that these cases are among the best known of all animals, the material being abundant and most favorable for the study of entire life cycles. CHAPTER II

GERM-LAYER THEORY

It will be recalled that the old issue between preformation and epigenesis finally resulted in the overthrow of the cruder type of preforn1ation which held that development was simply an unfolding of parts already existing in egg or sperm. As better understanding of the facts of development was obtained it became clear that, although preformation did not occur, there were definite signs of organization within the egg. The developing organs could be traced farther and farther back until it was evident that in general they came from what might be called three plates or layers of tissue lying one over the other. These layers give rise by various processes of folding, outpocketing, unequal growth, etc., to the fundaments of the future organs. It was further obvious that there is a great similarity in regard to this method of origins from these layers in different kinds of embryos. These facts were known in whole or in part to many of the early embryologists, including von Baer (1828), and others, even back to the time of Wolff (1768). ()f course the proper interpretation of cells and cell structure in the animal kingdom had not as yet been made and it had proven impossible to explain the origin of the layers in terms of any other lower units of organization. It is not surprising, therefore, that these early embryologists should have looked upon the formation and subsequent development of the germ layers as the most critical processes of embryonic life.

The germ-layer theory, which is distinctly an attack on the problem of the organization of the embryo, has been one of the most fruitful of all biological speculations. After the true nature of cells and their methods of reproduction and growth came to be understood, the theory acquired new significance and, in the hands of Oscar and Richard Hertwig, had attained the status of a full-fledged theory of development by the early eighties. Through a great variety of forms, blastulae and gastrulae were identified, their methods of origin understood, and the remarkably uniform character of all the processes involved in germlayer formation and in the laying down of the fundaments of the organs was made out. Exceptions occur; indeed, some of them are of great importance, but considered as a whole there is striking uniformity in

282 GERM-LAYER THEORY 283

the relationships of the layers to each other and to the subsequently developing organs.

The essential point of the theory is that the three layers are homologous throughout the animal kingdom above the Porifera. In the coelenterates, as in the gastrulae, there are present only ectoderm and endoderm. Since the layers are homologous, the organs which arise from them are also homologous wherever they are found.

In all metazoa there normally develops following the blastula, a stage called the gastrula, of which the two component layers are known as primary germ layers, the outer being the primary ectoderm (epiblast, ectoblast), and the inner the primary endoderm (hypoblast or endoblast). The primary ectoderm in etenophores, turbellarians, rotifers, annelids, and molluses contributes with the primary endoderm to the formation of the middle germ layer, the mesoderm (mesoblast) giving rise to the distinction of ectomesodcrm and cndomesoderm respectively. From the outer layer also come: (a) the covering tissues with all their modifications and appendages including hair, horns, nails, scales, skin, glands, (b) the nervous system and sensory epithelium, and (c) in many cases the stomodaeum and proctodacum (extreme anterior and posterior regions of the alimentary canal).

The primary endoderm, in addition to cndomesoderm, produces the lining of the midgut and of all the organs which are derived from it, as pancreas, liver, etc. There is also exceptionally endoderm participation, for example, in the formation of a part of the nervous system in some coclentrates, but in some other cases, as in formation of blood cells and endothelium of blood vessels, the evidence is not yet clear as to whether it takes part.

The mesoderm may come, as already indicated, from the two primary germ layers, but except as mentioned above, only the endoderm seems to be involved in its production. There are several methods of mesoderm formation. Isolated endoderm cells may push into a space between the two layers at the same time with the secretion of a jelly-like substance, thus giving rise to a filling-in layer known as mesenchyme from which certain organs or parts of organs take their origin. In a second method the typical epithelial character of the primary germ layers is preserved and by outfoldings from the walls of the archenteron (primitive gut), which becomes entirely disconnected from it, lateral coelomic pouches are formed. This type of mesoderm is known as mesothelium. There are also other processes by which coelomic walls may in special cases be produced. The inner or splanchnic wall of the coelomic pouch unites with the endoderm to form the splanchnopleure, and the outer or somatic layer forms with the ectoderm the somatopleure. In some 284 GERM-LAYER THEORY

animals the middle germ layer is entirely mesenchymous; in others, entirely mesothelial; and in many, both types are present. Either one may develop first; in the echinoderms the mesenchyme arises before the mesothelium and in the vertebrates after it. The mesoderm gives rise to muscles, blood, skeletal and connective tissues, the excretory organs (at least in part) and usually to the sexual organs, but not the sex cells.

The surprising uniformity with which these relationships are held throughout the higher groups of animals has been responsible for the great importance of the germ-layer theory as outlined by the Hertwigs. Probably no other theory or working hypothesis, with the exception of Darwin’s own contributions, has been so fruitful as a stimulus for constructive zoological work. The germ-layer theory has to its credit much of the most important embryological accomplishment. As a working hypothesis it is of the greatest importance.

As an analysis of the problem of organization of the embryo, less can be said for the germ-layer theory. Researches of later years with careful technique have shown that the exceptions which formerly were overlooked are in many cases difficult to harmonize with the theory and, indeed, often operate decidedly to limit its usefulness.

Among the objections that have been cited are the following: inverse relationships of the layers found in the sponges; the fact that the outer layers of the (-estodes are in part or in toto thrown off leaving the covering tissues doubtfully related to the eetoderm; the varying derivation (depending upon the viewpoint of the observer) of the notochor(l and mesenchymous connective cells in different chordate groups; the composite nature of some organs, for example the nephridia, from more than one germ layer; the identification of the mesoderm as the 4d cell, not a layer at all, in the individuals with spiral cleavage; and especially the facts of budding, differentiation, and regeneration. Some of these objections have proven difficult to answer although this fact should not make us underestimate the value of this conception as a whole. However, it is now known that there are many evidences of organization appearing long before germ layers are formed. The promorphology of the ovum in the eggs with determinative cleavage and the possibility of tracing out the cell lineage during cleavage and organ formation in embryos of this class distinctly minimize the importance of the germ layers. Back of this the organization of the chromosomes and their part in shaping development as is now known from studies of cytology and genetics again detract from the value of the theory.

We have now come to view the germ layers as representing a stage in development just as we regard the blastula or gastrula as progressive GERM-LAYER THEORY 285

steps. It is an essential stage in most cases through which the course of development must pass, but in special cases adaptive modifications have arisen. Homologies exist between blastomeres—sometimes, as in the 4d cell and the “cross” of the annelids and molluscs, of very striking character; they also exist between germ layers, between organs and between organ systems. All are important, perhaps equally so. But the germ layers are probably best regarded as temporary embryonic organs which play their part and give rise to subsequent stages of development rather than as units of organization which determine the future course of development. CHAPTER III THE RECAPITULATION THEORY

The corner-stone of the science of embryology as it developed during the last half of the nineteenth century was the recapitulation doctrine. This doctrine is also called the biogenetic law, or in Haeckel’s term, the fundamental law of biogenesis. To it was due much laborious and painstaking research, and the interpretations based upon it have had far-reaching significance. Yet during the last decade critical studies have dethroned this doctrine so that as a “law” it is now of value only historically. As a tendency, however, recapitulation is still a useful conception for it unquestionably expresses a partial truth, a fact to which is due the long-continued interest in the doctrine and the stimulating effect it has had upon embryological studies.

Recapltulation refers to the parallel which exists between the history of the race, in its largest sense, and the development which an individual organism belonging to that race goes through. “Ontogeny rccapitulates phylogeny.” The life cycle of an individual is a brief summary of racial history. The animal kingdom presents innumerable instances which illustrate this principle. The development of the frog tadpole, through stages showing successively external gills, hind legs, front legs appearing later, and the disappearing tail and gills, closely parallels the taxonomic series of legless apoda and the salamanders. This series begins with the lower urodeles which have external gills and weak legs, then comes Amphzuma with small posterior legs, the Salamandridae in which external gills are lost, the legs are about equally developed, and the tail is about equal to the body in length, and finally the Anura which have no gills or tail and the hind legs are the better developed. (fig. 190.)

The development of the decapod Crustacea, in which the larvae pass through stages comparable to those characteristic of some other orders of the Malacostraca (fig. 191), is an often-cited case to illustrate the biogenetic law. Another illustration involves the ascidians (fig. 192) which superficially resemble shapeless jelly-like masses, and whose relationships are therefore difficult to decipher. A study of their embryology revealed the fact that they pass through a tadpole stage with dorsal nerve chord, notochord, etc., all recognizable as vertebrate char acters, but when they settle down and become sessile these structures 286 THE RECAPITULATION THEORY 287

gradually undergo degeneration and the creature loses all recognizable signs of its former organization. An analogous situation obtains in the

d 8 fiG. 190. Early stages in the development of a frog tadpole compared with adults of Siren (e), Amphiuma. (f), Desmoonathus (0), and an adult frog (h).

Cirripedia or barnacles. Barnacles have heavy shells, are sessile, and in general are quite unlike the ordinary Crustacea to which their developZ66 'l‘l'1l!2 RECAPITULAT ION THEORY

inent clearly shows them to be allied. A second suborder of the Cirripedia doubtless presents the most extreme case of modification to be found in the animal kingdom. This is Rhizocephala to which the parasitic Sacculina belongs. (fig. 193.) During its larval stages Sacculina is a free-swimming form having about the usual external features of a young braiichiopod crustacean. It attaches itself to the abdomen of a crab, sends root-like branches into the body by means of which it obtains nourishment, and completes its development to the adult stage. The

F1G- 191 -\. \ young lobster at the time of the third molt (after Herrick), and Ii. An adult A1’,[”37-'3 (after Verrill).

(~x., exopodite, en., endopodite.

adult is so degenerate that it has no crustacean characteristics but is merely a tumor-like sac on the abdomen of the crab in which even the usual internal organs are scarcely present, the body being chiefly filled with the gonads and their products. Only its life cycle reveals its relation to the other Cirripedia. The anatomical relationships by means of which its phylogenetic position is determined are made clear by a study of its cmbryological development.

Vaguely foreshadowed by the writings of Meckel and others of the period, the recapitulation principle is first directly hinted at in the writings of von Baer. Indeed, by some von Baer’s laws have been conTHE RECAPITULATION THEORY 289

fused with the recapitulation theory. These laws are, however, Inore properly regarded as alternative to certain phases of recapitulation. They were formulated by Von Baer in 1828 as follows:

“1. The more general features of a large division of animals arise in the embryo earlier than the special features.

“2. From the most general features of structure arise those that are less general, and so on until the most specific features arise.

“3. The embryo of a definite species tends away from the specific forms of other species, instead of passing through them.


In. 19.2 An adult mcidmn (\) ((}Illl)LlrUd \\lli| 1 lirxal {min of the same type (B) ( Uter Deluge and Huounrd )

“4. Fundamentally, therefore, the embryo of any higher species is never like the lower species, but only its e1nbryo”—(Lillie).

It will be noted that these laws antedate the cell doctrine and the publication of the “()rigin of Species,” and that the simultaneously enunciated germ-layer theory represented the last word in emhryological knowledge of the time in the matter of early structural organization. The advances made possible by the cell doctrine resulted in the enunciation by Fritz Muller in 1863 of the recapitulation doctrine as such. Haeckel developed the theory and applied it in his famous blasteagastrea hypothesis.

Haeckel’s hypothesis lays stress on the importance of the universal occurrence in the embryology of animals of the single-celled egg, the 290 THE RECAPITULATION THEORY

blastula, and the gastrula, and supposes that the phylogenetic development has taken a similar course. The protozoa represent the first step and are comparable to the egg stage in individual development. No animal is known which exactly corresponds to the blastula or the gastrula, although there are protozoan colonies quite like the former in some respects and simple eoelenterates have features in common with the latter. Haeckel, therefore, supposed that there must have been stages corresponding to each of these forms which had now ceased to exist,

and to these hypothetical forms he gave the names “Blasted” and “Gastrea.”


Fm. 193. A nauphus (A) and u (‘ypris larva (B) compared with an adult ((‘) Saeculma carcmt. (After Deluge.)

Haeckel also pointed out the significance of certain characters as indicating phylogenetic history whereas others are to be regarded as embryological adaptations of importance to the individual organism, but not to the race. Characters of the first class are spoken of as palingenetic; of the second, as cenogenetic. A chick embryo, for instance, has a good many characters which recall fish or amphibian conditions, but it could not exist in the environment where these forms dwell, and is different in numbers of other characteristics including the important one that it will develop not into a fish or amphibian, but a bird. It cannot, therefore, in its development represent with entire correctness the ancestral forms. Some of its characters are those which adapt it to development in a shell at a temperature of 37° C. and enable it to live in the peculiarities of its own environment. These are new or ceno— genetic characters. Other features, as the aortic arches, gill slits, brain THE RECAPITULATION THEORY 291

vesicles, and others, are supposed to be of ancestral significance and are, therefore, palingenetic.

A critical consideration of many cases which may be cited, however, shows that the facts do not all easily fit into the biogenetic interpretation. When one attempts to classify clear cases such as the shell tooth on the one hand or the aortic arches on the other as adaptive or ancestral little difliculty is experienced, but the problem of applying the same classification to a doubtful ease becomes much more complex, and as a rule the results cannot be certainly relied upon. Indeed, recognition of a particular character as palingenetic or cenogenetic may be quite an impossible task.

Other difficulties may be cited which require modification of the strict biogenetic way of looking at the animal kingdom. For example, there is a general tendency which becomes more marked the higher one goes in the animal kingdom to shorten and condense the ancestral phases of an organism’s development in favor of the specializations which relate it to its own environment. This tendency, in addition to complete changes of developmental conditions (for example, the long placental life of mammals, or the abundance of yolk in bird eggs), may result in the entire omission of certain stages (as in the case of embryos where gills do not develop in connection with gill arches).

This abbreviation or contraction of development is called by some writers tachygenesis. In the brief period of embryonic development, if reeapitulation occurs even in the most sketchy fashion, an immense contraction of stages must be thought to take place so that the necessary abbreviation may be accomplished. To this shortening of the developmental time, or tachygenesis, there are two aspects, the actual quickening of the rate of development and the fusion and omission of certain stages. The one aspect may occur without the other in special cases as in the response of the developmental rate to rise in temperature, where the rate is hastened without fusion or omission of stages.

Hcterochrony also presents an argument against the reeapitulation doctrine, as was pointed out by Keibel, Mehnert, and others. By heterochrony is meant the disturbances, which now are known to be of quite common occurrence, in the time of appearance of structures in a known sequence of stages.

These modifications in the rates of development bring about results which cannot be interpreted either as of phyletic or adaptive significance. Stockard has lately pointed out the importance of the arrest of development, even over a small part of the germ ring, whereby various types of monsters are produced. Evidently, here are structural modifications not to be related to recapitulation. Furthermore, the normal develop292 THE RECAPITULATION THEORY

ment of the organ systems of the embryos of different classes does not preserve the same synchrony as may be noted by comparing tables of the development, let us say, of the chick and pig (Keibel, N ormentafeln). In addition, there are extreme cases in which the actual order of development is the reverse of what would be demanded by recapitulation, as, for example, in those cases in which the joints become rounded off before movement is acquired. Another illustration is the formation of the tongue and the teeth. There is no question that in the phylogenetic series teeth made their appearance before tongues, but in the embryological development of mammals the teeth are much later developed than the tongue. Ontogeny not only fails to recapitulate phylogeny in this case, but completely misrepresents the facts.

In a recent discussion De Beer has summarized the possibilities of variation which heterochrony offers in comparing the appearance of structures in the individual with that in the ancestral forms. This summary with no further elaboration is sufficient to make clear that some of the possible variations not only do not fit in with the conception of recapitulation but are actually opposed to it. The summary is as follows 2*

“A character which is present or makes its appearance in the young stage of an ancestral animal may in the ontogeny of a descendant

appear:

“A. In the young stage only, producing youthful adaptations or caenogenesis,T not affecting phylogeny.

“B. In the young and adult stage, producing a substitution of the new adult condition for the old, resulting in a progressive denation in the ontogeny of the descendant from that of the ancestor.

“C. In the adult, by a relative retardation of the development of the bodily structures as compared with the reproductive organs, resulting in paedogenesis and neoteny.

“A character which is present in the young and adult stage of an ancestral animal may in the ontogeny of a descendant appear:

“D. In the young stage only, resulting in the reduction of the character to a vestige.

“A character which is present or makes its appearance in the adult stage of an ancestor may in the ontogeny of a descendant appear:

“E. In the adult stage, resulting in those differences which distinguish individuals, varieties, and races: adult bariation.

  • Reprinted from De Beer's “Embryology and Evolution,” by permission of Oxford

University Press. ’{ The same as cenogenesis. THE RECAPITULATION THEORY 293

“F. In the late adult stage, 1'.e., too late, resulting in the reduction of the character to a vestige by retardation.

“G. In the same stage, which is no longer adult, the new adult stage being relatively delayed, resulting in overstepping the previous ontogenies or hypermorphosis.

“H. In the young stage, producing precocious appearance of the ancestral character and acceleration.

“Cases B and C which produce phylogenetic efiects by introducing youthful characters into the line of adults may be combined under the term paedonzorphosis. Cases E, G, and H which produce phylogenetic eliects by modifying characters which were already present in the line of adults may conveniently be included under the term geront0morphos2's.”

In Inany forms the problem is further complicated by the prolongation of certain stages while internal processes are going on. If the gradual internal development of a caterpillar were accompanied by gradual conversion of the biting type of mouth parts to the sucking type, the insect would starve, for during the transition the mouth parts would be adapted to neither the larval nor the adult method of nutrition. By the prolongation of the biting stage until the internal parts are ready for the metamorphosis, the animal’s relation to its surroundings are unchanged until the internal conditions are right when a sudden metamorphosis brings about the necessary adjustment to a new environment without loss to the insect. These facts are not in keeping with the biogenetic law as usually interpreted.

Experimental embryology and genetics have not been without their bearing upon the doctrine of recapitulation. It is now possible to show that external factors reacting with the internal, inherited constitution of the organism can produce such effects upon the oflspring that its entire ontogeny including the adult is modified. As stated elsewhere, Stockard has shown, for example, that developmental arrests will produce many types of modifications in Fundulus, including two heads, trunks, or even two individuals where only one would have otherwise been formed, and conversely that the age-old tendency of the egg to produce two eyes on the fishes’ head can be changed by the simple addition of a little magnesium chloride. The internal, inherited control of development is thus capable of modification. And Muller has shown that by exposure to X-rays the developing Drosophzla can be induced to react in such a manner that entirely new mutations, that is, selfperpetuating strains, can be produced, even at will. Thus is phylogeny deceived by ontogeny’. For these reacting ontogenies have produced an entirely new series of adults which can undoubtedly become an294 THE RECAPITULATION THEORY

cestral to others later to appear. Now phylogeny means to most thinkers just a series of adult forms having racial significance. Hence it would appear that such experiments as that of Muller have brought us face to face with an exact reversal of the usual causal role attributed to phylogeny, for here phylogeny is the direct result of ontogenetic modification and certainly not the controlling cause of it, as it is usually considered to be by the adherents of recapitulation.

From the criticisms which have been given the student can understand why the so-called “fundamental law of biogenesis” has passed from the high position of a natural law, and is little more than a general tendency. It is a tendency, furthermore, which is more valuable in retrospect than as a means of prediction. And since prediction upon the basis of known facts and postulates is the goal of science and the fundamental test of a “natural law,” this doctrine does not measure up to scientific expectation and cannot be regarded as a law.

Yet the partial truths which are involved are of sufficient value in view of the widespread occurrence of the tendency represented to warrant a revaluation of the essential idea of the doctrine. We find an attempt of this kind expressed some years ago by Lillie in his work on the embryology of the chick. His views appear to go far in the direction of harmonizing the useful parts of recapitulation and at the same time to avoid some of the contradictions which have been mentioned. He conceived that the entire life history of an organism is as necessary for the definition of species as any other character. Ontogenies are inherited also and are subjected to variation with resulting modification. Ontogenies of closely related species are more nearly alike than those less related. In the evolution of a species those stages of ontogeny latest to have arisen (those found in the adult) are the ones most easily to be modified and hence the embryo as a rule retains the ancestral resemblances the longest. This is not because these have phylogenetic, that is palingenetic, significance, but because the embryo is less susceptible to outside influences and therefore its characters are less the material upon which selection may operate. Embryonic resemblances being more conservative and actually older are nearer the ancestral condition. They are statements of historical facts rather than causes of recapitulation. But because of the chronological sequence of stages in a great many observed cases, the older recapitulationists came to regard each stage as strictly causal to the succeeding ones and thus to look upon the tendency exhibited as a law of nature. CHAPTER IV ASEXUAL REPRODUCTION

Asexual reproduction occurs in a great many plants and in many animal groups. Among the invertebrate phyla it is lacking only in the arthropods, molluscs, and nematodes of the more important groups; while among the chordates, the tunicates present many illustrations of this mode of reproduction. It should also be noted in passing that even in certain mammals a process of budding in the embryonic state occurs. This matter is discussed at length in the chapter on polyembryony where it is shown that the blastocyst of the armadillo regularly buds to produce four embryos. This gives asexual reproduction a place even among the highest groups.

In spite of the fact that this method of reproduction manifests itself in many different forms, it is essentially a very simple process. It occurs in organisms (or in portions of organisms) which have retained to a considerable extent their embryonic, undifferentiated character, and is really a mass division, due especially to the cells of some particular area undergoing a proliferation which presently results in the constriction and cutting ofi” of a greater or lesser portion of the animal. If the portions are approximately equal the process is spoken of as fission; if unequal, as budding. These, with sporulation, are the common forms of asexual reproduction, but each shows many variants in the animals in which it occurs.

Sexual reproduction, involving the participation of two individuals, is known as amphigony; asexual, since only a single individual is necessary, is monogony. In the former, germ cells or their equivalents are produced; in the latter, there are no special cells employed for the purpose. The alternation of a sexual with an asexual generation is called metagenesis. The alternation of a biparental sexual generation, that is, a case of amphigony, with a uniparental, a parthenogenetic, generation is heterogony. Sexual reproduction was further called gamocytogony or cytogony by Hartman, and asexual, agamocytogony (also agamogony).

fission is the division of an organism into two parts which are approximately equal and into whose formation very little new material has gone. The parent organism is lost in the production of the daughters,

which therefore can have no living ancestors, and can undergo only 295 296 ASEXUAL REPRODUCTION

what may be termed accidental death. It occurs when growth has taken place in excess of the needs of the individual. Contrasted to the condition in sexual reproduction, the new organism is at once provided with at least part of the organs which characterize the adult, and differentiation is always well advanced, considering that the organism is seldom high in the scale of animal life. Two categories were distinguished by F. von Wagner for organisms undergoing fission: in the one, paratomy, a special zone, in which the constriction will occur, is prepared before fission begins; in the other, architomy, no preparation is made, constriction taking place more primitively with little bodily reorganization. It should be noted that both of these categories may apply to either longitudinal or cross fission. Under the general head of fission may also be placed those cases of fragmentation, such as occur in oligochaetes and starfish, due to external influences, which may, if conditions are suitable, develop into mature individuals. These cases are also spoken of as autotomy, and sometimes as augmentation.

Budding, although not much more complex as a process than fission, is productive of much more complicated organisms and life cycles. It often is the means by which colonies are formed, and results in marked polymorphism with some of the individuals of the colony being specialized for nutritive and vegetative purposes and others for reproduction. Commonly where a considerable degree of specialization follows the budding processes the life cycle includes a sexual as well as an asexual phase and we have alternation of generations. A bud is a small portion of the parent organism which has begun to grow actively and to proliferate and from which will be derived a new individual having the full degree of differentiation characteristic of the species. There are buds in some triploblastic animals which involve only one of the germ layers, whereas in other animals the buds may include more than one layer. Furthermore budding may occur in embryonic, larval, or mature animals. Abundant illustrations of all these cases may be cited.

