Book - Outline of Comparative Embryology 1-10

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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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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.
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Part One General Embryology

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.


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.


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


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


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.


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


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.


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


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


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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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.

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

Cite this page: Hill, M.A. (2020, April 6) Embryology Book - Outline of Comparative Embryology 1-10. Retrieved from

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