There are several types of budding. The most familiar are the external buds such as occur in Hydra for example in which a small portion of the parental tissue grows and constricts off to become a new, small hydra. In some of the hydroids, however, the separation is incomplete and the new individual remains as a permanent bud. The so-called “free buds” of certain forms are also of the external type. As buds they break off and become for a time at least free swimming. A second type includes the internal buds among which are the gemmulae of sponges, the statoblasts of the bryozoa, the germ balls of trematodes and others. A group of proliferating cells becomes isolated within the mother organism and in time results in a new organism. A third type involves the formation OCCURRENCE OF ASEXUAL REPRODUCTION 297

of a stolen or a “runner” from which numerous buds arise. This might seem to be really a kind of external budding but it is sufficiently distinct from the usual cases of this kind to warrant special mention. finally a fourth series of processes should be included under budding, although they are often overlooked; they are the processes known as frustulation and laceration in which small fragments separate off from the parent organism, when unfavorable conditions arise, and form new individuals.

Closely related to asexual reproduction and of much significance to the comparative embryologist are the phenomena of regeneration. Morphogenic processes are involved in the reorganization of portions of the old individuals to produce new ones which do not greatly differ from the preceding. These processes involve the regeneration of the organism or of portions of it. The student of comparative embryology should give careful thought to these processes, for in them are manifested fundamental capacities and characteristics of living protoplasm. Indeed some of these processes take us far into the innate organization and give an insight into the nature of living stuff which the Inorc usual studies fail to offer.

The formation of colonies is closely correlated with the occurrence of asexual reproduction. Colony formation occurs in certain phyla in a striking manner, and it is in these very phyla that asexual reproduction is a dominant method. It may be taken as a general rule (not, however, without exception), that whenever individuals are found organized into colonies, either asexual reproduction, or polyembryony, or parthenogenesis will be found to occur in the same groups. The simple sexual mode of reproduction seems not usually adequate to produce enough individuals to be associated together in a permanent colony, and one of those three accessory modes must be depended upon for the increased task.

OCCURRENCE or AsEx}JAL REPRODUCTION

The first examples of asexual reproduction to be found in the animal kingdom are in the protozoa, but the process here is one of single cells and perhaps is thus somewhat outside the general problems of embryology. We may begin our study therefore with the Porifera.

Porzfera. In the phylum Porifera, asexual reproduction predominates; here are to be found fission, budding, formation of free buds, and of gemmulae. Since most sponges exist as colonies it is easy to see how the dividing processes have lacked completion resulting in a degree of union that is more or less extensive. Asexual reproduction commonly leads to formation of colonies rather than to independence of organisms. But budding and fission are shown to advantage in Leucosolenia. Some of 298 ASEXUAL REPRODUCTION

the individuals indicate fission as their mode of reproduction for the products are equal in size although they remain attached at the basal end. However, the presence of small immature individuals on certain


Fm 194 Budding and fission in Leucosolema blanca. (From Korsehelt and Heider)

specimens as well as the mode of colonial formation shows that budding is often the actual method of their origin. When fission does occur it begins as a split at the osculum and progresses toward the base. When


fiG. 195. A, Budding in Leucosolema botryozdes B, A bud which has become free and attached to an algal filament. (From Korschelt and Heider, after Vasseur.)

it is not complete the beginning of a colony is seen and these colonies

often become quite complex. In another species of Leucosolenia (botrymdes), Vasseur long ago THE PORI FERA 299

found free bud formation. The buds form from an indifferent group of cells, grow irregularly from the parent individual, undergo differentiation to a considerable extent, and at length break off, the ruptured end forming the osculum of the new little sponge; they then settle down to produce young sponges.

The sponges show what is perhaps their highest degree of asexual reproductive activity in the formation of gemmulae, seen to best advantage in the Hexactinellidae. They are derived from parenchymal cells which have wandered into the mesoglea and become separated from their original layers. Aggregates of these “archeocytes” (also called “sorites” by some) take on an oval or rounded shape, become


I‘it. 106 (:(‘lllI‘n1ll( forination in Eph;/dalm blrmbmata (From Korschelt and Heider. Liter Evans )

A, an early stage showing the aggregation of the ‘ germ" cells (g) from those which make up the covering membrane (m) B, the cutieular membrane (c) is beginning to form from the outer membrane

surrounded by a special membrane and thus make up a gemmulc. During conditions which are not favorable, this structure, which is really an internal bud with a protective covering, tides over the organism until a more suitable time. Thus this form of reproduction is a device which enables these sponges to adapt themselves to changing environments. The parental tissue degenerates and dies after the gemmules are formed. When the gemmules begin to grow, the cells multiply rapidly, those at the surface arrange themselves in a layer, and from the gemmules a larva issues which is strikingly similar to the sexually produced young in form, structure, and ciliation.

Division among sponges is often accidental so far as the organism is concerned, and the animals offer opportunity for experimental fragmentation as well as normal. H. V. Wilson’s work and that of J. S. 300 ASEXUAL REPRODUCTION

Huxley give illustrations of the extent to which sponges may be dismembered (in these cases by being squeezed through bolting cloth) and subsequent regeneration serve to produce new sponges. Often cell masses come together, fuse, and grow into a new individual from which a colony is formed. This is called concrescence and may also occur between larvae as they creep about on the bottom.

Coelenterata. By the eoelenterates many developmental experiments along the lines of asexual reproduction seem to have been tried as well as those which have already been shown for the various types of embryos, cleavage patterns, and methods of gastrulation. Nearly all types of asexual reproduction are exhibited somewhere in the phylum. In addi


Fm. 197. Trunsversc fission in Protohydra. (From Korschclt and Heider. ufter Aders.)

tion there is often manifested an extreme polymorphism in the forms which are thus produced, and the details of the manner of their production especially where a compound type of budding is involved are often extremely complicated. Mention here can be made of only a few cases which constitute a very meager outline indeed. fission, both transverse and longitudinal, budding both larval and adult, and colony formation by the production of permanent buds, metagenesis, stolen formation, fragmentation, frustulation, laceration, and the related, although in its results opposing, process of concrescence, occur in this group.

The Hydrozoa exhibit only a few types of asexual reproduction. Transverse fission occurs in Protohydra, according to Aders, and consists in THE HYDROZOA 301

the simple constriction of the animal around the region of its greatest diameter. The constriction cuts the animal into a proximal and a distal portion. The one develops a new base, the other a new oral region. A similar type of division may occur in Hydra; although undoubtedly very rare, this was one of the earliest cases to be described (Trembly, 1744; see also Koelitz, 1908). It is of essentially the same character as in Protohydra, the chief points of difference between the two being in the simpler structure and the lack of tentacles on the part of the latter. Longitudinal fission has been described for Polypodium only among hydrozoa.

Budding by larval as well as by adult hydroids is not uncommon. An example of budding in the larval condition occurs in Gonioncmus and in Ilaleremita as described by Schaudinn, Perkins, and others; the details of the life cycle in these forms have been lately worked out by Joseph. The egg hatches into a tiny planula larva. It develops a mouth and creeps about actively while feeding in Haleremita, although the planula of Gonionemus is sessile. On the sides of these larvae protuberances appear which grow into buds that gradually elongate to become like the planula, then constriet at their bases, and at length separate. The descriptions of the processes differ greatly in detail as described by the different investigators. For example, from one to six buds have been reported by the various students, according to Joseph, near the base of the larva, although Perkins found them about the middle rather than the base. In some cases the endoderm of the bud is said to be solid, in others to contain a cavity derived from the gastrovaseular cavity of the mother larva. There are also other differences in the details as given, some of which are doubtless to be attributed to the fact that both European and American forms have been used by the investigators. Lateral buds also have been described as occurring on Microhydra, where they may form tiny colonies of three or four polyps.

Among adult hydrozoans budding occurs in both polyps and medusae. In Hydra and the colonial hydroids it is of such common occurrence that mere reference to it is suflicient. The bud of Hydra consists of a protuberance which grows, develops tentacles, a hypostone, and at length a mouth, after which it is ready for separation from the parent. Both layers of the body wall participate in the formation of the bud, and the gastrevascular cavity is continuous between parent and bud until the time of complete constriction of the latter. Budding is much more common than sexual reproduction. In hydroids the process is essentially the same except that it is usually incomplete, the bud remaining in connection _with the parent stalk; in this manner a colony is formed. ’ 302 ASEXUAL REPRODUCTION

A special case of hydroid budding is that which gives rise to the medusa which is morphologically the equivalent of a bud from a polyp. There are cases, to be sure, where the ontogeny is so abridged that the polyp stage is extremely rudimentary or even entirely lacking, unless the planula be regarded as representing it, and the egg develops continuously into the medusa. But in general the medusoid generation is produced by budding from the hydroid generation or the polyp. The main stalk, or hydrocaulus, has attached to it in Obelia, modified hydranths, called gonangia, which bud to produce medusae. In Obelia these become detached to swim freely. In the Narcomedusae a proliferating stolon buds off medusae which may remain in clusters or may separate off completely. In the siphonophore, Halistemma, the planula develops an ectodermal thickening at the aboral pole which develops into the pneumatophore or float. Part of the planula becomes the eoenosarcal axis from which spring buds which become several different kinds of individuals. Those near the float are bell-shaped medusae, through whose efforts the colony is enabled to swim. Next come a series of covering scales which seem to be retrogressed medusae; they are protective in function. At various places along the coenosarc are feeding tubes in general similar to a hydranth. The tentacles and feelers also are probably to be looked upon as hydranths. finally there are the reproductive individuals which resemble certain types of medusae.

It will be seen from a consideration of all these cases that budding in the hydrozoa directly results in the formation of colonies. All hydroids which bud form colonies. Usually the planula develops directly into the first hydranth and the colony is formed by the subsequent branching and budding. This brings about in all except the simplest cases a very considerable degree of polymorphism. There are defensive and sensory individuals and in these the cnidoblasts are well developed. The gonanth or gonangium has for its purpose the function of reproduction, and various modifications of gonangia are to be found throughout the group. Medusae which are free swimming show a greater degree of differentiation than any of the other types of individuals produced in a hydroid colony. There are, however, numbers of medusa forms in which the development is incomplete, and some of them are quite simple in structure. As an accompaniment to the more complex polymorphism which we find in these colonies metagenesis, the alternation of generations, is perhaps shown here to a degree of completeness that scarcely exists elsewhere in the animal kingdom. The sexual functions are transferred to certain individuals while others specialize along the lines of feeding and protecting the colony. Hydroid colonies not uncommonly reproduce by another asexual method, namely stolonization. From the THE HYDROZOA 303

hydrorhiza of the original polyp cylindrical projections grow out which elongate, creep about on the bottom and may branch or even anastomose. These are stolons or runners upon which new hydranth buds appear to produce new individuals. Bougainvillia and Clavularia both serve as illustrations of colonies which grow by stolon formation.

In the second class of coelenterates, the Anthozoa, transverse fission occasionally occurs in young animals which have not yet developed sex organs. In Fungia as described by Bourne, the development of the larva at a certain stage results in the separation of its distal part and after a complicated series of processes two individuals are produced. Longitudinal fission is common among the Anthozoa. It is a slow process beginning at the oral pole in some cases, although in Actinia it may take place simultaneously from the aboral as well. In the adult Sagartia and in Paranemonia a constriction begins at the pedal disc and passes in the course of twenty-four hours to the oral region. In some others it is much more rapid. Furthermore the constriction of one individual to produce several at the same time may take place. In this case the resulting individuals will be of varying size, and it has been observed that one division may not even be completed before a new one begins. Strange complications thus arise in which the individuals may have several mouths or several systerrs of septa at the same time owing to this multiple fission. In the Anthozoa irregular longitudinal fission sometimes gives the appearance of budding. True budding, however, is rarely met with in the sea anemones. In the alcyonarians, however, much-branched colonies are formed by budding and the individuals undergo modification and even produce a very considerable polymorphism. The Zoantharia likewise owe their extremely complicated type of development to both fission and budding. In both these latter groups stolon formation and subsequent budding are commonly observed.

One of the most striking forms of asexual reproduction is that manifested by the scyphozoa in the process of strobilization. This has already been described in the chapter on “Types of Invertebrate Larvae.” The planula develops into a hydranth-like form called the scyphistoma. By a series of divisions which may be repeated perhaps a dozen times there are constricted off from the scyphistoma, ephyra larvae of which there may be one or several. If there is only a single ephyra strobilization is said to be monodiscal, if several are produced it is polydiscal. The question arises as to the nature of these divisions. The first ephyra is commonly said to be formed by terminal budding and it would seem that if the successive ones are produced only slowly they likewise are terminal buds. However, in certain well-fed scyphistomae the process of strobilization takes place so rapidly that the lower individuals are 304 ASEXUAL REPRODUCTION

already indicated by constrictions before the upper ones have progressed to any considerable degree of independence. It would seem that the distinction between terminal budding and transverse fission in this case is a difligult one to draw. The scyphistoma also for a considerable part of the year produces other scyphistomae by lateral budding in a manner similar to that in Hydra. All at length, however, undergo strobili— zation and produce ephyrae which gradually develop into adult jellyfish. In certain scyphozoans another type of asexual reproduction occurs in the formation of stolons from the original hydranth. They grow out from its base but remain in connection with it and their buds form a colony.

Before leaving the coelenterates the attention should be called to the other methods of asexual reproduction already discussed, namely, fragmentation or laceration and frustulation. In the actinians laceration is rather frequently seen, especially when the conditions of the water become unfavorable. A part of the basal rim begins to spread out, the ectoderm develops quite profusely and endodermal portions grow out into this new area. This then separates from the main body owing to the contractions of the latter and from the pieces so produced new anemones may at length regenerate, although the ability to do so is dependent upon the number of septa present. Frustulation occurs in the hydroids. Occasionally a small bud-like branch is observed to constrict off from the parent colony, to settle down on the bottom in which condition it is called the frustulum, to grow and to produce a hydranth. In hydranths also a process somewhat similar to laceration has been observed, although in this case it is spoken of as fragmentation, for a basal portion of the polyp is cut off and may develop into a young polyp.

A final question in connection with the coelenterates naturally arises as to which condition is the more primitive. There are three possibilities: one, that budding is the primitive type of asexual reproduction; two, that fission is primitive; and three, that both arose independently of each other. There have been interesting discussions of this question and transitions between them have been pointed out. It need only be said here that the evidence is not conclusive for either view.

Platyhelminthes. In the phylum Platyhelminthes the dominant type of asexual reproduction is fission, although there are also causes of budding. It is most common among the Turbellaria, although the polyclads have not been shown to reproduce asexually. Undoubtedly the phenomenon of asexual reproduction in this division of the animal kingdom is closely concerned with the ability which all members of the phylum have for extensive regeneration. In its simplest form, as for example, in the triclads, Planaria abissima and P. alpina, the reproducPLATYHELMINTHES 305

tion really consists in the separating of the animal by transverse fission into two portions each of which proceeds to regenerate the missing head or tail. In Planaria all the species described show that regeneration may take place at various levels proceeding from the anterior to the posterior. An area of regenerating tissue appears which enlarges and then differentiates. Sometimes a second fission makes its appearance before the complete regeneration following the first, and indeed there are recorded cases of several divisions with the appropriate organs already developing before the first is completed.

Among the rhabdocoels fission is an even more general phenomenon. The small fresh-water M zcrostoma reproduces mainly by fission. Commonly this process occurs before the young have developed sex organs in this form and in Stentostoma, and the divisions may take place in such rapid succession that chains of individuals incompletely divided are the result. Division takes place by paratomy very slowly, that is, a zone of division is prepared and the organs of the new portion of the animal are already developed to a considerable extent when constriction occurs. If the constrictions follow each other more rapidly they come under the category of architomy, no special region being A prepared in advance. The distinction pm 195

S\l(‘('(“§‘\l\(‘ lI‘f'lH§V€l'EaC fis betwcon pal-altolny and 3'1-chit/Oxny sions 111 (A) Stuwstmnum SM-boldi, and

. (B) '11 trrnslomum lmcarr (From Kormay perhaps be made clear by Saylng schelt and Holder after v Grofi )

that the regeneration Of the new Pharvnx is shown for each single inorgans precedes the actual fission in dividual, and the dn 131 111 planes of the

_ different ranks are numbered paratomy, no great change in the

organization of the animal taking place at the exact moment of division. On the other hand, in architomy, regeneration and subsequent reorganization follow the constriction. 306 ASEXU AL REPRODUCTION

In general, asexual reproduction in the trematodes is rare and certainly never occurs in any individuals which have a complete set of sex organs. The situation with regard to the germ balls which produce the rediae has already been referred to in connection with the chapter on in vertebrate larvae and also that on polyembryony. It is still looked upon as an open question as to whether parthenogenesis or asexual reproduction is the method by which the germ ball that forms the new rediae is produced. It has been pointed out that originally they were regarded as asexually produced, more recently as developed in parthenogcnie ova, and finally that the cytological study of these supposed ova has not yet shown evidence of a reduction division such as would be necessary to establish surely the fact of their parthenogenic nature. If we are to regard them as asexually produced then this type becomes of much more widespread occurrence among the trematodes than is usually considered.

Among the cestodes there are two aspects to the question of asexual reproduction. One has to do with the formation of the proglottids from the scolex, the other with multiplication of the eysticercus. The first of these involves a decision as to the fundamental nature of the proglottids. Is the tapeworm to be looked upon as a colony of individuals or as a single one? If the latter

fiG 199 * view is taken there eanof course be noquestion of asexual

fzvsli::;:::;;::)‘lf,? reproduction involved. If on the other hand the pro~ T‘”"“‘ "‘”““7’3 I ttid is re arded as an individual since each h‘ “ltll an accessory g 0 . ’ a v(..,,,.1e attached complete genital apparatus and since each has the ability S°°l°°°5 “"3 to live at least for some time after the separation from present in both _ _ (From Korschelt the remainder of the worm, then its method of forma;‘3';‘:tI){°'d°" “Mr tion must be looked upon as budding, it being thus

. produced from the scolex. It is the writer’s opinion that

the colonial view is not as generally held now as formerly.

There can be no question that in the development of the tapeworm from the eysticercus budding does occur. The egg develops into the onchosphere, the six-hooked embryo, in which condition it escapes from its adult host, and is taken in by the intermediate one. From it develops directly the eysticercus. The scolex of the eysticercus arises from a thickening in the wall of the bladder which becomes depressed into the cavity and later this bud-like structure is cverted to form the little worm.

It occasionally happens that two or more scoleces are formed by budPOLYZOA 307

like thickenings on the wall of the same bladder. This multiple production of scolices is rather rare but occurs regularly as is well known in Taenia echinococcus with disastrous results to the host. This is of course reproduction by budding. In some forms the bladders themselves may constrict and produce two vesicles each of which buds into a scolex. Polyzoa. Since the Bryozoa, or Polyzoa as it is now becoming custom~ ary to call them, commonly form colonies, it is to be expected that asexual reproduction will be found in this group, and the expectation is borne out. Three asexual methods, as well as polyembryony, are found here. They are budding, stolonization, and the formation of statoblasts. As a manifestation of the complicated condition which asexual reproduction may reach in a single group, the Bryozoa probably exceed any other branch of the animal kingdom. A student of the subject will find much to interest him in the group and may expect to see an everchanging variety of detail as he studies the different divisions of it. For


Fm. 200. Buds of ('ris!aleHa muredo in median section. (From Korschelt and Ileider. after Braem.) ee , ectoderm, m., mesoderm.

the general student of comparative embryology, however, it seems unnecessary to give more than a very brief consideration to the general types of asexual reproduction as they are developed here. From a consultation of the table of classification on page 260 the student will observe that the phylum Molluscoidea, of which the Polyzoa are a portion, consists of animals very diverse in structure and in their method of development. They range from rather simple colonies to aggregations of organizations which are complex in the extreme. Among the simplest genera is Cristatella, coming under the ectoproct order, Phylactolaemata. All the individuals of a colony of this form can be traced to the first one which develops from the larva. This individual produces buds commonly as thickenings of the pharynx on the oral side, both ectoderm and mesoderm participating in the process, although the ectoderm contributes a larger portion to the formation of the new individual. As the bud enlarges it grows out from the parent individual and its inner cell mass undergoes a very considerable differentiation. The intestinal tracts commonly remain in communication at least for 308 ASEXUAL REPRODUCTION

some time. An entire series of buds which in their turn repeat the process is involved in the production of the colony. The development of buds in the Endoprocta closely resembles that just described. The bud is first an enlargement of eetoderinal cells which receives migrations of meso W


0

F16. 201. A piece of Plumalella fungnsa showing the formation of the primary buds and of those which arise secondarily.

dermal cells as it develops. In this group a stalk makes the bud rather more independent than in the preceding. In some forms, notably the ectoproet groups Crissia and Tubulipora, budding takes place in the embryonic stages even before any differentiation of the blastomeres begins. The primary embryo produces a

32 B13 C D E F great number of buds in such a case and B, may become a stem and retain the others as secondary embryos or it may be en— tirely destroyed in their production. Of course the secondary embryos may also reproduce asexually. It is rather rare that the buds should separate naturally from each other, for it is by their uninterrupted relation to each other that the colony is Fm 202. Dmgmmmntic “_pm_ formed. They may branch laterally from

aem,m.,n of the method 0; i,m,ci.- the main stalk or may continue in a direct

in“ i" P“”"“"'”“ f"‘“‘”"*"“' (l“'°’“ line of the main branch. It is obvious that Korsehelt and Heider, after _ , . _ ’ Bmem) in such a highly organized type of animal as this, polymorphism of the individuals is to be expected. Special morphological changes take place so that some of the individuals of the colony become very much changed from the typical form and have very different functions. The Bryozoa. always reproduce by sending out stolons which then bud many times. The formation of the stolon itself is like that of the bud but it grows out as a stalk which

by repeated incomplete divisions produces a new portion of the colony.

A

I V AB3B‘~’BBC‘C D E 1‘ G POLYZOA 309

Some fresh-water forms produce hibernacula. which.‘ are essentially winter buds, club-like swellings on the stolons which enclose themselves in a cutaneous capsule during the period of severe winter. In the spring their development continues to form new colonies. Accidental subdivision of a colony is of course common, but the multiplication of the colony by fragmentation appears also to occur naturally.

fiG. 203. Production of zooecia ns buds from stolons (st.) of Pedicellina erhinala. (From Korschelt and Heider, after Ehlors.)

A final method of asexual reproduction is the formation of statoblasts. According to an old view a statoblast is supposed to arise from a single cell and upon the basis of this it was thought to be a sort of winter egg. It is now realized that the statoblasts are modified buds which have become changed into reproductive buds. They vary in shape, but are enclosed in a cutaneous capsule and contain several cells. They are 310 ASEXUAL REPRODUCTION

able to withstand extremes of temperature and thus serve to carry on

the colony during the cold of the winter. Amwlida. Asexual reproduction is of common occurrence in the two most important groups of the annelids, namely the polyehaetes and the


Fm. 204. Statoblasts of Cristatella mucedo. (From Korschelt and Heider, after Kraepelin.)

oligochaetes. This is due to the remarkable uniformity in the structure which the annelid body possesses, each segment being very similar to its neighbor. The growth of the annelid worm is accomplished by the


J __ ._5B.'5:'l!

w



C ‘SIN! _ .. " ifl‘-Jijurvl ‘ .u1l1“‘L4“ .


F10. 205. Developmental stages of the statoblasts of Crietazella. (From Korschelt and Heider, after Verworn.)

addition of the somites to the posterior end primarily, although anterior zones of budding are also found. In some instances the formation of new somites takes place more rapidly than their separation from the animal ANNELIDA 31 1

and thus a chain of individuals is formed. In a simple annelid chain in which the individuals of a series are spoken of as zooids in anticipation


fiG. 206. Germinating statoblasts of Cristatella. (From Korschelt and Heidcr, after Braem.)

A. the “germ disc" stage. B, its invagination preparatory to further growth.

of their future development to individual worms the anterior individual represents the original worm and is obviously the oldest. At its posterior


fiG. 207. Posterior end of Trypanosyllis misakiensis showing buds of difierent ranks. (From Korschelt and Heidor. after Johnson.)

end is a reproductive zone where the budding oil’ of new individuals takes place. The first individual budded off is of course the most posterior 3 12 ASEXUAL REPROD1 'C'l‘ION

of the chain, the others grading in age and size toward the middle of the worm where the budding zone is located. In the more complicated cases, of which the syllids are the extreme example, we may have not only terminal budding but also lateral and even ventral. In one of these forms, Trypanosyllis misakiensis, single budding soon produces numerous buds in all directions differing in age but ,.,:‘:.:-as *;:::r;..:" Merwisc giving the W231‘(Fmm Komheltamui ance of a rosette of small zooids. after v. Kenr}x]<:)l.) Between these two extremes lie gen‘: 0, S ‘V various degreesof complication in the forms produced. In many marine polychaetes a differentiation with respect to reproductive capacity is observed between the (lif ferent parts of the animal. The anterior portion of


the individual is sexless and is spoken of as the atoke. = H At the time of sexual maturity this slow-moving worm becomes very active, the hinder somites de- = 1

velop gonads, and special 1

‘W bristlesandparapodiagrow

El ‘ W _ out on them, developing

lllllllll them for rapid and exten sive movement. This sexual

portion is spoken of as the __

cpitoke, and individuals of "

this kind were earlier given

special systematic descrip tions. It is now clear, how ever, that N ereis, for ex— Fm- 209. Diu. grains to show the

ample; passes Over "Ito divisions zones in

H eteronereis or the epito— £0": hmlzaa. d(fir{or}1 - . . t kous stage. In many po1.v- dfflfnir c‘L'how..,°.3

chaetes, the epitokous por tion separates from the remainder and swims 

: ' , ' ' d t th —

Fm. 210 The mlom about a(t1vely for a certain perio a e sur

worm. Eunice vimkiis, show- face of the sea. This is the swarming which

5”‘! ‘he ‘“”°’°“°° be‘“"~‘°" takes place in N ereis and is especially notable the anterior ntokous part , ' . . . . and the posterior epitokous in the palolo-worm, Eumce 1)27'Zd’l8, whose

portion. (From Korschelt . ‘ ' ' ' d and Heme“ aim W00d_ swarmxngm the south Paeificisoften observe

ward.) as a very unusual phenomenon. ANNELIDA 313

A further (-lassificatioii of tho asexual methods of reproduction in this group may he based upon the degree of preparation which precedes

fiG. 211. J! yriamda fumata with 29 zooids. (From Korscholt and Heider. after Maluquin.)

the division. In the simpler cases the division of the worm takes place between two segments with no special zone of separation having been developed. Following the division regeneration occurs producing a head 314 ASEXUAL REPRODYCTION

or tail, or in some cases where a portion of the middle of the worm is cut off from both ends both head and tail are regenerated. As has been pointed out this regeneration after division is known as architomy in contradistinction to paratomy where a. separation zone is developed before division. Such a zone is really the beginning of an early regeneration and may be present in variable degrees all the way from a simple region of constriction to the formation of a well—developed head and sensory apparatus.

Architomy is illustrated in Ctenodrzlus monostylus where without much preparation the worm divides into an anterior and posterior part by constriction and the lacking parts are regenerated. Regeneration begins at once, although the new worms continue to creep about actively in spite of the fact that they cannot for a short while take in food. Architomy may be accomplished by autotomous division of the worm. A number of polychaetes and oligochaetes have such great powers of regeneration that they are enabled to separate without external stimulation. Lumbnculus is an annelid of this type.

Paratomy is illustrated by certain species of Ctenodrzlas also, especially C. serratus, in which the regenerative powers are so great that even single segments may in certain cases produce new worms. Beginning a few segments

Fm 012 Tami”: mulomm with a back of the head, cellular prolrferations pnmaw" ,e;;(.,,e,a,,,,g Dome" and mo takeplacewhichgraduallyformthicken ings on the anterior side of each segment.

' They become the head folds and give rise to the organs of the head region in the new zooids. Thus a chain of zooids is formed asexually. Additions of this sort produce what is functionally an alternation of generations. It is scarcely developed with the regularity that characterizes this process in such forms as hydroids. The original individual was developed from the egg. It produces asexually a chain of zooids which separate from each other and when weather conditions become suitable develop further into individuals which reproduce sexually. Of course second and third asexual generations may be produced in the same manner as the first one. PTEROBRANCHIA 315

Echinodermata. Among the echinoderms asexual reproduction is described, but it is certainly of rare occurrence and one has difliculty in distinguishing it from an extreme type of regeneration. Spontaneous division of the arms and in some cases the splitting of the disc have been described in the asteroids, ophiuroids, and in the holothurians. Asteroids have been seen to split and separate, beginning at the gullet, and then

flu. 213. S1/Ilis ramosa showing anterior end of worm and the complex branching. The gut is stippled in the figure. (From Korsehelt and Heidor. after Maclntosh.)

the missing arms and organs of the disc to become gradually regenerated. It is of course well known that where accidental separation of the parts of an echinoderm is brought about extensive regenerations follow and theoretically there is no great difference between this and a natural type of division followed by regeneration. However, the latter is certainly of earlier occurrence.

Pterobranchia. The two genera Cephalodiscus and Rhabdopleura which compose the anomalous Pterobranchia both illustrate asexual reproduc316 ASEXUAL REPRODUCTION

tion by budding. Their doubtful position showing similarities both to Balanoglossus and to the Bryozoa is nevertheless in line with their type of reproduction. Cephalodiscus occurs as a single individual from the side of which a stalk grows out. This stalk bears a bud as is shown in the well-known figure often copied from Maclntosh. The bud arises from the apex of the ventral stalk and after a certain age breaks off. The animal lives in a gelatinous coenoecium where a large number of free individuals may be found. The animal possesses practically all the important organs found in Balanoglossus and structurally seems related to that form. Its method of asexual reproduction, however, much more strongly resembles that of the Polyzoa. Resemblance to the latter group is rather more striking in Rhabdopleura which lives in a tube and reproduces in a manner similar to that of the stoloniferous Bryozoa. The general anatomy, however, closely resembles that of Cephalodiscus. In Rhabdopleura the individuals derived from the buds remain close together and form small colonies living in branched tubes. They are con— nected by a muscular cord which passes back to join a common stem or stolen. The cord is the narrowed proximal portion of the body. By its contraction the animal is retracted into a stalk. The stolen is developed as a bud from the original zooid,

1«'.c.. 214. ('c1)Iw,lod£scus with but the details of the process are not well §:f:‘lt'i$;:f’)“‘M“°I“t°*h'“'i”"“°‘ll‘ understood. Part of the stolen loses its

formative power and becomes merely a connection between the creeping parts of the colony. The remainder, however, buds, and the buds give rise to branches. In the free-growing part there always appear two buds, an anterior, well—developed one and a posterior much younger.

Tunicata. Among the tunicates asexual reproduction is widespread and occurs as an important means of multiplication in two of the main divisions of this subphylum, the composite ascidians and the salps. The dominant type is budding but the details show various departures from the simple form and even instances of fission are observed within this group. It will perhaps serve our purpose to limit our discussion to the budding in the two cases mentioned, understanding that there are some other minor examples to be met with in this group. The embryology of the ascidians has been described in Part One of this book. The young embryo grows and in many cases begins its process of budding TUNICATA

317

before it has become attached and begun its metamorphosis. It is customary to speak of the individual which is produced from the egg as an oozooid whereas the individuals which are produced from buds are blastozooids. However, the individuals so called may become modified

in various ways and be given other names to indicate functional and morphological differences which later occur, for budding in the tunicates as in some other groups leads to polymorphism and to alternation of generations.

In the compound ascidians there are two main types of budding, palleal and stolonial, differentiated according to the position on the oozooid in which they occur. By palleal budding, which also goes under the name of peribranchial or atrial, or also cntero-epicardial, is meant the growth of a bud as an oesophageal or even intestinal outgrowth; it is thus derived near the atrial wall and under the mantle or pallium. It is common for the buds to be formed as lateral evaginations of the body Wall in symmetrical parts, but usually only one of them develops. Mesoderm and germ cells migrate from the tissues of the mother into the bud which gradually becomes a complete individual. The processes are the same in the asexually produced blastozooid and in the oozooid which are developed from the egg, but the oozooid undergoes a retardation in development and never reaches sexual maturity whereas the blastozooid develops fully although it is to be noted that both may reproduce asexually as well as sexually. The oozooid is short lived. After it has reached the typical form of the ascidian it undergoes retrogression and its tissues are used to build up new individuals. In the composite aseidians although the buds are independent of each other they yet remain enclosed in a common cellulose mantle, and after a number of generations have



‘ ‘~ .-..-.-I!l!‘."'€.;',.7,_,,’

Fm. 215. Budding in Rhabdopleura normanni.

(From a diagram by Korschelt and Heider.)

b. buds of different ranks from a common stolon (st.).

been produced the mass takes on the form of buds united into a very definite system built upon the plan of concentric circles of buds. As the system becomes more and more complicated some of the individuals become crowded out of their proper place and so become the center of a new irregular subdivision of buds. In this way a colony is formed. The place of origin of the buds varies in difierent genera, a fact which 318 ASEXUAL REPRODUCTION

gives rise to the marked differences in appearance of different colonies of compound ascidians. Thus we have pyloric budding which is also called oesophageal, epicardo-oesophageal, and epicardo-rectal budding. In this type when the blastozooid buds it is really of compound origin, the new process arising from abdominal and thoracic outgrowths, the abdominal bud being an invagination of the oesophagus and the thoracic formed largely from the epicardium. From a diverticulum of the left portion of the epicardium the nervous system is derived. It is thus endodermal in origin in the blastozooid, although in the oozooid it is derived in the regular manner from the ectoderm. Pyloric budding is described chiefly in the didemnids and the diplosomids. Among the modifications of the general type of budding described for the compound ascidians are the cases spoken of as pseudo-stolonial, occurring especially in the distomid Distaplia and in the polyclinids. Authorities differ in the manner in which they regard the budding of these forms, some tracing it to the formation of a stolon and others regarding it as more nearly related to the type already described. In Distaplia the formation of the “primordial buds” has been described as coming from the epicardium, but Salensky, Julin, Della Valle, and others have described this as a proliferating stolon from the intestine. The first generation of these buds never develops sex products but later generations of buds may reproduce sexually. It may be noted that the epicardium is wrongly named in that it does not participate in the formation of the pericardium and the heart, although it was so described by van Beneden and J ulin. Actually it is the endodermal element of each bud. In the polyclinids the budding of the posterior part of the animal resembles horizontal division, for the caudal part of the larva clongates and constricts, forming thorax, abdomen, and post-abdomen; gonads and heart develop in the latter which subsequently segments to form buds. By some this entire caudal portion is regarded as a stolon.

As an example of stolonial budding reference may be made to Perophora and to Clavellina. In Clavellina, after its attachment, root—like processes are sent out from the base giving it a more firm hold. At least one of these processes becomes the proliferating stolon (stolo prolzfer). The stolon consists of the three germ layers in addition to the cellulose tunic which covers it. From it arise buds as well as side branches. If a particular outgrowth contains an endodermal layer it would develop into a bud. Otherwise it is merely a sterile branch. Buds arise near the growing tip of the stolon, but simultaneously with their development the top continues to grow, so those near the base of the stolon are the more mature. Younger ones sometimes arise as a new generation of buds between the older ones. Stolonial budding takes place only from TUNICATA 319

the oézooid for the blastozooid can reproduce sexually. It should be noted in regard to the formation of colonies that although the usual condition is the production of an entire colony from a single oozooid, yet small colonies sometimes grow so close together that concrescence results and they fuse into a larger colony.




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F16. 216 An adult of Clavellma with a stolen and .i young individual budded ofi from it (From Korschelt and Hcider, after Secliger )

In many respects the most interesting case of asexual reproduction in the tunicates is the formation of the Salpa chains from a proliferating stoloii. When investigators first began to study Salpa, solitary individuals were found, and also others which appeared to have a significantly different structure and were connected together like a chain or even a rosette were also occasionally discovered. At length the relation between the two was made out by the poet, Chamisso, who discovered that the solitary individuals can produce the chain salps and that certain individuals of the chains developed sex organs from which the 320 ASEXUAL REPRODUCTION

solitary individuals were again formed. The solitary individual always reproduces asexually but is itself produced from a fertilized egg. From the ventral side of the posterior half of such a solitary individual a bud, which first arose from the pharyngeal endostyle and is therefore in its beginning eiidodermal, grows out. As it enlarges, the mesoderm and ectoderm surround it, and finally it becomes a projection from the tunic as well. It is a direct continuation of the ectoderm and endoderm of the


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fiG 217. Nearly adult stages of Dolwlum dentwulatum (From Korschclt and H0|d(‘r, after Neumann.)

cl , cloacu, d c , dorsal horn or cadophore to which buds Will be uttuchcd, st , \CIlU‘dl stolon from whuh buds are produced, t , mil with chorda

parent individual and its parts are likewise related to the organs which develop in its buds derived from it. This is the ventral proliferating stolen and the individual producing it is the oozooid developed from the single egg of the gonozooid.

The history of the ventral stolon differs somewhat in Salpa and Doliolum. Perhaps the latter, as described by Uljanin, is the one more familiar to students. As in the compound ascidians the oozooid produces no sexual organs but a great many buds arise from it in a complicated manner and the chain thus produced exhibits a high degree of polyVERTEBRATA 321

morphism. Indeed, the oozooid itself degenerates until it becomes nothing but a locomotor organ of the rest of the chain. The buds are produced continuously for a considerable time from the ventral stolon. They do not remain in that part of the body, however, but migrate dorsally to a posterior dorsal horn, or cadophore, which is an outgrowth resembling somewhat a stolen but does not of itself bud. Its epithelial cells become specially suited for the attachment and nourishment of the migrating buds which will presently reach it. As a matter of fact, however, there are more buds in the dorsal cadophore than were produced from the ventral stolon, multiplication in the form of a simple division having taken place during the migration. The cadophore continues its growth and more and more buds are attached to it. They arrange themselves in two lateral rows and one dorsal median row. The lateral blastozooids which are attached by a short stalk are nutritive and respiratory. They are apparently unable to reproduce and are morphologically independent of the rest of the colony. The median blastozooids are spoken of as nurse individuals, or phorozooids. They are rounded and have a stalk on the ventral side. It is this stalk which bears the buds that in their turn are to give rise to the sexual forms. Like the lateral blastozooids, the nurses are non-reproductive. The buds which arise from the stalk of the phorozooids are usually spoken of as protogonozooids. From these the sexual blastozooids, that is, the gonozooids, are produced. They are free swimming, undergo a considerable change in their general structure, develop sex organs, and the cycle is completed, for from the fertilized egg comes the new zooid ready to begin the asexual cycle again. Thus there are two distinct asexual generations, the oozooid and the protogonozooid, and some of the blastozooids have also multiplied by simple division in passing to the dorsal cadophore. These two asexual generations alternate with the one sexual generation. The development of all forms of Salpa is not understood yet and in some cases it is difficult to interpret the forms that have been found. The life cycle of Doliolum, however, illustrates satisfactorily the degree to which asexual reproduction is developed in these forms.

Vertebrate. In forms higher than the tunicates asexual reproduction does not commonly occur. However, the case of the armadillo which is described in detail in the chapter on polyembryony must be mentioned. Here a blastocyst is formed as a result of the cleavage of the egg which produces by budding four individuals. This is, of course, an asexual method of multiplication, and may be of general significance, as is suggested by the production of identical twins in various other forms of mammals. CHAPTER V PARTHENOGENESIS

I. NORMAL PARTHENOGENESIS

A. GENERAL DISCUSSION

As an embryological problem the phenomenon of parthenogcnesis has been of interest since its discovery in 1762 when Bonnet found that the summer generations of aphids reproduce by means of unfertilized eggs. The literature dealing with the subject is a vast one, for parthenogencsis is of wide occurrence in the animal kingdom and is also known among the plants. In spite of the vast amount of research on the problem, however, it has only recently become possible to bring the known cases into any kind of systematic order. The problem also has a great deal 01 cytological and genetical interest for we are here dealing with uniparcntal inheritance and it is obvious that the chromosomal mechanism which explains the inheritance of bisexual forms must undergo some modification to account for the appearances in unisexual organisms. While the cytological and genetieal aspects of parthenogenesis are closely related to the embryological, we can treat them only briefly and must devote ourselves chiefly to the embryological problems.

Confusion sometimes develops in the mind of the student in relation to parthenogencsis for at first thought one is apt to class all types of uniparental inheritance together and think of parthenogcnesis as a modified asexual type. The fallacy of this conclusion is easily seen, however, for parthenogenesis deals with the development of an egg although without the cooperation of a spermatozoon. It is clearly a gametic form of reproduction; its relationships are perhaps more easily understood if we speak consistently of unisexual and bisexual reproduction. It would perhaps be still clearer to use the terms monogametic and digametie, although these are not commonly found in the literature. The critical point in the evidence that we are here dealing with a second type of sexual reproduction is seen in the formation of polar bodies and the behavior of the chromosome during the maturation division. In some cases of parthenogenesis polar bodies are often seen to be formed and in other cases the behavior of the chromosomes in reduction is

well known. In addition to this evidence, the sporadic occurrence of 322 TERM INOLOGY 323

parthenogenesis in diverse classes of the animal kingdom, the occasional occurrence of parthenogenesis along with the bisexual method in the same species of animal, as for example the bee, and the not uncommon alternation of the parthenogenetic mode with typical sexual reproduction in the course of several generations within the same animal all bear out the same conclusion. Furthermore, the fact of artificial parthenogenesis, that is, the activation of an egg which would otherwise develop only by fertilization, shows that we are dealing with what must be a modification of the usual type of bisexual reproduction. Artificial parthenogenesis means the initiation of development on the part of the egg by chemical or physical stimulation artificially induced to take the place of the type of initiation usually to be seen only when the sperm enters the egg. It is really a study in experimental embryology which has been of the greatest value in giving an insight into the true nature of the process of fertilization.

a. Terminology. Throughout the animal kingdom parthenogenesis occurs in a wide variety of types and under many different conditions. Owing to this fact the literature concerning it contains many descriptive terms that are of special application and about which some confusion of meaning has grown up, as has been the case in certain other processes that are familiar but not clearly understood by the majority of students. In some species parthenogenesis is of rare occurrence and the eggs simply possess the power of developing without the intervention of the sperm, although they usually develop after fertilization. Such cases are known as facultative or optional and are of such irregular occurrence in the series as to be of no great embryological significance. Obligatory parthenogenesis occurs regularly in the life cycle of organisms which show it as a constant feature or only at certain intervals. Its importance is manifested by the fact that parthenogenetic eggs are often structurally different from those that are to be fertilized and there are morphological differences between the animals which are produced parthenogenetically and those which are produced bisexually. For instance, the eggs of daphnids which are fertilized usually develop only during the colder seasons of the year; they are known as winter eggs and have a protective shell that is very different from the summer eggs. Oftentimes cases of obligatory parthenogenesis show an alternation of generations although not of an asexual generation with a sexual, but of a unisexual generation or a series of them, with a bisexual generation. Where this type of development is firmly established a series of par thenogenetic generations may be developed to such an extent that it becomes the predominant method of reproduction and sexual genera3 24 PARTHENOGENESIS

tions appear only at infrequent intervals. Many of the more familiar cases of parthenogenesis are of this type.

Even in the extreme obligatory type it is often possible by experimental means to induce the sexual process, for instance, by a change of the environmental conditions. The rotifer, Hydatina senta, as shown by Shull and by Whitney, in old culture infusions will continue parthenogenetically for long periods of time, but if a fresh culture fluid is used bisexual animals soon make their appearance. Conversely, it is possible by maintaining appropriate conditions to postpone or even entirely to suppress the sexual process, as in the case of the rose aphid when cultivated through a series of years in a greenhouse.

In cases where structural differences are to be observed between the parthenogenetic and the bisexually developed eggs, a functional difference also is frequently seen in that the eggs of certain individuals are exclusively male producing, that is arrhenotokous, and of others female producing, or thelytokous. Where both males and females are produced in one brood, parthenogenesis is said to be amphoterotokous. Where the number of parthenogenetic generations which occurs before the sexual animals are produced is indefinite we say that the species has an “open life cycle.” Such cases occur in the aphids and in some species of phylloxerans. In others the female which produces the parthenogenetic eggs and hence is known as the stem mother must develop directly from the previous fertilized egg. This is the “ closed ” type, and it occurs in certain other phylloxerans and in the gall flies.

Considering the embryological aspects we should classify known cases according to the grade or degree of parthenogenesis shown. It is possible to distinguish seven or eight different grades of parthenogenesis as follows: (a) Pathological. In the ova of birds it is frequently observed that a few cleavages take place resembling the normal but not leading to the formation of the blastula. Similar phenomena have been observed in some other eggs as well. (b) Casual parthenogenesis. In the case of the silk moths under exceptional conditions aspermic development takes place. (0) Occasional parthenogenesis. In the ants, bees, and wasps, the development of the egg without fertilization always produces a male. (d) Partial parthenogenesis. The queen bee by the copulation on the nuptial flight receives all of the sperm which she will ever use, and afterwards she can fertilize the egg to produce a female, that is, a worker or a queen, or leave it to develop parthenogenetically into a male, since she has control over the process. (e) Seasonal parthenogenesis. In the case of Daphnia already mentioned and other Entomostraca and also the aphids the summer eggs are parthenogenetic and the winter fertilized. (f) Larval parthenogenesis. The case of Miastor is described CYTOLOGICAL RELATIONSHIPS 325

in the chapter on paedogenesis. Some larvae are produced parthenogenetically and inside of them others through a number of generations. each eating its way out and producing yet others. finally the last larvae pupate, undergo metamorphosis, and develop bisexual forms. (g) Total

parthenogenesis. Only parthenogenetic eggs occur through many generations as is especially illustrated by the rotifers.

b. Cytological Relationships. A consideration of the cases of parthenogenesis upon the basis of their cytological conditions leads to the common classification of haploid and diploid parthenogenesis. By haploid parthenogenesis is meant the development without fertilization of an egg which has gone through the process of chromosome reduction. Haploid eggs in general are sexual, and in most cases in which aspermic development is possible the eggs are found to be capable of development either with or without fertilization. Hymenoptera, some of the Hemiptera, and the arachnids often exhibit haploid parthenogenesis. One case, the nematode Rhabdites (R. aberrans according to Kruger and R. pellio according to P. Hertwig), is worthy of note, however. Here the eggs develop parthcnogcnetically and are of the haploid type but the penetration of the sperm is necessary to initiate the development although it takes no further part and no true fertilization is accomplished. After it has penetrated the cortex of the egg, and thus set going the developmental processes, the sperm degenerates and the further development of the egg is as much parthenogenetic as if no sperm had been involved.

Diploid parthenogenesis is much more frequent, occurring in most of the other groups where parthenogenesis is found at all. Copepods, ostraeods, and the Hemiptera-Homoptera have this type characteristically whereas trematodes, nematodes, echinoderms, the phyllopods, the Orthoptera, and the Lepidoptera exhibit it in certain forms. An intermediate condition is found in the rotifers, both diploid and haploid parthenogenesis having been described for these forms. Triploid parthenogenesis is also known but is not common. The best understood case is that of the plant genus Hieracium which has been described by Rosenberg. There are two sections of this genus which differ in their cytological behavior. The sexual form of H. umbulatum has a diploid chromosome number of 18 whereas the variety linearifolium has a diploid number of 27. There are also some in which the diploid number is 36. The parthenogenetic Archieracium, which is closely related to this species, shows a chromosome number of 27. Rosenberg explains these facts upon the basis of hybridization. The triploid races, Rosenberg maintains, cannot easily beproduced by the usual bisexual processes. Triploid parthenogenesis, however, is of rare occurrence, and the triploidy in 326 PARTHENOGENESIS

animals which result from fertilization of a diploid egg, if that can occur, certainly produces only an abnormal zygote.

Usually the number of polar bodies which is given off by the animal egg permits, the observer to distinguish whether he is dealing with the haploid or diploid mode of development; in the haploid case two polar bodies are produced in the haploid manner, whereas in the diploid a

single maturation division produces only one polar body and no reduc-'

tion of chromosomes can take place. There is one special case of parthenogenesis to which was early ascribed theoretical significance in working out a theory of fertilization. O. Hertwig in 1890 described a process in the maturation of the starfish Astropecten which has been many times referred to since, namely, the reunion of the nucleus of the second polar body with that of the egg. A similar condition was reported by Lefevre for the egg of Thalessema in which the second polar body is not extruded, the spindle remaining “submerged” in the cytoplasm of the egg. Upon the basis of these observations parthenogenesis was for a long time supposed to be explained as a kind of fertilization by the polar body. It is now known, however, that such cases seldom occur. A somewhat analogous case is that of the wasp H abrobracon in which a cytological study shows parthenogcnetieally produced males to be haploid on account of the fact that the first spermatocyte division is abortive while the second is equational (A. Whiting, 1927). Of course cases in which only one maturation division occurs are not rare.

c. Parthenogenesis and Sex. Much of the work upon parthenogenesis has been due to the bearing of the problem upon sex determination. Many experiments have been made for the purpose of discovering what factors can influence the production of males or females within the parthenogenetic strains. Especially have the rotifers been used for experiments of this kind. Punnett observed various kinds of females as follows: arrhenotokous females or those which produce males; thelytokous females (female producers) of three kinds, namely, those which produce, respectively, a large percentage, a small percentage, and those which produce no arrhenotokous females. In the attempt to influence the sex of the progeny of these forms conflicting results have been obtained. The studies of rotifers have been most extensively carried on by Whitney and by Shull. In general Shull’s experiments on the modification of sex have yielded positive results, for he has found a relationship between metabolism and sex determination. When the quantity of food given H ydatina senta is small the number of male producers is increased; old food reduces the number. Creatin, ammonium salts, beef extract, and low temperature prevent the formation of male producers. Longcontinued parthenogenesis results in a decrease in male production. INTERSEXES 327

Oxygen in the water increases it, although osmotic pressure, alkalinity, and acidity were not found to be effective. Whether the egg is to develop into a male or a female producer is decided during the growth period but not in the early oogonial stages. Sex is determined a generation in advance.

Whitney, on the other hand, has found less evidence that male production is a response to external conditions, although he did find that crowding in H. senta permitted the development of fewer male producers in direct proportion to the degree of the crowding. He found, however, that neither oxygen, temperature, nor starvation is a factor. One of his strains when fed continuously upon a diet of Polytonia produced nearly all females for twenty-five generations, only three per cent of the daughters being male producing. But a change of diet to Dunaliella increased the percentage to 57. When they were fed again upon Polytonia, the percentage fell off. The influence of the food was found to be upon the grandmother.

In addition to the work of Shull and of Whitney, Noyes has reported a series of experiments on Proales decipiens lasting through 250 generations in which no males appeared although the animals were subjected to various environmental changes including changes of chemical composition, of temperature, and of feed. More found Brachionus to give increased arrhenotekous females upon treatment with chemicals such as ferric chloride (FeCl), whereas constant diet and temperature gave only thelytokous individuals.

Banta has studied the sex production in the parthenogenetic Cladocera, especially in M oina macrocopa. His studies with Brown upon sex control showed that experimental crowding brought about male production along with lowered metabolism in the females. The amount of food was not found to affect the results but a change in its character did have a profound effect. Male production was associated with an accumulation of excretory substances. Aeration with oxygen decreased the production of males even in crowded cultures. Similarly carbon dioxide, urea, and ammonium salts as well as other products related to excretion reduced the number of males.

d. Intersexes. Another problem in relation to sex has appeared in some of the parthenogenetie strains of Cladocera. It is the condition of intersexes or, as originally described by Banta, sex intergrades. The intersex condition manifests itself through the secondary sex characteristics in that a typical female has a series of eight secondary sex characters which are identified with her sex, and similarly for a typical male. The eight characters are as follows: (1) body size, the females are the larger at maturity; (2) size and position of the eye, the eyes of the 328 PARTHENOG EN ESIS

females being smaller and crowding the margin of the head less than those of the males; (3) outline of the head, the angle of the anteroventral margins of the head being more acute in the male; (4) absence in the female of the nuchal protuberance; (5) and (6) character of first antennae, the males having swollen basal portions and two lateral stylets; and (7) and (8) the outline and armature of the lateral postabdominal margins, these being more concave and not serrated in the female. The intersex individuals may have the sex organs of either sex accompanied by from one to several of the secondary sex characters of the other sex. There are also hermaphroditic forms with various combinations of the male and female secondary characters. It is Banta’s opinion that these intersex conditions in Cladocera and other parthenogenetically reproducing forms are probably determined by environmental factors.

A relation of hermaphroditism to parthenogenesis appears in certain cases and it has been suggested by Winkler that it is one of transition, hermaphroditism leading over into parthenogenesis. At least the case of Rhabdites aberrans as described by Kruger points in that direction. These animals are free-living nematodes found in moist earth and are almost exclusively females, two counts showing four males out of 10,000 females and thirty-two males out of 2026 individuals, respectively. But the females are hermaphroditic and the entrance of sperm into the egg is necessary for the initiation of development, although it takes no further part in the process and the cleavage of the egg is as truly parthenogenetie as if no sperm had penetrated into it. In addition to this relationship, hermaphroditism may be superimposed upon parthenogenesis at least in one family of the Phyllopoda where it appears that Lepidurus which under favorable conditions reproduces parthenogcnetically “may become hermaphroditic when food is scarce ” (Bcrnard,1896).

e. Geographical Races. Another matter of interest is the occurrence of geographical races which are parthenogcnetic. The phyllopod, Artemia salina, according to Artom, reproduces differently in different localities. Races which are exclusively parthenogcnetic occur in Marseilles, at Capodistria and in certain other Italian localities. Bisexual races occur in Cagliari in Italy and in Utah; and a third class in which both bisexual and parthenogcnetic modes occur is found at Odessa in Russia. Vandel described the conditions in the isopod, Tr2‘chom'scus provisorius, in which there are two distinct races, one bisexual in the usual sense, and the other a female-producing parthenogcnetic race. These occupy distinct regions, the latter occurring in northern Europe, but at some points the two may co-exist. These two races are looked upon by Vandel as incipient species. Geographical parthenogenesis has also been observed CAUSES OF PARTHENOGENESIS 329

in the moth Solenobia by Seiler. Solenobza triquetrella and S. znfleti occur in both bisexual and parthenogenetic forms, the latter being permanent and thelytokous. Of S. triquetrella the parthenogenetic form is widely distributed in Germany, Austria, and Switzerland, but the bisexual form has been found in a single locality only. In S. pineti the bisexual form is common but the parthenogenetic is restricted to a very few localities. finally Trialeurodes vaporariorum, a white-fly has two races, according to Schrader, that are unlike in their parthenogenesis, in that the English race produces females with only three per cent males and the American parthenogenetic females produce males only.

f. Causes of Parthenogenesis. Of the causes of natural parthenogenesis little is known. It would seem that the developmental mechanism of the egg is capable of activation in more than one manner. Usually the entrance of a sperm into the egg sets off the processes which are involved. This initiatory action is capable of imitation by both chemical and physical means as in the cases of artificial parthenogenesis. There are also conditions in which, it would appear, development may go forward automatically, the participation of the sperm being entirely dispensed with. In the case of the normal fertilization of any egg there is no reason for regarding the developmental processes of the egg as brought to a. standstill before the sperm enters. Rather they are slowed down to a speed from which they will not recover unless external influences are operative, usually in the form of the sperm. Perhaps monogametie development is possible only where the inhibition is less intense, thus giving automatically normal parthenogenesis. On this hypothesis the failure to induce the development of sperm, by placing them in suitable media as has been reported by Locb and others, may mean nothing more than that the developmental processes in the sperm are reduced to a still lower speed from which no means thus far tried have been effective to return them to a functional level.

Other suggestions have also been ‘made as to the factors which are responsible for parthenogenesis. Issakowitsch held that in Cladoeera the alternation of bisexual and parthenogenetic stages was governed by changes in the nucleo-cytoplasmic ratio. Papanicolau reached similar conclusions. Shull, however, investigated the nucleo-cytoplasmic ratios in the rotifer, H ydatina senta, without finding any correlation between it and the mode of reproduction. Although it has been claimed that food, oxygen content, and other similar external factors influence the sex ratios of parthenogenetically produced animals, there is no good evidence that these factors are responsible. Banta thought the formation of an ephippium (winter egg, which develops upon fertilization) to be 330 PARTHENOGENESIS

due either to unintentional change in the media, in which parthenogenetic daphnids had been developing, or to overcrowding.

Another suggestion (which is so far merely record of an observation rather than a cause) relates to the lagging chromosome of the phylloxerans which is observed to accompany parthenogenesis. Peacock and Harrison working upon lepidopteran crosses reached the conclusion that parthenogenesis is a result of hybridity and later supported this conclusion by a study of the data of other crosses including Nabours’ experiments on parthenogencsis in Apotettix. finally Nabours, working upon Parateltirc, studied genetically two strains one of which was highly parthenogenetic and the other had never so reproduced. He obtained genetic evidence that parthcnogenesis is a character which segregates in a Mendelian manner and believes it due to certain genes. Robertson’s cytological studies on Nabours’ material fall into line with this hypothesis. The entrance of the sperm is necessary for the second polocyte division, and when it is lacking the diploid chromosome number is retained. In this latter case if the specific genes for parthenogenesis are present development is initiated. It is to be noted that Agar working upon Daphnia and Whiting upon Habrobracon failed to find genetic evidence of the cause of parthenogenesis. But Punnett as long ago as 1906 had suggested the probability that the question is concerned with the zygotic constitution of the egg and thought that it might be a matter of Mendelian segregation. These different hypotheses show the need of much further study of this most elusive subject.

B. THE OCCURRENCE or NORMAL PARTHENOGENESIS

Natural parthenogenesis is of much wider occurrence in the animal kingdom than is generally recognized, and it is not rare among the plants. Examples are found in the following groups of animals: rotifers, nematodes, trematodes, Dinophilus, three orders of Crustacea, myriapods, arachnids, and ten orders of insects. It seems desirable to point out some of the important studies in each of these groups, although no attempt can be made toward inclusiveness. For references and a more nearly complete listing of cases the reader should consult Winkler.

a. Rotzfera. Among the rotifers, as already described, typical arrheno— tokous parthenogenesis occurs in the same groups of animals with thelytokous parthenogenesis. The studies on Hydatina senta are among the best known of all studies on the type of reproduction. Three types of females, as previously indicated, are found here, and by experimental means it is possible to change the strains from parthenogenetic to bisexual. CRUSTACEA 331

b. Nematode. For the nematodes the case of Rhabdites aberrans as described by Kriiger has already been mentioned. The trematodes are commonly described as giving rise to rediae from cells which are segregated at one end of the body of the sporocyst and become an ovary. The new rediae arise from these so-called “ova,” which must be thought to develop parthcnogenetically if the view of their origin is maintained that these are true eggs. This controversial subject is discussed in other chapters in this work.

c. Annelida. Among the annelids parthenogenesis is suspected in Dinophilus conklini from the preponderance of females. In the leech Ilemiclepsis marginata the early finding of parthenogenesis has failed of confirmation in more recent experiments (Brumpt, 1900).

d. Crustacea. Two orders of the Entomostraca exhibit parthenogenesis and include in their number some cases that have been given a great amount of study, while a third offers a case which is suspected to be parthenogenetic. Among the Phyllopoda examples may be cited from both the Branchiopoda and the Cladocera. Of the former, Apus, Lepidurus, and Artemia are well known. Reference has already been made to Lepidurus because of its hermaphroditic relationships. Thelytokous parthenogenesis occurs in these forms. Artemia salina likewise has been mentioned in connection with geographic parthenogenesis. On this form the most recent studies are those of Artom (1912). Two polocytes are formed in the development of the egg. Regularly a reduction of chromosomes from 42 to 21 takes place. The parthenogenetic forms are tetraploid and of a type called somatic. There are therefore two strains of Artemia, one diploid and bisexual, the other tetraploid and thelytokous parthcnogenetic. The following explanation has been upon the basis of the very slight evidence that in the parthenogenetic strain only one polocyte is formed (Brauer) and that without reduction. If the egg and polocyte nuclei, both of which retained their somatic number of 42 chromosomes, should fuse, then an individual with the tetraploid number would be produced. As yet this explanation must be looked upon as purely speculative. Numerous others of the true phyllo« pods, such as Branchipus streptocephalus, have been observed to repro duce parthenogenetically and still others are suspected because of the scarcity or absence of males.

Of the work on the Cladoeera, which dates from Weismann’s studies in 1879, the general facts are well known. Bisexual generations are followed by parthenogenetic which may continue indefinitely. The various races differ greatly in the number of generations produced within a year and in the frequency of the bisexual forms. Apparently most if not all forms are parthenogenetic at some stage of their life cycles, but 332 PARTHENOGENESIS

those genera most studied have been Daphnia, Simocephalus, M oina, Bosmina, Chydorus, Polyphemus, and Leptodora, the first four being best known. The more recent students of the group include Olofsson (1918), Woltereck (1909-1911), Langhans (1911), Kuehn (1908), Chambers‘ (1913), Taylor (1914), Thiebaud (1913), and especially Banta and his co-workers, whose work is published in a series of papers beginning in 1914 and is not yet completed. In all forms the males are rarely seen and in some species are unknown. As already stated much of the work concerns the control of sex and the intersex conditions in these

forms. There is good evidence that sex ratios and intersex conditions are both subject to environmental influences.

In the order Ostracoda, parthenogenesis was discovered in 1880 by W. Mueller and by Weismann for a number of genera, it having been shown that virgin females produced eggs that developed into females; that is, produced a thelytokous race. No reduction division was found to occur by Woltereck (1898) or by Schleip (1909) for a considerable number of forms which they studied and parthenogenesis for these animals is therefore of the diploid or somatic type. In 1914 Wohlgemuth studied carefully the reproduction of numerous fresh-water ostracods and thought they fall into two groups, one of a purely bisexual and the other of a purely parthenogenetic type, although there are transitional forms between the two. Other investigators of the Ostracoda have been Menzel (1911), Alm (1916), and Olofsson (1918). Their chief concerns have been to describe the facts of parthenogenesis, the relation of the bisexual generation to the parthenogenetic, the duration of each and the conditions under which they occur. Not much of importance to an embryological account is gained from these forms, although SchIeip’s work on the various species of C3/pris offers perhaps the best cytological description of parthenogenesis in any crustacean form. His observation of synapsis not followed by reduction is worthy of note. It may be remarked that some of the studies of ostracods have taken up the question, raised for many Crustacea, as to the possible impairment of vigor of a strain due to long-continued parthenogenesis. Here as elsewhere among the members of the class the general consensus of opinion seems to be that no loss of vigor can be noted.

Mention should be made of the possibility of parthenogenesis in the third order of the Entomostraca, the Rhizocephala. In the genus Sylon belonging to that suborder Smith reported his complete failure to find males and so suspected that parthenogenesis is the method of reproduction.

In one order of Malacostraca parthenogenesis has been reported, INSECTA 333

namely in the Isopoda. Vandel (1928) has given an account of geographical parthenogenesis, already mentioned in Trichoniscus. Two races occupying different localities were described, one bisexual, the other exclusively parthenogenetic. In some places they may exist side by side, but mating does not occur between the two races. Physiological factors tend to keep the two races distinct and to increase the divergence between them. The parthenogenetic race is found to be triploid in its chromosome relations. The eggs of the parthenogenetic female do not undergo synapsis.

For both of the two Inyriapod groups, the Chilopoda and the Diplopoda, cases of suspected parthenogenesis are recorded. Of the former Geophilus and Lomyctes, and of the latter N opoiulus and Polyxenus, have been studied. All of these include races which either lack males entirely or in which they are to be found in certain localities only. In addition observations were long ago made by Sograff (1882) upon Geophilus proximus of which unmated females laid eggs that began to develop.

Among the spiders accounts of parthenogenesis have been reported for nearly a century and it may still be suspected, but Montgomery in 1903 concluded that it is “very rare among spiders, and it is probable that most species do not show it at all.” Since Montgomery’s finding, it does not appear that any work has been done which successfully establishes parthenogenesis in these animals.

Among the mites there is no doubt that parthenogenesis occurs, for Ewing (1914) described the process in the bisexual Tetranychus telarius and showed that the unfertilized eggs give rise to males exclusively. It is arrhenotokous parthenogenesis. Among the ticks, the Brazilian form, Amblyomma agamum, has been shown by Aragas (1912) to multiply by thelytokous parthenogenesis.

It has been conjectured by Hennecke (1911) that the tardigrade. M acrobiotus macronyx, has an alternation between parthenogenesis and bisexual generations.

0. I nsecta. Parthenogenesis is of very general distribution in the insects, having been described in the ten orders. The following table, compiled in part from Winkler, summarizes the occurrence of the phenomenon. For references to most of these cases the reader is referred to Winkler, but a few of especial significance are mentioned following the table.

Aptera

M achilzls. Heymons, 1-905 ; doubtful but could find no males. Forbicina. Verhoeff, 1912; all females, so no doubt parthenogenesis occurs. 334 PARTHENOGENESIS

Orthoptera Mantidae

Mantis religiosa Przibram, 1909; induced experimental parthenogenesis, Sphodromantis not natural.

Phasmidad

Eurycnema. v. Wuelfing, 1899; three generations of parthenogenetic females in Java. Hanitsch, 1902; two generations of parthenogenetic females.

Bacillus. Dominique, 1896-99; two thelytokous generations of parthenogenesis. Males are rare. Also Stadelmann, v. Bachr, Cameron, Daiber.

Dixippus. Pantel and de Sinety, 1908. Parthenogenesis established. Schmitz, 1906. Four generations of thelytokous partheno genesis.

Hammerschmidt, 1910. five generations of thelytokous parthenogenesis.

Jeziorski, 1918. Four generations of thelytokous parthenogenesis.

Phasma. Thurau, 1899. Only females.

M onandroptera P . Raphidems }Bordoz, 1913. arthenogenetic. Leptinia. de Sinety, 1900. Thelytokous parthenogenesis. Pantel and

Ucles also found parthenogenesis. Phyllium. Bordas, 1898. Suspected parthenogenesis.

Locustidae Saga pedo. Claus-Grobben, 1917. Report parthenogenesis. Gryllidae M yrmecophila acervorum. Schimmer, 1909, suspected parthenogenesis. Tettigidae fig Nabour and colleagues, 1919-1929. Thelytokous parthenogen' . B . Telmatemx esis est understood cases

Coleoptera. Parthenogenesis is of rare occurrence and most of the older accounts are not trustworthy.

Tropiphorus carinatus. Calwer, 1916, reported parthenogenesis. Otiorrhynchus turca. Ssilantjew, 1906 0. ligustici. Wassiliew, 1909 Thelytokous parthenogenesis. 0. cribricollis. Grandi, 1913 Calandra oryzae. Hinds and Turner, 1911, report parthenogenesis common. Eggs produce both sexes.

Strepsiptera Stylops}Brues, 1903 Xenos Nassonov, 1910 Elenchus. Muir, 1906

Parthenogenesis probable due to morphology of female genitalia. IN SECTA 335

Thysanoptera

Most species are bisexual. Many may multiply parthenogenetically. The1ytokous parthenogenesis is established for Parthenothrips, Anaphothrips, Heliothrips, Taeniothrips, and Liothrips; for a number of others it is probable. Arrhenotokous parthenogenesis is experimentally shown for Antlwthrips verbasci.

Corrodentia Ectopsocus. Ribaga, 1904. Probably parthenogenetic.

Hemiptera

Aleurodes. Morrill and Back, 1911. Arrhenotokous parthenogenesis.

Trialeurodes. Schrader, 1920. English race thelytokous. American race ar rhenotokous.

Aphididae. Many species of Aphis are known to be parthenogenetic and types vary. In north they reproduce bisexually during colder seasons but in south may be exclusively parthenogenetic.

Other genera include Callipterus, Ceratophis, M acrosiphum, M yzus, Pemphigus, Rhopalosiphum, Schizoneura, Toxoptera; Chermcs, Pincus,Phyllozera.

Coccidae. Many genera of scale insects are described as parthenogenetic although some cases are not known. Included are Aspidiotus, Ceroplastes, Cryptococcus, Diaspis, Eriopeltis, Lecanium, Lep1.'dosaphes, Orthezia, Parthenolecanium, Pseudococcus, Pulvinaria, Saissetia.

Lepidoptera All proven cases belong to family Psychidae or are closely related to it. Acanthopsyche, Pachythelia, Psyche, Sterrhopteryx, Phalacropteryx, Apterona, Cochlophora, and Lufia are included. The best known is Solerwbia liclwnella. Hoffmann, 1859.

Solenobia triquetrella. Hofimann, 1859-1869. Usually bisexual. Both bisexual

and parthenogenetic modes described. Geographical parthenogenesis. v. Seibold, 1871; Rolph, 1884; Rebel, _1906; Dampf, 1907; Seiler, 1918. Solenobia pineti

Diptera. Parthenogenesis seldom found in this group.

Chirmwmus. Godlewski, 1914. Paedogenesis and parthenogenesis intermingled. Corynoneura. Goetghebeur, 1913. Rarely parthenogenetic. M etriocnemus. Picado, 1913. Males few in number.

Hymenoptera. Six families show parthenogenesis.

Tenthredinoidea The following show thelytokous parthenogenesis: Albia fasciala ' Allantus pallipes

Allantus canadensis Amauronematus puniceus 336 PARTHENOGENESIS

Amauronematus semilacteus Phyllotoma aceris Caliroa limaama Phyllotoma nemorata Cimbex connata Pontania capreae Croesus varus Pontania viminalis Emprfu abdominalis Pristiphora pallipes Empria pulverata Pristiphora fulvipes H emichroa alml Pteronidea spiraeae Hemichroa crocea Pteronidea tibialis Nematus erichsoni Thrimax mixta

Pachynematus obductus The following are probably thelytokous:

Caliroa aethiops Selandria stramineipes Phyllotoma vagans Strzmglylogaster lineata Producing both males and females are: Ametastegia equiseti Pseudoclavellaria amerinae The following are arrhenotokous:

Albia nitens N ematus luteus

Allantus cinetus Periclista albida Allantus viennensis Phymatocera aterrima Ametastigia glabrata Priophorus padi

Arge, all species Pristiphora conjugate Caliora annulipes Pristophora crassicornis Cladius Pristiphora geniculata Croesus brischkei Pristiphora testacea Croesus litipes Pristiphora alnivom Croesus septentrionalis Pteronidea, 15 species Lophyrus, all species Trichiocampus viminalis Nematus coeruleocarpus Trichiocampus lucorum

Cynipoidea.

The following genera contain species which are parthenogenetic and in most cases the males are unknown, so they are probably thelytokousz

Andricus ' Cynips Rhodites

Aulacidea Drastrophus Dryophania Ceroptres Phanacis N euroterus

Ichneumonoidea Chalcids

The following are arrhenotokous:

Ageniaspis Entedon Paracopidoswnopsis Anaphmldea Litomastix Pentarthron Copidosoma M elittobia Pteromalws Encarsia M icrtmzelus Schedius

Encyrtus M icroterys Tropidopria IN SECTA 337

The following are thelytokous:

Asphclinus Coccophagus Tetrastichus Aspidiotiphagus Odtetrastichus Tripoctenus

The following contain species that produce both sexes or are uncertain as to sex although parthenogenetic:

Eupelmus I sosoma Scutellista H abrocytus Paniscus Trichogramma

Braconids: All parthenogenetic species are described as arrhenotokous.

Ichneumonids: All parthenogenetic species produce mixed broods.

Proctrotrupids: Anagrus, Gonatopus are thelytokous. Balus, Paranagrus, Phanurus produce mixed broods, or first females then later males.

Doubtless many more parasitic hymenoptera are parthcnogenetic.

Formicoidea

Arrhenotokous parthenogenesis is very widespread among the ants. Many workers are fertile and lay unfertilized eggs from which males develop. Some hold the view that both males and females may develop from parthenogenetic eggs. A few cases are recorded in which thelytoky is claimed to be established. Certainly it is much less common than arrhenotoky.

Vespoidea

Parthenogenetic eggs of queens and workers develop into males only. Examples are Polistes gallicus, v. Seibold, 1871 Vespa germanica, Marchal, 1896

Apoidea For many bees arrhenotokous parthenogenesis is conclusively established. Haploid males are so produced, and diploid males probably do not occur, that is, males produced from fertilized eggs, although that possibility has not yet been excluded. In a few genera both males and females are produced

parthenogenetically but this is not usual. Queens and workers are females produced bisexually.

As is to be seen from the preceding table, a great deal of work has

been done upon insect parthenogenesis. It has, however, been to a large extent concerned either with the general life cycle or with the cytological and genetical aspects of the problem. Many studies of very fine character have been made upon gametogenesis and sex determination, and upon the factors involved in the control of sex. Of recent years the problems which are bound up with uniparental inheritance have attracted much attention. It must be admitted that much of this work has not advanced our general embryological knowledge of the insects to any great extent.

Among the many investigations may be mentioned a few to which 338 PARTHENOGENESIS

the reader is referred if he would pursue further these aspects of the problem. The work of Nabours and his collaborators upon the various forms of grouse locut promises much in the cytological analysis since grasshopper chromosomes are among the most favorable for study. The saw flies have been studied especially by Doncaster and by Peacock and Harrison. Of the aphids and phylloxerans a very careful cytological study was made by Morgan. An earlier study by Tannreuther is a good account of the general embryology of the aphids. Parthenogenesis in the moths is most recently made known to us by the studies of Goldschmidt and of Seiler. Of the Hymenoptera the extensive work done by Patterson on Paracopidosomopsis will serve to introduce the student to the relation of parthenogenesis and polyembryony, and the best detailed account of the cytology of the bee is undoubtedly that of Nachtsheim. Other investigations have already been mentioned in connection with other aspects of the general parthenogenesis problems.

f. Plants. Among plants a considerable number of cases of parthenogenesis are already known and it is thought of interest to mention the conditions found there in this discussion although the problems involved are outside the scope of this work. It is difficult without careful study among the plants to distinguish between cases of parthenogenesis and those of the simple vegetative apogamy. Among higher plants haploid parthenogenesis is exceedingly rare, although several cases have been described for the lower forms. Haploid parthenogenesis is also described as generative parthenogenesis by Winkler and as true parthenogenesis by Strasburger. Diploid parthenogenesis is less common among the lower forms but more so among the vascular plants. It is due to the failure of the maturation process to occur to completion. The forms which are known to be parthenogenetic are as follows:

Haploid parthenogenesis: Spirogyra, Ernst, 1918; Vaucheria, von Wettstein, 1920; Ectocarpus, Kylin, 1918; Fucus, Overton, 1912 (probably haploid); Gastrodia, Kusans, 1915; Oenothera, Haberlandt, 1921, 1922; Datura, Blakeslee and Belling, 1922, evidence from breeding experiments; Nicotiana, Clausen and Mann, 1924.

Diploid parthenogenesis: Chara crinita, Ernst, 1918; Athyrium fel2':cfoemina, var. clarissima, Farmer and Digby, 1907; Scolopendrium vulgare, Farmer and Digby, 1907; Marsilia Drummondii, Strasburger, 1907 ; Allium odomm, Haberlandt, 1923 ; Atamosco texamz, Pace, 1913; Calycanthus, Schiirhofi, 1923; Alchemilla, Murbeck, 1901, Strasburger, 1905, Boos, 1917; Wikstroemia, Winkler, 1906; Eupatorium glandulosum, Holmgren, 1919 ; Erigeron annuus, Tahara, 1921; Antennaria alpina, Juel, 1900; Chondrilla, Rosenberg, 1912; Taraxacum, Juel, 1904, Osswa, 1913, Sears, 1922; Archieracium, Rosenberg, 1917. ARTIfiCIAL PARTHENOGENESIS 339

II. ARTIfiCIAL PARTHENOGENESIS

Of great embryological significance is the phenomenon of artificial or experimental parthenogenesis. It has been the subject of much of the work on experimental embryology of the present century and its chief consideration should be a matter for a treatise on experimental embryology. However, its importance for an understanding of matters which have to do with the normal embryological process is so great that a brief account should be included here. For details and bibliography the reader is referred to the extensive accounts which have been published by Loeb (see his “Artificial Parthenogenesis and Fertilization”) and by Morgan in his “Experimental Embryology.” Wilson has also critically considered the cytological aspects of the problems concerned with artificial parthenogenesis in “The Cell.”

The student should be reminded of the double function which fertilization serves in normal development; the one is hereditary in character in that fertilization provides the mechanism for conveying the contribution of the male to the offspring. The other is strictly developmental in that it sets in motion those processes which have been inhibited or are latent in the egg at the time of maturation. It is with this second aspect of fertilization that experimental or artificial parthenogenesis deals. These experiments have sought to imitate and to interpret the normal processes of development as initiated by fertilization, and because of that a much clearer understanding of the normal process has been reached. The experiments have shown that it is possible to cause the unfertilized egg of a great many animals to develop into larvae largely under the influence of chemical treatment, although physical means have also been used to accomplish the same end less perfectly.

The work on parthenogenesis is chiefly a monument to the insight of Jacques Loeb and his analytical experiments have been of the most importance in solving the many problems involved. However, numerous other students have contributed to the progress of the work both before and since his announcement of the discovery that it was possible to induce eggs to develop artificially. Among the preliminary studies which antedated Loeb’s discovery in 1899 may be mentioned the paper of Loeb himself in 1892 in which he studied the effect of addition of sodium chloride to the sea water in which the eggs of Arbacia developed; Richard Hertwig’s observation (1896) on the effect of treating unfertilized sea-urchin eggs with strychnine; a series of experiments by Morgan (1896, 1899, 1900) on the effect of salt solutions on the segmentation of eggs and the formation of artificial asters; the work of Mead (1896-98) showing that unfertilized eggs of Chaetopterus will 340 PARTHENOGENESIS

form polar bodies in certain solutions in which the amount of sodium chloride is increased. Loeb’s papers upon this subject are many, and to him is due the chief credit for the developing of our knowledge of the subject. Ampng those who early worked upon the problem was Delage, who in a series of papers from 1900 to 1913 added a great deal to the understanding of this difficult subject; he succeeded in rearing through metamorphosis the larvae of both sea-urchins and starfish which had been induced to develop by artificial parthenogenesis. Loeb and Bancroft (1913) brought a parthenogenetic frog through metamorphosis and found that its sex glands contained eggs. Shearer and Lloyd (1913) succeeded even better than Delage in bringing parthenogenetic larvae of Echinus through metamorphosis, and more recently (1918) Loeb has brought a considerable number of parthenogenetic tadpoles to the adult stage. It is to be noted, however, that only in the case of frogs has it been possible to imitate in the laboratory the conditions of nature sufficiently to bring animals developed by parthenogenesis to sexual maturity. Since Loeb’s work, Bataillon, R. S. and F. R. Lillie, Goldschmidt, Gray, Harvey, Heilbrunn, Herbst, Herlant, and Just are among the many who have made extensive studies into the embryological phases of artificial parthenogenesis.

VVhen one begins to consider the significance of artificial parthenogenesis he is at once led to inquire as to how general the phenomenon is or how generally it may be expected to be possible in the animal kingdom. It may well be that eggs are so constituted as to permit their development without fertilization, at least into the cleavage stages, and that we are merely unable to understand the requirements in each case and to devise the correct procedure. A broad generalization of this character is hardly safe, however, for up to the present time the only forms in which it has been possible to induce experimental parthenogenesis are those in which the experiment is relatively easy to perform. In every case the eggs are of the type which is shed freely into the water. The difficulties of the experimental work which is involved may be the reason for this limitation or it may be that a deeper limitation is operative so that eggs which are adapted for other kinds of development may not be stimulated to cleave artificially. Thus far the following groups have responded to the treatments that have been devised to induce parthenogenesis artificially. By far the most work has been done on the sea-urchins. Arbacia, Strongylocentrotus, T0:copneus'es, and Paracentrotus have all shown themselves excellently adapted to experiments of this type and they have been used for much important work, especially the first two mentioned. The sand dollar, Echinarachnius, has proved adaptable for similar experiments. Among the starfishes ARTIfiCIAL PARTHENOGENESIS 341

the eggs of the commoner species of Asterias as well as some of the more unusual starfishes, as Asterina gibbosa, have been used successfully. It is to be noted, however, that the methods which have proven most successful with the sea—urchin give but very poor results with the starfish, and conversely little success has been obtained by applying the two best methods of inducement for the development of the starfish egg, namely, carbon dioxide and mechanical shaking, to eggs of the sea-urchins. The eggs of the frog, Rana fusca, have often been induced to develop by parthenogenesis, and the most successful treatment has been again a mechanical one, namely the simple pricking of the surface of the egg. Various annelids have been studied, especially Chaetopterus, Amphitrite, Thalessema, but the best results in this group have unquestionably been gotten for the eggs of Nereis. Here again the means of inducing parthenogenesis is physical rather than chemical, namely, the subjecting of the egg to heat.

A second question arises in attempting an embryological interpretation of the experiments in artificial parthenogenesis, namely, do these experiments produce animals that are fairly normal. As already pointed out Loeb’s own studies led him to the belief that “parthenogenetic larvae may be normal and apparently healthy,” and indeed, he said, “if the raising of the larvae was not such a tedious process parthenogenetic animals would exist today in large numbers.” His methods have certainly produced, both in his own hands and in those of other investigators as well, larvae which resemble the normal in every particular, and Delage, Shearer, and also Fuchs were able to bring parthenogenetic larvae to adulthood. The chromosome relations of the individuals as produced, however, have not been made out with certainty as yet and it is still doubtful whether haploid larvae produce normal adults. Parmenter (1925) has shown that in the larval and adult stages Loeb’s parthenogenetic frogs have the diploid chromosome number. The direct evidence is entirely lacking as to whether the adults produced from diploid larvae can themselves produce offspring. It should be said that most investigators are of the opinion that the parthenogenetic larvae which are experimentally produced are not merely normal in appearance but that they really are in every respect what they seem, that is, normal animals.

‘Loeb developed a theory of parthenogenesis as a result of his experiments, and what he spoke of as his improved method is based upon that theory. According to his View the formation of the egg membrane is the deciding criterion by which the initiation of development may be recognized. Indeed he traced a causal relation between the formation of the egg membrane and the subsequent development of the egg and 342 PARTHENOGENESIS

attached much more importance to this process than had previously been done. Membrane formation is the deciding condition of development. Not all later workers have agreed with Loeb in this view, but unquestionably his explanations have not been out of harmony with the facts which he observed.

The so-called improved method of Loeb for inducing artificial parthenogenesis consists of two steps. Its details as to concentration and length of exposure must be worked out for the particular species of sea—urchin eggs used and indeed different individuals will respond differently so far as the duration of the exposures are concerned. With regard to these points the method is entirely an empirical one. The

procedure as worked out for Arbacia eggs is as follows: Unfertilized

. . . . N . eggs are placed in a sea water mixture containing 2 cc. of T6 butyric

acid to 50 cc. of sea water. Apparently any monobasic fatty acid would

serve equally well for this purpose but Loeb found butyric to be satis N factory for the experiments (2.8 cc. of I5 butyric were necessary in the

case of Strongylocentrotus purpuratus eggs). The duration of the exposure must be brief, from 1% to 3 mintues. The eggs are then transferred to normal sea water and after 10 or 15 minutes to hypertonic sea water consisting of 8 cc. of 2% M NaC1 to 50 cc. of sea water. At a temperature of 23° the eggs must remain in this solution from 17% to 25 minutes after which they are transferred to normal sea water. The effect of this double treatment has been shown many times and in many different localities. A very large percentage, usually about as great as is obtained from the development of fertilized eggs, go ahead with the cleavage process and develop to larvae; doubtless the inability to rear the larvae is not in any way due to the fact that they were parthenogenetically produced.

The explanation of this double procedure has been a matter of some discussion. Loeb believed that membrane formation sets going certain chemical reactions upon which the future development of the egg depends. These chemical reactions, however, leave the egg in a condition from which it will not itself recover, and unless a second factor is employed in the process it will disintegrate rapidly. These reactions are on the nature of oxidations and are at least to a certain extent cytolytic in nature. The second factor is therefore necessary as a corrective to regulate the extensive oxidization which is produced by the exposure to the first solution. Loeb’s conclusion that cytolysis must take place unless corrected by the hypotonic solution has been questioned by some ARTIfiCIAL PARTHENOGENESIS 343

later experimenters, notably by Just, who has been able to induce the development of normal plutei of Arbacia by the use of hypertonic solutions alone. The exact preparations of the salts which are used to render the sea water hypertonic and the durations of the exposure to this mixture must be regulated with a great exactness if successful results are obtained. His optimum solution is made up of 22 parts of 2% M NaCl or KCI plus 78 parts of sea water, although variations from this mixture were also used. Of course great care was used to control the experiment in every way necessary. Eggs subjected to a treatment with this solution form membranes while still in the solution. Subsequently the eggs are returned to sea water and their development proceeds. Upon the basis of these experiments Just holds that the treatment with the fatty acid is not necessary and therefore that the hypertonic sea water is not serving as a corrective to stop the cytolysis induced by the unusual step in Loeb’s procedure. He is disposed to relate the activation of the sea-urchin eggs by this treatment to the egg secretion, fertilizin, which is given off by the unfertilized eggs into the sea water and which has been shown to be a necessary intermediary to normal fertilization with sperm. Just suggests that the activating agent which will accomplish experimental parthenogenesis serves to bind the fertilizin produced by the egg and thus to complete the necessary cortical changes whic}

must take place if development is to proceed. The full explanation or the artificially induced changes has perhaps not yet been offered with regard to the experimental facts. However, there is no question that the

entire subject has been one of the most successfully studied of all problems of experimental embryology. CHAPTER VI PAEDOGENESIS AND NEOTENY

A series of conditions is known that have to do with the early sexual maturity and reproduction of certain animal forms which otherwise retain their youthful characteristics. These are to be taken up under the general heads of paedogenesis and neoteny although not all the cases included come under a strict definition of either of these terms. They occur in a great many widely scattered groups of the animal kingdom and present a great many variations some of them so wide that they are scarcely to be recognized as of related processes. When such diverse conditions appear, it goes without saying that confusion is to be found in the literature dealing with them. Regarding the processes under consideration in this chapter exactly such confusion is found, some writers using the terms loosely and failing to classify with sharpness the cases cited.

The biogenetic law comes into the discussion for the reason that one may regard a particular phenomenon as recapitulating past phylogenetic conditions, or he may look upon the animal showing it as exhibiting neoteny, at least of the characters in question, and perhaps generally. Thus the familiar axolotl which is the sexually mature, unmetamorphosed Amblystoma is the usual example of neotenous development, but it is also cited by the proponents of recapitulation as explained by the general progress in development of the Proteus, Necturus, Amblystoma, Salamandra series of urodele recapitulation. Most of the cases of this kind, however, are concerned with adult conditions quite as much as with those of immature forms and therefore would seem to be rather outside the scope of the present discussion.

The general subject of neoteny also calls up the problems of heterochrony, by which is meant a disturbance of the synchrony of development. That is, if one might take the normal series of developmental time stages with each organ in its proper relation to the others as a standard, representing perhaps the phylogenetic series, then any departure from this standard would be spoken of as heterochrony. (See also Chapter III, Part Two, for discussion of heterochrony.) Similarly, the sequence of embryonic events when disturbed, as in neotenous development, involves heterochrony. The principle is one with an

344 PAEDOGENESIS AND NEOTENY 345

interesting history, recalling especially the work of two investigators, Oppel and Keibel, although many others have contributed to it, some independently and others in collaboration with Keibel in the publication of his famous “Normentafeln zur Entwickelungsgeschichte der Wirbeltiere.” Oppel began this study comparing the different developmental stages of different animals and arranging them in tabular form to show the comparative progress of the most important organs of vertebrates. He thought himself to have found similar ontogenetic stages and to be able to compare the young stages among themselves as well as the adults among themselves. The recapitulation doctrine found support in his Work in that the young stages of higher forms are similar to the older stages of the lower animals. Departures from the series thus established were to be attributed to heterochrony. Keibel as a result of his studies and tables concluded that the time of the appearance of an organ is dependent upon the time at which it will be required to function. Thus the order of appearance of organs in a developmental series is of itself of phylogenetic significance. But Keibel did not recognize the biogenetic law as valid in these cases.

Another early student of heterochrony in vertebrates was Mehnert, who devoted his attention particularly to the relation of the subject to recapitulation. His view on this matter is of interest, for he thought that only the early development of an organ had recapitulatory value in any precise fashion, whereas in later stages the processes are quite schematic. He studied also organs which undergo regression as well as those whose development is only progressive. Heterochrony he found to be due (1) to precocious development of an anlage, (2) to rapidity of growth, (3) to rapidity of histological differentiation, and (4) to abbreviation or omission of intermediate stages. Retardation of these processes as well as their acceleration call forth heterochrony.

Heterochrony is thus seen to deal with parts of organisms rather than the animal as a whole and to-show the effects of disturbances of developmental rate and rhythm upon the entire animal only through its effect on its component organs. At first thought paedogenesis might be considered as but very indirectly concerned with a matter such as this, but a reconsideration of the facts easily brings out a very clear relation, for we find paedogenesis to mean merely that, in an animal exhibiting this phenomenon, the organs of the body which have to do with reproduction have been much accelerated in development, while at least some other parts of the body have failed to keep up the pace set by these organs; or in some cases we must think that the reproductive organs and related parts have retained their customary pace while the others have been very considerably inhibited. 346 PAEDOGENESIS AND NEOTENY

During the present century many investigators have contributed to the knowledge.of the general subject. It will perhaps serve as an illustration to point out the importance of Stockard’s very extensive study on the development of Fundulus, particularly with regard to the effect of changes in the rate and to the various means by which abnormalities may be produced, notably by temporary arrests of development.

It is thus clear that the matters which are the subject of this chapter really constitute but special cases of heterochrony. In assigning to these phenomena as a causal factor the disturbance of the speed of development, we bring them all into one category. It is sometimes difficult to decide whether one organ has undergone a retardation of development or whether another is accelerated with respect to the normal and so it has not always proven easy to separate sharply the processes which are involved. By some, especially Giard, Chun, Kollmann, and others, fine distinctions have been drawn, the need for which is not entirely clear if we but relate the different processes to heterochrony.

By paedogenesis is meant sexual reproductive maturity in a pre-adult stage; it is of two types, parthenogenetic and bisexual. As a special form of paedogenesis, Packard has given the term “chrysallogenesis” to a case in which the pupa of Chironomus has been found to lay eggs.

By progenesis is meant the permanent retention on the part of the somatic structures of the conditions reached at the time when sexual maturity is attained.

Neotenous organs have youthful characters although the animal possessing them has developed its adult condition. Or, to put it in another way, animals with neotenous organs retain the ancestral larval conditions in the particular structures which show neoteny.

Disogeny is the “sexual maturity of one and the same individual in two different conditions, between which a metamorphosis with retrogression of the sex products occurs” (Chun).

It is true that these definitions savor of dogmatism and of course require much elaboration. It would seem, however, that neoteny and progenesis are not far apart and that paedogenetic animals may easily exhibit disogeny. It will perhaps be best for the purposes of our present discussion if we limit ourselves fairly sharply to the cases which illustrate neoteny and paedogenesis. Of these there are certain classical ones which should receive especial attention. There are only a few of these cases in which the animals as a whole are spoken of as paedogenic or neotenous, but when we come to consider the organs to which the latter conception in particular may be applied, the illustrations abound and important explanations of obscure phenomena have been worked out on this basis.

Of all the cases undoubtedly the axolotl is the best known. As already PAEDOGENESIS AND NEOTENY 347

stated, Amblystoma tigrinum occurs in two forms, the one of which is technically immature, although it is sexually active. This paedogenic form was first described from the lakes about Mexico City and was thought to belong to the genus Siredon (S. lichenoides). The relation of this form to the well-known salamander was only discovered accidentally in Paris in 1865. Sexual maturity is reached at six months of age and sex products are shed. This is paedogenesis, for the animals have not yet lived long enough for metamorphosis.

However, metamorphosis may never occur. In many high mountain lakes axolotls live their entire life without undergoing the necessary


Fro. 218. External views of an axolotl (A) and an Amblystoma showing difierences of gills. body form. and leg development.

changes to transform them into Amblystoma. The reason for this is not clear. If the animal be fed on thyroid, if it be forced gradually to leave the water and adopt a land life, if it be transferred from deep to shallow water, from cold to warm, or if it be brought into the presence of certain chemicals it will undergo metamorphosis promptly, but the causal mechanism is not yet understood. If it remains in the same environment as that in which it became paedogenetically mature, however, it will live its entire life without metamorphosis. This is neoteny, for the larval characters are retained long after the normal time.

The neotenous animal differs in a number of important characters from the type form. It has large external, red gills with gill slits, its tail is long and broad but flattened laterally so that it is adapted for swimming, and the body features are those of a water-living animal. Internal conditions likewise show immaturity, the skull bones, for example, never becoming properly developed. With metamorphosis the animal 348 PAEDOGENESIS AND NEOTENY

undergoes a very extensive transformation. It loses its gills, its legs develop for crawling upon land, and the tail becomes rounded and tapering. It is now a land salamander resorting to the water only for egg laying.

The neotexiy of axolotl is thus facultative, for with the proper conditions the animal does not remain neotenous but becomes an adult Amblystoma. Other urodeles, the perennibranchiates, correspond in their adult structure very nearly to axolotl and may be looked upon as permanently neotenous. Typhlomolge, of the underground streams of Europe and Texas, Proteus, Necturus, and Siren, belong to this group.

Another illustration from the chordates is the tunicate group called Appendicularia or Larvacea. These animals are small tadpole-like creatures averaging about half a centimeter in length and living perhaps one year. They swim in the surface waters of the sea of all parts of the world and the young have been taken in plankton between February and summer, but their development is almost unknown. There is no evidence of reproduction by budding, gemmation, or other modes of asexual type such as are found in the Salpidae, for example, nor is any metamorphosis known. Development is direct and the small appendicularia correspond in a general way to the tailed larvae of the ascidians; that is, they retain the tail portion of the body with its typical chordate characteristics which is lost in the metamorphosis of the more familiar forms such as Molgula, Ciona, Cynthia, etc. Hence the group has been named Larvacea and the animals have been looked upon as larval forms which have become sexually mature. They have also been looked upon by some as primitive forms from which other Tunicata have been derived, and, it must be noted, by some they have been thought of as larvae of some adult form which is pelagic. In any case the sex glands are developed and the products shed by the animals as known to us, and we have a clear case of neoteny.

Among the insects a number of cases are known, and some of these are among the most important of all for they illustrate parthenogenetic paedogenesis. The example usually given is M iastor, a cecidomyiid fly, but certain species of the genus Cecidomyia also show it. The case of M iastor has long been known as an illustration of paedogenesis, and is given by Hertwig along with certain other Diptera as an example proving his statement that paedogencsis is parthenogenesis in an immature organism. As is already seen, this statement is much too restricted, for the term paedogenesis is of equal application to cases in which inheritance is biparental.

In Miastor paedogenesis occurs normally during the spring, early summer, and autumn, according to Hegner who has been the principal PAEDOGENESIS AND NEOTEN Y 349

student of this genus in America. No reproduction takes place during the winter, and the process is interrupted in midsummer by the appearance of male and female adults. The larva of Miastor possesses two ovaries in the tenth and eleventh segments. In each are thirty-two

oocytes each with nurse cells and follicular epithelium. After a time one of these oocytes with its nurse cells and its follicular epithelium is separated off from the rest of the ovary and in a distant part of the body grows and develops at the expense of the tissues of the mother larva. This process is repeated until five to seventeen separated growing oocytes are thus produced from one mother larva. Then one division takes place, the polar body which is given off divides again and both products degenerate. Parthenogenetic cleavage follows with chromatin diminution as previously described in connection with the history of the germ cells, the pole plasm is segregated and the embryo gradually takes on its characteristic form. No oviducts are present in the mother larva nor is there provision for the escape of the young thus paedogenetically produced. They escape by rupturing the body wall of the mother larva, which is left to die. After the production of a number of generations in this manner, the last larvae pupate and emerge as normal adult males and females.

In the spring of 1869 Grimm found a pupa of Chironomus laying eggs. To this form of paedogenesis in the chrysalis Packard gave the name chrysallogenesis, although the differences from other types of paedogenesis are so slight as to make the retention of the term of doubtful necessity. In the autumn other pupa change to flies without laying eggs and these adults are more prolific than the spring pupae were. The process was described as a seasonal phenomenon depending upon temperature.

Pacdogenetic reproduction has also been reported for the Tenthredinidae, the saw flies, thus extending this phenomenon to a second order of the insects, the Hymenoptera. '

The molluscs show one case of neoteny in the shell-less snail, Stamedorsia verrucosa, which according to Cuénot reproduces long before true adulthood is reached.

Among the trematodes paedogenesis is found in the most striking form. Two excellent illustrations occur in the suborder Monogena, and conditions in the Digenea offer material for interesting speculation. In the former group the genus Gyrodactylus exhibits what is perhaps the nearest approach to the old preformationist theory of “emboitement” to be found in the animal kingdom. The young individual comes to sexual maturity before it is born and produces young in its own uterus. 350 PAEDOGENESIS AND NEOTENY

This process is repeated and as many as four generations have been seen, one within the other.

The second case of this group is that of Polystoma integerrimum originally described by Zeller in 1872. The embryo hatches in the water and swims Freely. It seeks for a young frog tadpole which it must find within twenty-four hours or die. If one is found it creeps over the surface until it finds the branchial opening, which it quickly enters; it undergoes metamorphosis, and passes down the alimentary canal to the rectum and thence to the urinary bladder. Here it remains for three years to become sexually mature. However, it may happen that the young worm has attacked a very young tadpole which still has external gills. In this case it remains in the gill chamber where nutriment is abundant, grows rapidly, and becomes sexually mature in the short space of five weeks. It does not then pass further along the alimentary tract but dies before the metamorphosis of its host. It differs in its structure as well as its life cycle from the usual form, in that it develops but one male gland instead of several, and it lacks entirely the intromittent organ, vagina, and uterus, or they are developed only to rudimentary vestiges. It is of interest to note that Polystoma ocellatum is structurally quite similar to the paedogenetic P. integerrimum.

Among the digenetic trematodes the life cycle of the liver-flukes involves questions which are of interest in this connection. The main facts are well known and are referred to in several chapters of this work. In both rediae and cercariae reproduction may take place and daughter rediae, and daughter cercariae may be produced. If it can be shown that these daughter forms are produced from eggs, either parthenogenetically or bisexually, then this is a case of paedogenesis. However, it has lately been shown for some flukes that the germ balls from which the daughter larvae develop are budded off asexually and never undergo any chromosome reduction (F. G. Brooks), so that for these forms at least it cannot be said that paedogenesis occurs in the flukes. It has been the usual view, however, that there is here the production of parthenogenetic ova, and hence paedogenesis.

Of the examples usually recognized, the final one is that of the lobate ctenophore, Bolina hydatina. Here the cydippid larvae become sexually mature, producing eggs and sperm. Fertilization follows and the eggs develop in the regular manner. The larval gonads subsequently degenerate, metamorphosis takes place, a new set of gonads appear, the animals again attain sexual maturity, producing eggs and sperm, this time as adults.

These are the classical cases, and they illustrate both neoteny and paedogenesis, both parthenogenetic and bisexual. PAEDOGENESIS AND NEOT ENY 351

In addition to these, experimentally produced delay or acceleration of development are well known. Frogs transferred as larvae to alpine heights where the winters come early have remained in the larval condition over the winter. High temperatures hasten sexual maturity. Brackish water or fresh water will often hasten the maturity of oceanic forms. Hunger in some forms and overfeeding in others result in heterochronic growth. Termites which are fed in a certain manner mature very early while the wings are still undeveloped and eyes have not yet appeared (Grassi). Parasitism may be looked upon as a strong factor accelerating maturity because of the abundant food supply.

It may be observed that there have been omitted many cases of larval budding and other forms of asexual reproduction such as may be so commonly found, for example, among jellyfishcs, liver—flukes, bryozoa, and tunicates. These cases, though not a far step from the types discussed in this chapter, are not properly considered here, for paedogenesis and neoteny are matters of sexual reproduction. It is admitted that in some cases, as already shown for the 1iver—flukes, the distinctions are hard to draw, but for the sake of clarity it is usually thought wiser to adhere to the definitions given.

Thus far we have discussed this subject from the point of view of the entire organism. There still remains the matter of neotenous organs rather than organisms which deserves mention before the subject is closed. This phase of the subject was developed by Garstang and by Bolk and recently discussed by De Beer. There are many instances in the animal kingdom of forms having organs that retain embryonic characters although the organism as awhole has passed on to a new adult condition. Organs of this kind are neotenous. In the succession of somatic stages the organs in question have fallen behind the others, in short they have become distinctly heterochronic. Bolk has discussed the features of man which resemble the structure of embryos of anthropoid apes, assuming that the latter‘are nearer the ancestral forms of structure. Among the features of man which show resemblance to the embryonic structures of the ancestral types, for which he uses the term foetalization, are the relatively high weight of the brain, the retention of the embryonic cranial flexure with the resulting erect posture as Bolk thinks to have demonstrated, the position of the foramen magnum, the late closure of the skull sutures, the flatness of the face, lack of hair on the body, and others. Bolk’s study of cranial flexure and human posture comparing both adult and ancestral conditions is particularly interesting. He finds as a result that the flat face as compared with the elongated muzzle of other mammals is largely responsible for the trend of human evolution with regard to vision and other special senses, the character 352 PAEDOGENFSIS AND NEOTENY

of the teeth and of the anterior end of the alimentary canal. And all the characteristics which are distinctly human are clearly neotenous and related to the embryological derivatives from the ancestors.

One other illustration, from those given by De Beer, may be cited to show the part that neoteny may have played in evolution. It is a comparison between the important structural characteristics of adult insects and larval myriapods. The larva of Iulus has a head composed of six or seven segments, an elongated segmented body, the first three metameres of which bear pairs of legs whereas posterior segments bear only rudimentary legs at the time of hatching or shortly thereafter (Metchnikoff). These features are quite insect like, in that the insect head has six or seven segments, the thorax three, each bearing a pair of legs, and the abdomen of about ten segments, legless or bearing appendages only as a larva. Insects are known among the lower orders whose structure corresponds more closely with this immature myriapod than does the structure of insects of the very specialized higher orders, and it is sug— gested by students of these matters that the ‘insect derivation passes through these intermediate forms from neotenous larvae at least not unlike those of the myriapods.

From these cases it would appear that the study of neoteny from the standpoint of embryology offers a productive field of quite a new order for investigations and that the conclusions reached from researches of this kind may profoundly affect our ideas of phylogeny. CHAPTER VII POLYEMBRYONY

By polyembryony is meant among zoologists the production of multiple embryos from a single egg. (This definition does not apply to botanical nomenclature.) The number of individuals produced from a single egg ranges from hundreds as in the parasitic Hymenoptera down to two, although in the latter case the condition is usually known as twinning, and not all types of twins are properly thought of as polyembryonic.- Polyembryony occurs very widely distributed through the animal kingdom in groups which are totally unrelated to each other. Because of this wide distribution the literature to which reference can be made in this connection is really very extensive and the significance of some of the cases extends beyond the realm of embryology. Of the numerous investigators who have studied the question only a few need be mentioned here, but it may be noted that a reference to their work will serve as an introduction to the much broader literature which is not included in this discussion. Patterson has summarized the knowledge of polyembryony in a paper in Volume II of the Quarterly Review of Biology and it is suggested that the student consult this paper in beginning a more extensive study of these problems.

Patterson recognized three types of polyembryony: “ (1) experimental polyembryony, or the production of multiple embryos by artificial means; (2) accidental or sporadic polyembryony, or the occasional production of multiple embryos in the species which is typically monembryonic; (3) specific polyembryony, or the habitual production of multiple embryos in a given species.” The general student of comparative embryology is interested in the last type much more than in the first two, although cases of the first two throw much light upon many fundamental problems of organization of the egg and embryo and offer a very stimulating field for the experimental embryologist. Many types of eggs whose normal development includes no hint of polyembryony can be induced to produce double monsters and even complete embryos by experimental means.

Cases of occasional or sporadic polyembryony are recorded for coelenterates, cestodes, annelids, echinoderms, arthropods, and vertebrates. Perhaps because the latter group is so much more studied, there

353 354 POLYEM BRYONY

have been more cases reported for the vertebrates than for the others and, as Patterson points out, it is here that the occasional identical twins of the human species should be classified.

Specific polyembryony, to which our attention is drawn as the special problem of the comparative embryologist, is found in the following groups of animals: flatworms, bryozoa belonging to the Cyclostomata, earthworms, parasitic Hymenoptera, and the mammals, especially as illustrated by the armadillo. It is of more widespread distribution, however, than is indicated by these groups, but here are included the more important cases.

An inspection of this list is sufficient to show that polyembryony has no phylogenetic or taxonomic significance, for the groups are too widely separated and too diverse in structure to admit of an interpretation of this kind. Moreover, the structural differences both of adults and embryos in these various groups are so great that it is not possible to look for the causes of the phenomena in any simple embryological process common to all. Doubtless in the final analysis all these processes have a common underlying causal factor which is bound up with the innate protoplasmic organization of the egg substance.

As Patterson has pointed out, it is really not much more strange for an egg to give rise to two embryos than to one. The remarkable fact is that a new organism can be produced from an egg at all, and those qualities of the living substance which make possible its reproduction are basic to the one case no more than to the other. We must recognize that specific polyembryony is as much a characteristic of certain animals as is the formation of a coelome. At a certain stage in development there occurs a series of events which lead perhaps to two buds, or more, from each of which individuals grow. Very little thought is necessary to convince oneself that the directive forces behind this type of budding are not much more astonishing than those which cause, in the other case, the archenteron to bud out to form an enterocoele.

A. THE Causns or POLYEMBRYONY

Of the explanations of polyembryony, probably the most prevalent is the theory of blastotomy, according to which the blastomeres of the cleaving egg become separated in the 2-, 4-, 8-cell stage or later, and lead entirely independent existences, each arriving at length at the stage of a completely formed embryo. This theory is the basis of the familiar explanation of the origin of identical twins in human beings, that the blastomeres in the 2-cell stage become separated and each gives rise to an embryo. This is a view with few observational data to support it, but it may be presumed to find considerable support in the THE CAUSES OF POLYEMBRYONY 355

experimentally induced development of isolated blastomeres. Numerous experimental devices are well known by which blastomeres can be separated. To mention only two of these devices as examples, it is possible more or less successfully to cut apart the blastomeres with a knife or delicate thread drawn about the egg, or to keep them apart by subjecting the eggs to calcium—free sea water in which the blastomeres do not cohere to one another. In some of these experiments the isolated blastomeres have lived and developed for a time; in others they have produced partial larvae (ascidians etc.); and in others they have developed into whole larvae (amphioxus, Cerebratulus). But in forms where direct evidence for blastotomy is possible none has been found which forces one to this view for cases of polyembryony. As will be seen presently, the facts in the armadillo make the explanation based on blastotomy untenable there, and render it highly doubtful elsewhere.

A second explanation takes the form of an assumption that polyovular follicles, that is, follicles containing several ova fused together, may provide the mechanism by which polyembryony is accomplished. It is only necessary to say that the evidence for this supposition is entirely insufficient and the theory may now be regarded as abandoned.

In the budding theory we have what is perhaps a closer correspondence with the observed facts, although it is more of a descriptive explanation than an attempt at developmental analysis. After cleavage there arise in the blastulae or gastrulae of lower animals or in the blastocyst of mammals certain areas or “growing points” which are essentially buds. If a single one is produced it becomes the apical or head end of a normal embryo and assumes dominance over the remaining parts. If two are formed they are the beginnings of twin embryos. Similarly secondary buds may be formed and four or more embryos result, depending upon the number of buds. The facts observed in the armadillo will be seen to harmonize well with this explanation.

This ‘theory of budding has been criticized rather severely, particularly by Assheton, on the grounds that budding cannot take place unless there is a stock from which the buds may arise and the presence of a stock Assheton claims was not demonstrated in the cases to which the theory was applied. Rather he interprets the described facts as cases of fission. The blastocyst of several mammals, for he was particularly considering the theory as applied to the armadillo, he described as undergoing direct fission into two embryonic rudiments. As a matter of fact the fission hypothesis does not differ from the idea of budding in relation to the facts as described, but is primarily a redefinition of them, for in both cases the embryonic vesicle is regarded as divided into several primordia, each of which is the beginning of a distinct formative area 356 POLYEM BRYONY

and consequently will give rise to a separate embryo. Whether the emphasis is placed upon the embryonic mass which is thought to bud or upon the separate areas which arise from it as would be the case in fission does not seem to involve any particular difference in the result nor to carry the explanation of the environmental processes much further toward a final analysis.

As an explanation of the process a physiological interpretation must be called on. Stockard has pointed out that if a developmental pause occurs at the critical moment in the formative stages of an embryo, a series of consequences ranging from simple malformation up to the production of double monsters or even two individuals may result. He applies this conception to the explanation of polyembryony, supposing that the reason for the loss of dominance of the first formative region of the embryo and the subsequent ascendency of the primary and secondary buds is connected in some way with the developmental pause. He points out that in the armadillo a period of physiological isolation intervenes at one of the critical moments, making possible the four resultant buds. Certain observed facts bear out this conclusion. In any case within the growing germ the isolation of formative areas occurs and from these formative areas the multiple embryos are produced.

An obvious connection exists between the phenomenon of polyembryony and that of metagenesis which involves at least the alternation of one sexually produced generation with an asexually produced one. It is usually the practice to limit alternation of generations to the lower forms of animal life and to say that it does not occur in higher forms, including the vertebrates. Stockard, however, speaking in terms of the budding hypothesis, has pointed out the fact that the embryonic mass of cells may be looked upon as one generation, namely the one produced from the fertilized egg, and that it is completed when it becomes a stock from which other buds, that is growing points, begin their development. This point of view has its application even to mammals whether only a single organism results or several as in the case of the armadillo. Here the blastocyst would be regarded as the sexually produced individual and the buds which give rise to the four young as those asexually produced from it.

Stockard says, “From a general biological standpoint the adult body of higher animals may be very correctly considered to be derived from a sexually produced embryonic axis, the stock which gives rise by an asexual method of budding to the various special organs. The vertebrate body is thus composed of a group of different zooids, the organs. There are seeing, hearing, excretory zooids, and so on, comparable to the zooids of a siphonophore colony. OBSERVED CASES OF POLYEMBRYONY 357

“Alternation of generations is here considered a phenomenon, not limited as is generally taught to lower forms, but occurring throughout the animal kingdom.”

If the blastocyst is to be looked upon as a sexually produced individual from which arises asexually another or several others of a second generation, it is suggested that in this fact lies the explanation

fiG. 219. The development of the ovicell in Crista remosa. (From Patteron, after Harmer.)

A, external view. B, median longitudinal section of young ovicell. fol., follicle formed from polypide-bud; ov., ovary; ovi., oviccll.

of the difliculties that have met every attempt to homologize the early development of the mammals with that of the lower vertebrate classes. These differences have been discussed in Chapter X on the formation of the mammalian embryo; they constitute a problem of major importance to the comparative embryologist.

B. Onsnnvnn CASES or POLYEMBRYONY

We may now devote ourselves to the consideration of the groups of organisms in which specific polyembryony has already been noted to 358 POLYEM BRYON Y

occur, bearing in mind the different types of explanations that have been offered and attempting to discover how the facts conform to the suggested explanations.

flatworms. Among the flatworms are many cases which depart from the usual methods of reproduction. Of these some which do not fully fit into the classification have been described from time to time as polyembryony. There is one flatworm in which polyembryony undoubtedly occurs, however; it is the cestode Taema echmococcus, or Echmococcus coenurus as it is sometimes known. This small tapeworm produces eggs which develop into the usual hooked embryo, the onchosphere, and these in their turn produce a cyst which becomes the bladder worm or cysticercus. As is usual in the further development of a cysticcrcus, an invagination from the outside wall of the bladder into its cavity develops a new scolex and neck region which will later become inverted and form the new tapeworm. However, the matter is complicated in this case in that many scolices may be produced within a single bladder by the budding process, and even secondary bladders which produce multiple scolices in their turn are described. Thus the encysted worm may grow to an enormous size to endanger the life of the host and oftentimes bring about its death.

Bryozoa. Polyembryony occurs in the cyclostomatous bryozoa belonging to the Gymnolaemata of the Endoprocta. These animals live in colonies made up of zooecia

fiG 220- Section through which are in general tubular with densely

a follicle of Cnaza remosa show- - mg primary embryo (1) which calcareous walls. The circular orifices of the

§>ré>dt:)c1I(IiL(zisecorZ<I‘i‘ary erlgnbgnis zooecia give the group their name. At the time son, Xftei’ H$fi;e,_,r°m 3 e ' of the breeding season a curious specialized zooecium develops which is called the oecium

or ovicell. In this is developed the young embryo. Fertilization of a rather unusual sort having been successful, the oecium serves as a brood chamber about the developing embryos and larvae. The primary embryo undergoes a process of budding, and secondary and tertiary buds are EARTHWORM 359

produced all of which may develop into larvae, as many as 150 being on record from a single egg. They develop into ciliated larvae and each is capable of forming a new colony upon escape from the oecium. Earthworm. In the earthworm of the species Lumbricus trapczoides (Helodrilus caliginosus trapezoides) polyembryony results in the production of twins, a process which by Kleinenberg was regarded as universal for the species, but by Vejdovsky was held to be abnormal. It is due to a process of fission of the embryo. The cleavage of the egg



C D

fiG. 221. Twinning in the earthworm, Lumbncus trapezoides. (From Patterson, A, B, C. after Kleinenberg.)

A, Section of young twin embryos. the right one being the more developed. B, Double embryo, in section. C, Double embryo about to break apart. D, Type of double monster formed when embryos fail to separate.

is much modified from the typical spiral form of the annelids and indeed is variable. A blastula is formed, the endoderm and mesoblast cells pass into the cavity and the entire mass begins to elongate. Across the equator of the elongating mass a transverse furrow now appears from one side. As it deepens, the embryo is divided into two hemispheres held together by a few ectodermal cells only. Each half is destined to form one of the twins. Differentiation, gastrulation, and the completion of the internal organization go ahead while the worms remain connected. But at length they separate after a series of rotations which breaks them apart, except in a certain proportion of cases which become double 360 POLYEMBRYONY

monsters of various degrees of union. Thus from the single egg twin earthworms are produced.

In two other genera of oligochaetes double monsters have been described, and one infers that the twinning phenomena, though rare, may occur in a number of families. These cases were Tubifea: tubifex, found by Welch, Tubzfex rivulorum by Penner, and Sparganophilus eiseni by Hague.

Parasitic Hymenoptera. In the parasitic wasps we find some of the most important and complex cases of polyembryony in the entire animal kingdom, and certainly here the results of the process are exemplified in the most striking manner. In a single brood hatching from one parasitized caterpillar hundreds of individuals may be seen to issue all developed from one egg. Our knowledge of polyembryony in insects dates from the work of Marchal in 1898 and of Silvestri in 1906. Although a number of important points still remain to be satisfactorily cleared up, a number of investigators have contributed to this subject since then. Among them are Martin (1914), Patterson (1915, 1917, 1921, 1927), Hill (1922, 1923), and Leiby and Hill (1923, 1924), as well as others. The important genera studied include Litomastix truncatellus, Ageniaspis fuscicollis, several species of Copidosoma, Paracopz'dosomopsis floridanus, and three species of Platygaster. The most recent study is that of Parker (1931) upon the braconid, M acrocentrus. Undoubtedly many other forms of insects show polyembryony, but the ones mentioned include the more important cases studied.

The manner by which a single egg produces multiple embryos in these forms is perhaps best understood by beginning as Patterson has done in the paper earlier referred to with a description of Platygaster hiemalis, a parasite of the Hessian fly, which usually produces two individuals from one egg. From this comparatively simple case we have a gradual increase in complexity which at the end of the series is only incompletely understood, but the simpler cases at least are suggestive of the methods by which the more complicated probably develop.

In this species the parasite lays from four to eight eggs either in the egg or young larva of the host. If fertilized, the egg nucleus divides twice, producing two polar body nuclei; these are not passed to the outside of the egg but remain in the cytoplasm where after a time they come together to form a large polar nucleus called the paranucleus. With the fusion of the male and female pronuclei the egg becomes differentiated into two separate regions. The cleavage nucleus and cytoplasm surrounding it become cut off from the remainder and constitute the embryonic region, for only from it comes the material which will go into the formation of the developing embryos. The rePARASITIC HYMENOPTERA 36 I

mainder of the egg containing the paranucleus and its own cytoplasm entirely surrounding the embryonic region functions to absorb and

fiG 222. Polyembryonie development of Platyoaster hwmalw (From Patterson, after Leiby and Hill )

A. Egg of four hours, showing sperm head and first maturation division B, Egg showing two polocytes. and both pronuclei C, Egg with pronuclei in comunction and polar nucleus D. Embryo, two polar nuclei and a. parasitic body showing four nuclei E, Enclosed within a cyst formed from tissue of the host are two embryonic bodies each surrounded by trophamnion F. A later stage in the development of two embryos G, A thirteen-day-old polygerm in section, showing several embryos.

elaborate the tissues of the host for the nourishment of the young embryos and it is therefore spoken of as the trophamnion. In this species, although it is not characteristic of all, the host tissues form a 362 ‘ POLYEMBRYON Y

cyst wall around this developing body which then is spoken of as the parasitic body.

The paranucleus as development proceeds divides amitotically twice and the daughters distribute themselves in the trophamnion surrounding the embryonic region. The zygotic nucleus of the embryonic region divides first into two, then four, embryonic nuclei. Thereupon, the embryonic region becomes constricted and presently separated into two regions, each provided with two nuclei, and the trophamnion with its paranuclei also divides into two corresponding regions. The two halves of the parasitic body thus differentiated remain held together within a single cyst of host tissue, but develop independently. Four, eight, and sixteen nuclei arise from the division of each of these germs, as they are called, and these arrange themselves into the form of a typical spherical blastula, the cell walls being cut off around each nucleus. The remainder of the development is unimportant, for the process characteristic of these blastulae go forward through regular stages. There is produced from each a new individual which hatches in the next year.

In another species of this genus, P. vernalis, eight embryos are regularly developed. Here the process has a fundamental similarity to that just described, but the details of development differ. The parasitic body develops a number of embryonic nuclei surrounded by an appropriate amount of cytoplasm and a cell membrane. Each of these becomes a germ for the production of the later embryo and the entire mass is spoken of as a polygerm. It happens that the more complex cases were studied before the development of Platygaster was understood and some of the problems that were not clearly worked out would now probably be more easily followed through. It is known now that in Copidosoma gelechiae in the formation of the polygerm many primary germs are produced in a manner similar to the eight of Platygaster vernalis. These separate germs of the last polygerm stage all divide and give rise to two which develop into separate embryos.

Leiby and Hill believe that in Paracopidosomopsis, which is even more complicated, a secondary germ divides to form tertiary ones before the larval differentiation begins.

Armadillo. The final case of polyembryony to be discussed is perhaps the one in which the greatest interest lies. The Texas nine-banded armadillo Dasypus (Tatusia) novemcinctus normally produces four young from a single egg, the quadruplets being identical in respect to sex and to most of their morphological features. The work on the armadillo from the standpoint of polyembryony is of rather recent date, Fernandez concluding in 1909 that it occurs in a South American ARMADILLO 363

species Dasypus hybridus, and Newman and Patterson in the same year publishing the beginning of their important studies on the Texas species. Subsequent publications by these authors working independently have made available an account of the development of this form which is practically complete. The processes have been shown to be identical in respect to all important features in the two species which have been studied. The reader is referred to Chapter X for a discussion of the formation of the blastocyst in mammals.

In the armadillo as in other mammals, a monodermic blastocyst is formed which becomes differentiated into a trophoblastic portion and a formative portion, the inner cell mass. Then from the inner cell mass the endoderm is differentiated off, the remainder becoming ectoderm. Up to this point the blastocyst has remained free in the uterine cavity, but now attaches to the uterine mucosa. Attachment takes place directly over the embryonic ectoderm and the Trdiger forms at this point; then the inward growth of the spherical endodermal mass begins which brings about the so-called inversion of the germ layers. Within the ectodermal mass the formation of the ectodermic vesicle marks the beginning of the amniotic cavity. Above it an extraembryonic cavity is formed in the mesoderm. With progressive development the shift of the ectodermal cells takes place, resulting in the formation of the em~ bryonic shield with its thick ectoderm and the true amnion above it. In this stage the first sign of polyembryony makes its appearance, for from opposite sides of the ectodermal vesicle thus formed blunt projections extend laterally. Patterson called these primary buds. By this time that portion of the trophoblast which has not become involved in the attachment to the uterine wall disappears and the yolk sac endoderm is directly exposed in the uterine cavity. The two primary buds now divide each to form two secondary buds, making in all four buds which are rudiments of the four embryos subsequently to arise. Although they arise in this bilateral fashion and develop in the right and left halves of the uterus respectively, they later come to occupy positions that are about equally spaced from each other.

Meanwhile the vesicle grows, and the endoderm of the yolk sac, including those portions with which the embryonic ectoderm of each bud is in contact and which will form the gut endoderm of the embryo, faces the uterine cavity. The anterior ends of all the embryos point toward the apex of the common ectodermal vesicle, that is, toward the original amniotic cavity, and the entire vesicle may now be spoken of as the common amniotic vesicle. The entire structure now grows very rapidly, especially that portion of it which originated from the trophoblastic knob or the Trdger. This growth finally comes to occupy most 364 POLYEMBRYONY

of the space in the fundus of the uterus. The further history is especially concerned with the embryonic buds. Their posterior ends lengthen out with the growth of the vesicle and finally unite at a point opposite the original attachment and from their point of union the umbilicus later arises. The common amniotic vesicle by this growth procedure is left

fiG. 223. The development of the blastocyst of the armadillo. (After Patterson.) ec., ectoderm; en., endoderm; icm., inner cell mass; mes.. mesoderm; tr., trager; tro., trophoblast; u.. uterus.

as a small structure at the lower apex, in contact with each bud, while most of the remaining portion of the cyst mass with its developing embryos is derived from the growth of the Trdger. The buds meanwhile continue their growth, each forming a primitive streak, which is a substitution for the embryonic shield as described for other mammals. The further development of the embryos and the subsequent changes which lead to the production of the four foetuses need not be traced ARMADILLO 365

since it is simply a problem of organogenesis and of the steps normally following. The relations which are necessary for the understanding of

fiG. 224. A, The uterus and entire blastocyst of the armadillo showing paired origin 01' embryos. B, Half-grown foetuses spread out from uterus wall. (After Patterson.)

the polyembryonic condition all grow out of the budding processes of the embryonic vesicle and are completed with the establishment of the four embryos. There are many interesting problems connected with 366 POLYEMBRYONY

the later stages from the standpoint of later embryology and hereditary correlations of the characters of the four offspring as well as from other points of view, but the special problem of polyembryony is explained by these earlier stages.

C. EXAMPLES or DOUBTFUL POLYEMBRYONY

Two other cases which resemble polyembryony in some respects should be mentioned. As a matter of fact there are some departures in each of them which do not justify their inclusion with this type of development.

Among the trematodes the egg of Fasciola hepatica, the sheep fluke, is fertilized in the body of the adult fluke, makes its way down the bile duct and out of the intestine of the sheep and hatches when it rains as a tiny ciliated larva, a miricidium. Entering the intermediate host, the snail, the miricidium becomes a sporocyst and within it parthenogenetic ova appear which develop into rediae, the next larval form. Within the body of the rediae the process may be repeated but at length cercariae are developed which escape from the snail and bring about the reinfestation of the adult host. This case has been called polyembryony by some, but by others it is regarded as paedogenesis, for here the new larvae are said to be produced not asexually but from parthenogenetic ova, a difierence in method which, if true, would seem to be fundamental. However, the reservation must be made that if the germ masses from which the new larvae arise are not ova, but are produced asexually (as F. G. Brooks believes, having found no maturation phenomena or other egg—like behavior), then we have to do here merely with asexual reproduction, and not even paedogenesis,

A second case which at first thought suggests polyembryony occurs in the tunicates. Among the Thalaceae as represented by the genus Salpa it has long been known that two forms of individuals are to be expected, one a solitary form and the other a colony which is usually found as a chain of individuals. The first of these develops asexually, although produced from a fertilized egg. The second is known to be budded ofi’ from a stolon which grows out from the asexual individual, and among the colonial forms some at least are sexual, producing the eggs and sperm which in their turn start the cycle over again. The genus Dolielum is rather more complicated than Salpa but it seems to illustrate the situation quite well and it is here that the type of development of particular interest to us may be said to occur.

In Doliolum an oozoid is developed from the fertilized egg and it reproduces asexually. By some it is regarded as a larval zooid, and certainly it has not yet reached its final character. If it is correct to EXAMPLES OF DOUBTFUL POLYE-MBRYON Y 367

regard the oozoid as a larval form, this case is very closely akin to polyembryony. From the ventral posterior part of the oozoid a proliferating stolon is formed as a protrusion of the ectoderm into which the mesoderm penetrates. From the stolon buds arise which break loose in a very immature condition and Worm their way upward and dorsally over the surface of the parent. Since the number given off from the ventral stolon is less than the number later found on the dorsal process, it is assumed that the buds must divide en route, and some evidence of this process has been found. Arrived at the dorsal side of the oozoid, the buds attach themselves to a posterior process of the test which arises as a middorsal projection (occasionally spoken of incorrectly as a dorsal stolon). These bodies attach themselves in three longitudinal rows to the outgrowth. The two lateral rows of buds are known as trophozooids or gasterozooids and their only function is to nourish the colony. The dorsal row of buds undergoes metamorphosis into several kinds of zooids. Some become phorozooids or nurse zooids, and according to some investigators they produce from a ventral stalk buds which are protogonozooids or primary sex buds. These latter either by budding or fission produce the sexual animals, the gonozooids or blastozooids, in which with further development sex organs are formed and the cycle is completed. Here an alternation of generations occurs in which there are three asexual generations and one sexual generation in one cycle. Whether it is to be regarded as polyembryony depends upon the interpretation of certain stages. It is very complicated in the extreme, and is at least close to true polyembryony. CHAPTER VIII THE DETERMINATION PROBLEM

A. INTRODUCTION AND STATEMENT or PROBLEM

A problem which has run through the entire history of embryology and is yet a live question at the present time concerns the extent to which the egg represents a fixed and definite system whose course is set when its development has begun. This is the determination problem. It first became a live issue during the controversy between the preformationists and the epigenesists of the seventeenth and eighteenth centuries and was even in that crude form an attempt to solve the question of the organization of the egg. The one school held that development was

simply an unfolding of an organism already present in an infolded con—'

dition; that is, organization was complete and development brought forth nothing new. The other held that the egg was unorganized and that everything in development was new. The history of embryology since these crude beginnings, at least of that part of the science which has concerned itself with the earliest stages in ontogeny, has been an attempt to make clear the manner in which the organization of the egg becomes manifest. Except for historical reasons it is not necessary to trace the course of these studies nor would it be possible except in a much more extensive treatment of the subject than is given here, for the literature is voluminous. It is not even possible to summarize in a short discussion the work which has been done. All that can be attempted is to bring together briefly the lines of work which have been responsible for the present conceptions in regard to determination.

Two sets of facts confront the student who would consider the determination problem. Neither bears directly upon the question at issue, but both serve to limit it. In the first place an egg goes through certain steps with surprising uniformity and produces an individual which is structurally very complex and very much differentiated. It is organized in the highest conceivable degree. In the second place modern genetics has shown that the egg to begin with possesses in the mechanism by which the genes are controlled and distributed a type of organization likewise complex in the extreme; and there is no doubt that this mechanism operates to produce the conditions found in later ontogeny. Yet differentiation is a matter of the cytoplasm of the cells. The repeated

368 INTRODUCTION AND STATEMENT OF PROBLEM 369

mitoses do not affect in a differential fashion the elements of the nucleus and it is clear that the nucleus contains in the chromatin the non differentiating material, the germ plasm, while the cytoplasmic portion of the cell is the basis of specialization and is indeed the somatoplasm which gives rise to all the differentiations later seen in the course of ontogeny. Between these two sets of facts must lie the third set, little understood and often little appreciated at the present time. Almost nothing can be offered in the way of explanation as to the method by which the gene mechanism produces its fundamental effect upon differentiation. The gene mechanism concerns heredity, that is, by it is explained the similarity existing between generations, but as yet its study has offered little which enables us to understand its relation to the differentiating soma. It was earlier said that heredity was the central problem of biology. Differentiation is certainly a central problem of development, and, let it be said, at the present time one of the most elusive. The questions of differentiation and of determination have dominated a surprisingly large part of the embryological work of the last century.

These two questions are really two aspects of the problem of organization, for differentiation is the manifestation of the operative mechanism of the egg as modified by extrinsic factors. To discover the extreme to which this operative mechanism is already present in the early stages and to which it gives a definite “set” to the differentiating embryo is the aim of the work on determination. If differentiations become visible early and are little modified by extrinsic factors with the result that the course of development is orderly in a high degree, we say that the egg is strongly determinative. But if the egg retains its embryonic plasticity and easily adapts itself to environmental disturbances, that is, is easily modified by extrinsic factors, it is said to be indeterminative or of the regulatory type. If differentiations manifest themselves early, little regulatory capacity is retained by the egg. In other words, the capacity of the egg for regulation is inversely proportional to the progress of differentiation.

It must be borne in mind also in considering the problem of differentiation (and hence of determination) that the chemico-physical organization of the cell limits the conclusions which may be reached. Differentiation manifests itself through colloidal materials. The chemistry of the protoplasmic system is so imperfectly known that whatever conclusions are reached regarding these problems must be subject to revision when a better understanding shall have been attained, for example of the phenomena of gelation which plays a very important part in the physical expression of mitotic phenomena. It has been shown by the studies of 370 THE DETERMINATION PROBLEM

Conklin and of others that the position and size of the spindle are matters of great importance in differentiation. Yet the physico-chemical factors which are involved in spindle behavior have not yet been adequately analyzed. Other problems of physico-chemical nature similarly affect our"conclusions. It is not too much to say that in spite of the vast amount of embryological research differentiation and its mechanism is one of the least understood fields of biology.

It has been pointed out that the function of cleavage is to sort out the materials of the egg into cells so that differentiation may progress. The uncleaved egg represents all of the materials present, although not necessarily all that are later to appear. Yet the progressive development of the organism in its usual course at least as indicated by our present knowledge depends upon getting these materials separated from each other. It does not follow, however, that this sorting-out process of cleavage is the cause of the subsequent development. Rather there must be a fundamental underlying mechanism of organization, the manifestations of which are the cleavage phenomena. Primarily determination concerns itself with the manifestations of these underlying methods of organization. It seeks for evidence of pre—1ocalization of areas or substances within the egg or even of an early promorphology which gives visible expression to the underlying mechanism. Some of the questions involved may perhaps be formulated in the following manner: Are there special structures or substances or fundaments which exist in the egg at the very beginning of development and which are independent of each other and of other parts of the egg? If so, how are they formed? Must all appear at the same time, or may some appear later on? Conversely, are the definite structures of the embryo never independent of each other? Are the parts always influenced by the whole of which they are constituents? Or finally, are there some eggs which are determinative in their character and others which are not, or are some parts of the individual embryo determinative and other parts not? Perhaps all these questions may be said to depend most largely for their answers upon this one. At what time and from what sources do differentiations begin in the embryo? It may be noted that the answers to these questions are not the same for all organisms.

B. CLASSICAL THEoR1Es or THE NATURE or DEVELOPMENT

Historically there have been a number of theories developed in response to these questions. They represent the various forms which the answers of different investigators have taken and must be considered from the standpoint of the information available when they were formulated. One of them was the theory of organ-forming regions of CLASSICAL THEORIES OF THE NATURE OF DEVELOPMENT 371

Wilhelm His (1874). This is the doctrine that definitely localized areas perhaps even in the unsegmented egg are the forerunners of the'organs and parts of the embryo, that “the germinal disc [of the chick] contains the preformed germs of the organs spread out over a flat surface, and conversely . . . every point of the germinal disc is found again in a later organ.” Ray Lankester supported His in his views, saying that it was quite possible for the cell to “contain already formed and individualized, various kinds of physiological molecules. The visible process of segregation is only the sequel of a differentiation already established and not visible.” Whitman as a result of his work on Clepsine concluded that the embryo is predetermined, even if not predelineated. Rabl and van Beneden likewise were among the early supporters of the view that even in the unsegmented egg an organization of protoplasmic particles which predetermines the development of the embryo is present. In the bald form in which this doctrine was proposed by His it can scarcely be accepted, however, and as a matter of fact His had no great amount of observational and experimental evidence on which to base it. The study of cell lineage offers what of evidence there is in support of this doctrine but even at best it does not force as rigid an interpretation as His placed upon it. Many authors have denied it in its entirety and there are few who do not criticize it.

Another form of answer to the question of determination is the theory of organ-forming substances, according to which the materials within the egg rather than the areas which they occupy receive the chief attention. Here again it is obvious that not all materials within the egg, even though they be definitely localized, are formative. Yolk, pigment, oil globules, and other inclusions in the cytoplasm are definitely located in many eggs, yet clearly are not formative. In some instances visibly differentiated substances within the unsegmented egg have been shown to have no formative function. At least they have been displaced by pressure or by centrifugal force, and normal embryos have nevertheless resulted. Yet in other forms the materials of the egg have been traced in a precise manner to the organs of the embryo. Surely a principle of determination is here involved which is too important to deny because of a particular formulation of a doctrine. Perhaps the importance of the visible organ-forming substances has been overemphasized and these are but manifestations of a more fundamental mechanism. Yet in very many eggs the mechanism undoubtedly exists, and later researches have certainly demonstrated the essential correctness of the principle involved in the conception that the egg is not without an organization before cleavage begins which conditions the future course of its development. 372 THE DETERMINATION PROBLEM

As a result of the early work on cell lineage by Whitman, Rabl, van Beneden and others the former view that blastomeres were indifferent both in position and significance was gradually replaced by another to the effect that the cleavage pattern was in the nature of a mosaic, and that a blastomere occupied its particular place because of the material contained in it, that is because of its mosaic character. The views were supported not only by the extensive studies on cell lineage, but also by the experiments of Roux, Chabry, Conklin, Wilson, and others. These experiments are discussed later in this chapter.

The mosaic theory of development, if understood in a sense not too rigid to take account of the fundamental plasticity of living protoplasm, certainly expresses one of the underlying truths of embryology. One may, however, raise the question of the manner and the time of origin of the mosaic work and also whether it is so fixed that it is not subject to the regulatory processes of which the organism is capable.

The question of regulation brings up yet another theory of historical significance which We owe to Driesch. His terms prospective significance, prospective potency, his equipotential system, are all well known to those who are familiar with the history of the determination problem. By prospective significance of a cell he meant the actual destiny in the developmental process. By prospective potency he meant the possible fate which the cell might attain. Prospective potency includes the sum of the different developmental possibilities. As the result of numerous experiments, Driesch reached the conclusion which he thought of general application, that the egg is essentially an equipotential system, for the cells of a blastula of a sea-urchin, for example, are of uniform material and might be interchanged like balls in a pile without affecting the result in the development of the embryo; in other words that the fate, the prospective significance, of a particular blastomere is a “function of its position.” Driesch’s theory was in opposition to the mosaic theory of development according to which the fate of the blastomeres did not depend upon their position alone but upon their organization. It was based upon the conception current at the time when work on cell lineage first rose to an important place. Pfliiger had held that the egg and its blastomeres were homogeneous throughout and that cleavage simply multiplied the units out of which diiferentiations were later to arise. This view was also favored by Oscar Hertwig. Driesch, who although chiefly interested in philosophy, set himself to carry out experiments in development upon which certain philosophical decisions might be based, made this conception the starting point of his theory of development.

Some experimental evidence is at hand upon which to a certain MORPHOLOGICAL EVIDENCE 373

extent the theory of Driesch may be based, while there is also evidence upon which the mosaic conception may rest. On the one hand certain eggs possess a high degree of regulatory capacity and are hence indeterminative in their cleavage. On the other hand certain other eggs show the marks of differentiation appearing at a very early stage in the

development of the egg; these eggs possess but slight regulatory ability and are hence determinative in character. Between the mosaic type

and the regulatory type no sharp boundary line can be drawn. Rather there is a gradation from one extreme of the series to the other. If we sum up the results of these researches we may arrange the animal series from the regulatory to the mosaic forms in about this order: amphioxus, teleosts, mammals, nemerteans, urodeles, anura, ctenophores, annelids, molluscs, arthropods, nematodes, and ascidians. But it is to be noted that purely regulatory and purely mosaic types do not occur. In this we are merely emphasizing what has been said before, that the time at which differentiation appears is the real criterion upon which we may recognize the differences between determinative and indeterminative types of eggs. In other words if differentiation sets in early the regulatory capacity of the egg is correspondingly reduced. Conversely, eggs with high regulatory capacity show little evidences of early differentiation.

C. EVIDENCE BEARING ON DETERMINATION

The present status of opinion in regard to the determination problem has been reached as the result of two different lines of evidence. One of these is the morphological study of normal embryological stages. The other line of evidence embodies the results of many experiments which

have sought an insight into the fundamental nature of developmental problems.

1. Morphological Evidence

Of the morphological evidencesthat some type of determination exists to some extent in all eggs reference should perhaps be made first to the contributions of genetics. The breeding experiments of this century have very clearly shown the existence of hereditary units within the germ cells. Although we do not by any means identify these units with visible structures in the egg cell nor do we know how they express their influence upon the developing organism, yet any theory of particulate inheritance (that is inheritance based upon the presence of organized particles within the germ cell) is, in so far as it is justified, evidence in favor of a morphological basis of determinate development. This evidence bears out the conclusion stated above that, although 374 THE DETERMINATION PROBLEM

the regulatory processes may dominate in certain types of eggs, there are none which are purely regulatory.

The first signs of differentiation in the developing egg have to do with the general features of polarity, symmetry, and pattern of the egg. From these’ general features more detailed diiferentiations with respect to polarity, symmetry, location, and pattern of the constituent cells and parts of the embryo arise and later the differentiations of tissues and the beginning of organs. Development is thus progressive, and differentiation, at first relating only to the most general features, gradually passes to specialized details. Since polarity, symmetry, and cleavage pattern are general in character their importance is sometimes overlocked by the student, yet very little thought is required to convince one that they are really basic. Our morphological knowledge with regard to the development of polarity and symmetry has been discussed in the chapters which have to do with the different types of cleavages and reference should be made to those chapters. These observations have been checked by many experiments of the greatest importance and it will perhaps suflice to refer to these experiments under the second line of evidence as listed here.

Morphological studies of the cleavage pattern, as has already been indicated, became the foundation for the mosaic theory of development in the studies at the hands of the students of cell lineage. It early became clear that certain types of cleavage were predominately determinative. Some eggs with bilateral cleavage, certain types of eggs with superficial cleavage, those with spiral cleavage, with disymmetrical, and even an occasional form having radial cleavage, such as Strongylocentrotus, were shown at that time to be determinative in their development. Most forms with radial cleavage, some with bilateral, and even occasional examples of eggs with spiral cleavage show the regulatory type, however. For a discussion of these the student is referred to the chapters on cleavage types.

2. Experimental Evidence

The second line of evidence which bears upon the problem of determination is perhaps no more important than the morphological evidence but is certainly not less so and is much more recent. It is obtained from those special experiments* which have to do with this problem.

‘ As pointed out in the chapter which deals with history of embryology, the present is the period of acperimental embryology. Much of morphological character remains to be learned, but nevertheless the dominant note in embryological research of the present day is the experimental one. It is now sought to discover those underlying principles which account for the form changes by which the structure of the organism is produced rather than simply to give a descriptive account of those characters. EXPERIMENTAL EVIDENCE 375

The first series of experiments of significance for study of determination is concerned with the localization of the median plama. Here as with the other experiments to be summarized the student is referred to Morgan’s critical discussion as well as to the original papers which describe them. It would be impossible in a work of this size to give even a brief account of the experiments themselves. Reference can only be made to those which seem most significant.

The matter of the localization of the median plane is of importance because it indicates the early determination of symmetry and polarity on the part of the egg. According to some the polarity of the egg may be traced back even into an ovarian condition, and some believe that the type of symmetry is determined in the egg cytoplasm before fertilization. Although the evidence of these relationships seems good in some cases it has not been made clear how much the appearance of symmetry_in these early stages is related to the cleavage plane or the symmetry of the embryo. No mechanism for bringing this about has

Experimental embryology has seemed to cover a wide range of topics and the results of the investigations in this field are scattered throughout many journals. There have been but few attempts to bring this material into the scope of a single volume. The first section of Korschelt and Heider’s “Lehrbuch der vergleichenden Entwicklungsgeschichte der wirbcllosen Thiere” deals with the experimental results obtained up to that time (1902). In 1909 Jenkinson published his book entitled “Experimental Embryology” and summarized much of the work available at that time. The contribution to experimental embryology most important now, however, is the volume by Morgan entitled “Experimental Embryology” and published in 1927. Morgan has promised a further volume which will deal with such topics as growth, reflex reactions, tropisms of the larvae, the influence of environment upon the embryos, the source of energy of development, etc. It is to be hoped that this volume will appear at no distant date.

In spite of the diversity of topics which have engaged the attention of experimental embryologists it is possible to classify them into a few divisions. (1) The early students of this field were specially interested in the discovery of the effect that external factors have upon the developing embryo. Among these factors are gravitation, mechanical agitation, electricity, light, heat, atmospheric pressure, osmotic pressure, and the chemical composition of. the medium in which development takes place. (2) In addition to this the growth problem, the problems centering around fertilization, have occupied much attention during the present century. Something of the nature of these problems is suggested in the section of this book which has to do with artificial parthenogenesis, although this is but one of the many topics that have been studied. (3) finally a great deal of attention has been given by experimental embryologists to those problems which are concerned with the forrna— tive changes of the egg. These factors are internal in their nature and seem to take the experimenter further in his attempts at the analysis of the innate, vital character of the organism than do the other problems enumerated. The experiments which bear on the problem of determination come under this head. Those experiments which have sought light on this problem fall chiefly within a few animal groups, namely: the ctenophores, some hydromedusae, the nematodes, annelids and molluscs, echinodcrms, ascidians. It may be remarked that not only are these the forms which seem to have yielded results most capable of analysis but they are also the forms upon which it is easiest to experiment. 376 THE DETERMINATION PROBLEM

been demonstrated. In many cases where a relationship between the first cleavage plane and the planes of symmetry of the later embryo have been made out it is thought that the point of entrance of the spermatozoon and the path traveled by the sperm pronucleus in approaching the egg pronucleus determine the position of the plane. Suggestions have also been made that the pressure of the enveloping membrane of the egg or pressure from the oviduct or other external factors may be related to the position of the plane. Certainly the causal character of such factors has not been demonstrated. It may be said, however, that so long as the possibility remains of a relationship for example at the point of entrance of the spermatozoon it is necessary to assume that the symmetry of the embryo goes back to a predetermined symmetry of the egg.

The question of a relationship of the median plane and the first cleavage plane arises in the history of embryology in relation to the frog egg. As long ago as 1851 Newport had reported that the two coincide, and from that time the question has been often discussed. In the frog egg at the time of cleavage there is already present a bilaterality as shown by the presence of the gray crescent. The real question involved in determining the symmetry relationships is: what in the uncleaved egg causes the material to take the position of the gray crescent, and why does the first cleavage plane cut through the middle of it? Experiments have shown that its position is determined after fertilization and that any meridian of the unfertilized egg may become the median plane. After fertilization the meridians are not equivalent in this respect, however, for usually the crescent forms opposite the point of entrance of the sperm. A long series of experiments can be cited to show that in nearly two-thirds of the cases the first cleavage plane does coincide with the middle of the gray crescent. It is clear, however, that if 30 per cent or more of the eggs fail to show this relationship the mechanism of determination is by no means a fixed one. In other amphibia the experiments of Jordan indicate that the first cleavage plane is at right angles to the axis of the egg of Diemyctylus, and Spemann has found for Triton that the second cleavage plane coincides with the median plane of the embryo. Of course it is immaterial from the standpoint of determination as to whether it is the first or second plane which shows the relationship. In the teleost fishes according to the work of Morgan and of Clapp no definite relation between the second plane and the median plane of the body can be made out. For the sea-urchin a considerable amount of evidence is available. In Toxopneustes, Wilson and Mathews related the appearance of the first cleavage plane to the entrance of the spermatozoon, and Boveri held that it coincided with the median plane of the EXPERIMENTAL EVIDENCE 377

embryo. In the eggs of Echinus, Driesch found the second plane to correspond to the median plane and Runnstrém assumed that the first cleavage coincides with the median plane. Recently Von Ubisch has performed a very ingenious experiment by which certain portions of the egg were stained with intra vitam stains; in three species of seaurchins he obtained results which are in agreement. He was able to demonstrate no fixed relation between the planes of symmetry and planes of cleavage, but found some evidence that the first cleavage plane more nearly coincides with the median plane. On the whole for the sea-urchins perhaps this is the most acceptable conclusion. In his study of ascidian embryology Conklin determined that the first cleavage plane is the median plane of the embryo, and that in Cynthia its position is indicated before the pronuclei meet. In the nematodes, according to Boveri’s work on Ascaris, the third cleavage plane of the dorsal cells is the median plane of the embryo. In Nereis, Just has found that the second cleavage plane usually corresponds to the median plane of the embryo but the first cleavage plane is determined by the position of the entering spermatozoon. Insect eggs are distinctly bilateral so far as their orientation is concerned, the position of the egg as laid corresponding to the symmetry of the mother’s body and definitely indicating the position of the embryo in the egg. For the chick and pigeon Bartelmez has held that bilaterality is present even in the small ovarian eggs.

A second series of experiments related to the problem of determination has sought to discover to what extent localization of germinal areas is present before cleavage, using as a method the development of egg fragments. Eggs of Cerebratulus were out along definite planes by Wilson, Zeleny, and Yatsu. Cuts were made both before and after fertilization and development followed without difficulty. The cleavage of the fragments in general corresponded to the type of cleavage of the whole egg but upon a much reduced scale. It was not found to make a difference from which part of the egg the fragment was taken. The experiments show that either factors which determined cleavage were not yet definitely localized at the time of maturation or the egg is capable of very extensive regulation. According to Yatsu if the operation occurred between the formation of the first and second polar bodies the cleavage was entirely regular but if it was after the second division irregularities developed in some of the cases. Wilson experimented with fragments of the egg of Dentalium. Here the presence of the yolk lobe complicates the result. If the yolk lobe is entirely present and only the apical portion of the egg cut off, the resulting larva is nearly normal; likewise an entirely symmetrical division of the yolk lobe seems not seriously to interfere with the course of development. If the cuts are made in any other manner, however, irregularities appear. The ctenophore Beroé when out into fragments in the unsegmented condition produces in some cases partial embryos and in others whole ones depending on whether the cut is symmetrical or oblique. Driesch, Morgan, Yatsu, and fischel have experimented with this form. With sea-urchin eggs conflicting results have been obtained from experiments with the development of fragments. Taylor and Tennant using accurate methods of cutting with a micro-dissecting machine obtained small pluteae from the developing fragments which were like the normal ones. But Harnley obtained evidence that the materials of the egg were qualitatively different. finally experiments on the development of parts of Triton eggs have been performed by Spemann and Baltzer. Non-nucleated fragments, obtained by separating the egg by means of a hair tied around it, developed but rarely and the nucleated fragments produced dwarf larvae which did not live long enough to undergo metamorphosis although normal in most particulars.

An interesting result of these experiments is the conclusion that the entrance of the sperm into the egg is not of itself sufficient to start development, for, if an egg is cut just after the penetration of the sperm so that the female pronucleus is in one half and the male pronucleus in the other, it is the half containing the sperm pronucleus that develops but not the other. Something else besides the mere initiation of division is accomplished by the entrance of the spermatozoon. The cleavage of egg fragments demonstrates that for many types of eggs the pattern develops along with the mitotic figure.

Another series of experiments has sought to discover to what extent it is possible for a whole embryo to develop from an isolated blastomere. In some few eggs it is possible to cut the blastomeres apart at the time when they are most widely separated from each other as the first cleavage is closing. In others it has been found possible to separate them by shaking them in a tube of water, or by squirting them from a pipette. Again eggs of echinoderms permit the easy separation of the blastomeres if they are kept in calcium-free sea water while the first cleavage is taking place. Isolation experiments have been performed on sea-urchins, the hydroid Clytia flavidula, Cerebratulus, amphioxus, teleost fishes, Triton, and the frog, and in all these cases whole embryos were obtained from the isolated blastomere. On the other hand blastomeres of ctenophores, molluscs, and ascidians when isolated give rise to half embryos only. It would seem that this emphasizes again the distinction between determinative and regulatory eggs.

The question arises as to whether the development of the isolated blastomere is strictly comparable with the results that would be obtained if the material of the missing portion of the egg were present. Experiments have been performed in which the single blastomere has been allowed to develop in contact with the material of its sister cell, which owing to various kinds of injury was prevented from any active participation in the normal result. Experimenting upon the frog, Roux injured one blastomere with a hot needle but did not kill it. He thought that the subsequent development of the uninjured blastomere in contact with the inactive one was in the nature of regulation and that gradually the missing portion of the embryo was restored. This conclusion seems doubtful as there is now good evidence that the resulting embryo is more nearly one-half than a whole. Later studies have shown that, in experiments of this kind, if the plane of the first cleavage goes through the middle of the gray crescent a half embryo results. If the plane is parallel to the gray crescent and the injured blastomere is the one which contains it, nothing recognizable is produced from the opposite one. But if the opposite blastomere is injured the one containing the gray crescent will produce the anterior end of the embryo. Even if the cleavage plane is at other angles the blastomere containing most of the gray crescent will produce an anterior end.

McClendon working on the tree frog, Chorophylus (Pseudacris), sucked out the injured blastomere to determine whether its presence has any effect. In his experiments the remaining blastomere produced a normal whole embryo of one—half size. Injuries to one blastomere of the egg of Ascaris led to the conclusion in the experiments of Stevens, of Boveri, and of Schleip that each individual cell contains the factors which are responsible for its own development; in short, that there is little self-regulation on the part of the blastomeres. The egg of Cyclops after the injury to one blastomere has been studied by Fuchs and by Miss Jacobs. The evidence goes to show that for this egg the contact of the injured blastomere with the uninjured one does not materially affect the result of the development of the latter. This results in a partial embryo. In this same connection the experiments of a number of investigators, of whom Hegner and Reith are typical, on the effect of injury to the eggs of insects should be mentioned. Insect eggs apparently may be among the most determinative with which we have to deal, for these experiments indicate that different cytoplasmic areas on the surface of the egg are fixed in their prospective significance even before the cleaving nuclei with their surrounding cytoplasmic islands migrate to the surface and they have no great powers of readjustment. There is indeed a considerable degree of independence in the development of the respective parts. If the injury is not too severe to a certain localized portion of the egg the remainder will go ahead and develop without much dependence upon the injured portion, but will produce only that part of the embryo which was to be expected. Reith found that, if the posterior end of the egg of the house fly is injured, the parts normally resulting from the anterior end will develop. If the anterior end is the location of the injury, a larva without a head end develops, and in some cases injury to the middle portion of the egg was not so severe but that both anterior and posterior organs developed.

Hegner’s experiments on the eggs of the chrysomelid beetles Calligrapha multipunctata and Leptinotarsa decemlineata are Well known. Here the posterior end of the egg is the location of the pole plasm which Hegner found to pass into the germ cells in development. By injuring this region with a hot needle he was able to secure embryos without germ cells. Evidently the cytoplasmic regions in the eggs of these insects are very early set aside to produce definite parts of the embryo. Yet it must not be inferred that the regions in question retain no powers of adjustment. As cleavage progresses the possibilities of readjustment are lessened but are not entirely lacking.

A very important series of experiments carried out in the laboratory of Spemann on the embryos of Triton have shown that the future of certain ectodermal areas in the gastrula are much modified by their position. The method by which these experiments were carried out was that of transplanting a portion of the ectoderm by means of a micro-pipette from one portion of the body to another and studying its relationship to the development of the neural plate. From this study it appeared that the presence of the endomesoderm beneath the surface of the ectoderm is immediately necessary for the neural plate to be formed. Spemann and his collaborators have shown that the prospective ectoderm is capable of producing entirely different organs upon transplantation. For instance ectoderm from the top of the young blastula or gastrula implanted on the lip of the blastopore and carried to the interior may become notochord, mesoblastic somites, pronephros, or perhaps other organs. Ectoderm taken from a slightly later stage, that is, after the closure of the blastopore, if carried into the mesoderm becomes mesodermal somites; if carried into the endoderm goes to the formation of the archenteron. It should be pointed out that particular organs which differentiate from given substances may through the process of rearrangement be induced in an entirely different direction from that which their normal determination indicated. Throughout the animal kingdom there are many cases which serve to emphasize the difference between the determination of an organ and the actual differentiation which sometimes results from the modification of normal processes. What is shown by such cases, however, is not that the unusual condition is one of indetermination but that the organism has responded to modi— fying factors to produce a result different from that which would have occurred had not the unusual factors been present. Determination of an embryo does not always correspond to its differentiation.

A problem which has given rise to a great deal of experimentation in relation to the question of determination is the influence of pressure upon cleaving eggs. The work began with the experiments of Pflfiger in 1884 in compressing the eggs of frogs between two glass plates. The direction of the first three cleavage planes was found to be at right angles to the plane of compression. When the compression was released, normal embryos developed. Similar experiments have been performed in numerous other eggs with the result that normal development is found to follow the release of pressure on eggs of hydroids, sea-urchins, frogs, and Cerebralulus. In eggs of N ereis, Ciona, and molluscs, abnormal development follows compression. In the first group of eggs it is to be noted that differentiation does not begin until there is relatively a large number of cells present. In the second group signs of differentiation are to be noted very early. This series of experiments was used by 0. Hertwig and by Driesch in support of their opposition to the mosaic theory of development. Perhaps the experiments are less crucial than was formerly believed and merely emphasize the distinction previously insisted upon that there are two types of eggs with respect to their capacities for regulation as distinguished from determination.

finally the literature of experimental embryology contains many records of attempts to bring about the redistribution by centrifuging of egg substances, particularly those which are visibly different. These materials as well as the formed materials of the egg yolk, pigment, fat, and other inclusions are often of different specific gravity and hence respond to centrifuging by redistributing themselves in different zones or strata. This transfer of materials throughout the egg takes place as a rule without injury to its living substance. The use of the centrifuge in experimental embryology began with the work of Lyon in 1906, although it had been utilized for the study of the constitution of the cytoplasm by Gurwitsch in 1904. Lyon’s paper is a classical one in embryology both because of the introduction of a new method and because of his discovery that the redistribution of the egg constituents does not afiect the development of the eggs from the standpoint of determination. Many other investigators have used this method for the study of eggs through a wide range of animal forms. The results of the experiments with the centrifuge have rather uniformly indicated that the visibly stratified substances in the egg are not determinative in the sense that they are organ forming. It would seem that the method, though productive of results which have great value from other standpoints, has failed to give critical evidence as to the determinative character of development in the eggs to which it has been applied.

As a conclusion to this long catalogue of evidences, the position earlier talfen in this chapter may be reiterated. The animal series can be arranged in such a manner as to show a transition from eggs which are highly regulatory to those that are highly determinative in character. N 0 eggs are known which are purely regulatory or purely determinative, but at one end of the series differentiation sets in very late and the regulatory capacity is high. At the other end the marks of difierentiation begin even before cleavage and the powers of regulation are correspondingly lessened.


CHAPTER IX ECOLOGICAL CONTROL OF INVERTEBRATE LARVAL TYPES

Throughout the animal kingdom many diverse environmental relations surround the eggs and young so that many responses might be catalogued. Environmental influences find expression in the places where the eggs are laid, in the amount and kind of food provided for the young during the early development, in the different devices for their protection, in specialized modifications for accomplishing locomotion and other vital activities, and in many cases in the production of forms of larvae ‘which are totally different from the adult organisms. These special types of larvae present a great range of variations from the modes of direct development with which the student of the embryology of vertebrates is familiar. These larval types involve a metamorphosis to the adult form which may be more or less complete and which in such cases brings the growing organism into an environment quite unlike that of its earlier development; metamorphosis is necessary in those forms in which the food and habits of the adult are unsuitable for developing young. If we assume the sea to have been the original home of most primitive stocks, an assumption which is more or less common and seems in line with the fact that very many types of animals develop in a moist atmosphere or liquid medium, we should expect the majority of unusual larvae to be found in the species living in salt water. The transition from salt water to fresh or to the terrestrial forms of life has presented many difficulties to the developing young and as a result those animals which live in fresh water or are terrestrial are more often characterized by direct development than are the salt-water forms. It may be regarded as an axiom of development that sessile adults have active young. This activity has two obvious results; first, the species secures its dispersal through the migration of the young, and econd, it extends the range. The migration is commonly passive but over a period of time serves to extend the range of the species as successfully as if the adults themselves were able to move. To insure dispersal, vast numbers of gametes must be produced, for the chance method of fertilization that usually accompanies such cases results in a failure of very many eggs and sperm to become further activated, and of those eggs which are fertilized only a few can come to maturity. The larval mortality is very high indeed, for these young are the food of many species as well as the victims of physical forces and of their own inability to find continuously satisfactory conditions for growth. The vast number of eggs produced may be realized by reference to the turbot which produces 9,000,000 in a single season, the cod with 5,000,000, and to the flounder with 1,000,000. In higher animals the reproductive energy is conserved by various means for caring for the young during early life, but in marine forms this is usually not the case. The second consequence of larval activity is to bring the growing forms into an entirely difierent range. This is illustrated in the case of the lobster, which is a bottom feeder, lurking in the crevices between stones and elsewhere to capture whatever prey may come within its reach, or feeding upon such dead forms as may be found nearby. The larvae, up to the time of the fourth molt, however, swim at the surface of the sea water. In addition to this, they are positively phototropic to light of the intensity of ordinary daylight, but the adults are negative. Thus the pelagic larvae are brought into a range of environment where their food, which consists of plankton, especially copepods, is abundant. Special structural modifications adapt these larvae to their surface pelagic life. They are the better enabled to swim on the surface of the water because of the possession of exopods, the outer branches of the walking legs characteristic of lower crustaceans but not present in the adults of the higher forms. These are retained to the fourth molt, when they are cast off, being no longer useful; the larva then goes to the bottom. Herrick makes note of several changes in structure and instincts which take place at the beginning of the fourth stage, which marks the most surprising leap in the whole history of development. Among these are the following: the primitive swimming branches of the thoracic appendages are lost; the cuticle becomes shell— like, containing more lime; the pigments are denser, the colors brilliant, and the color pattern variable; otocysts are present and orientation is perfect; rotation of the great forceps is complete; the animal, during at least a part of this stage, moves toward the light and swims steadily at the surface with the great claws directed forward and held close together; the preying instinct is more marked; the fighting instinct, the instinct of fear, “feigning,” and hiding are all developed by the close of the fourth stage or in the fifth, when the animal goes to the bottom to stay. In many other animals similar gain is accomplished by a specialized form of larval structure. The larva finds itself adapted to-securing food which is suitable for it, and structures which have only temporary employment are present and useful. It follows, however, that the gain to the larva would become a loss if the subsequent stages in the life cycle were not radically changed in such a way as to enable the organism to undertake a new mode of life. In other words, metamorphosis in such cases is a necessity for bringing about those adaptations which fit the organism to live in its permanent environment and

there to undergo those further changes which look toward the production of new germ cells.

It is not usual to find metamorphosis in animals which live in fresh water, although there are some outstanding cases in which larvae totally unlike the adult are developed in species inhabiting fresh water. It may, however, be taken as a general rule that development in freshwater forms with the exception of certain few highly specialized cases is direct. Fresh water presents a great lack of constancy in living conditions as compared with those of the sea. With but few exceptions the bodies of fresh water lack sufficient depth and area to maintain even a low degree of constancy. Fresh water becomes heated much more easily than the sea, it freezes comparatively quickly, its streams are subjected to periods of flood during which the water runs rapidly and scours out the beds or overflows, and when it recedes leaves innumerable forms of life stranded to perish. Every stream has narrows and depths where it runs rapidly and flats where its current is slow, an environment in which the fragile larvae would scarcely be able to maintain themselves, and there are but few animals which go through an independent larval history in fresh water. The lack of suitability of fresh water to larval development without doubt explains why so many groups of marine animals have not been able to gain a foothold in fresh water. A very few sponges, almost no coelenterates, occur in this environment, and many groups of marine fish and ascidians, cephalopods, king crabs, and some of the worm groups have not a single representative in fresh water. Animals that cannot produce eggs which develop into young like the adult are prevented from gaining ‘a. foothold by such a changeable medium as fresh water. In addition to the difficulties of fresh-water life already noted, a zone of brackish water between the fresh water and the sea is itself an almost impassable barrier to the entrance of marine forms.

Terrestrial life presents to developing larvae even more dangers than fresh water. To this situation is due the fact that in land forms development is either direct and fairly simple or else specialized with complicated devices for caring for the young during their immature period. The latter condition is illustrated by many forms of insects in which metamorphosis is complete, often involving very complicated life histories. Some of the disadvantageous features of the terrestrial 386 ECOLOGICAL CONTROL OF INVERTEBRATE LARVAL TYPES

environment are the following: temperature undergoes a wide range of variation, often passing quickly between the extremes. This condition is quite unknown in the ocean and is much less in fresh water. The very changeableness as well as the extremes of heat and cold are hardships for the developing larvae. The weight of the body is no longer buoyed up by water and must be supported at every moment. This involves consumption of much energy as compared with the almost passive drifting of larvae in aquatic habitats, and renders movement much more difficult and restricted. Food no longer streams by as in the contrasting case, but must be actively sought, is often very much more restricted as to kind, and presents an increased toughness since in the composition of land forms the percentage of water is much less, and the food is necessarily more difficult to find. The glare of daylight and the consequent difficulty of avoiding enemies puts the terrestrial larvae to a disadvantage which forms living in the subdued shadows of the water do not share. finally the rapid evaporation to which terrestrial forms are subjected requires special devices for protecting the soft exterior of the organism. A heavy shell, mucous glands, and other similar devices show what a serious drain upon the organism requirements of this kind cause.

These considerations account in a large measure for the lack of uniformity in the occurrence of larval types throughout the different groups of the animal kingdom. The particular forms of larvae within a group are of adaptive rather than taxonomic significance.

The general subject of the care of young animals was briefly but instructively discussed by Gamble in “The Animal World” (Holt and Company). Some of the ideas mentioned on the three preceding pages are suggested by his discussion. Gamble sums up the responses of animals to different environmental conditions in which the young must be produced as follows:* “We find isolated examples of the retention of the young by diminution in the size of the family. Speaking generally, marine animals pour their eggs broadcast, and leave their minute larvae to complete their metamorphosis unaided and unsheltered, but in every group there are malthusian species which not only restrict their families in number, but enclose them by protective envelopes. The varied experience of larval life in this curtailed and direct development supplants metamorphosis. The eggs become larger and the young stronger at birth.

“In fresh water the limitation and protection of the family is more generally the rule. Insects and Amphibia are the only large classes

‘ Quoted by permission of Henry Holt & Co.

which go through their larval life in fresh water. But the protection

is usually of the simplest kind and is confined to the earlier stages of development.

“On land the insects form the only class in which the majority still pursues a free larval history. Others develop directly, either growing up into full stature without guidance or protection, or carried and fed by their parents for some time both before and after hatching.”

Cite this page: Hill, M.A. (2026, November 3) Embryology Book - Outline of Comparative Embryology. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Book_-_Outline_of_Comparative_Embryology

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