Book - Comparative Embryology of the Vertebrates 3
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Nelsen OE. Comparative embryology of the vertebrates (1953) Mcgraw-Hill Book Company, New York.
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Part III The Development of Primitive Embryonic Form
Part III - The Development of Primitive Embryonic Form: 6. Cleavage (Segmentation) and Blastulation | 7. The Chordate Blastula and Its Significance | 8. The Late Blastula in Relation to Certain Innate Physiological Conditions: Twinning | 9. Gastrulation | 10. Tubulation and Extension of the Major Organ-forming Areas: Development of Primitive Body Form | 11. Basic Features of Vertebrate Morphogenesis
The general procedures leading to the development of primitive embryonic body form in the chordate group of animals are:
( 1 ) Cleavage. Cleavage is the division of the egg into progressively smaller cellular units, the blaslomeres (Chap. 6).
(2) Blastulation. Blastulalion results in the formation of the blastula. The blastula is composed of a cellular blastoderm in relation to a fluid-filled cavity, the blastocoel. The blastoderm of the late blastula is composed of neural, epidermal, notochordal, mesodermal, and entodermal major presumptive organ-forming areas. In the phylum Chordata, the notochordal area is the central region around which the other areas are oriented (Chap. 7). The major presumptive organ-forming areas of the late blastula exist in various degrees of differentiation (Chap. 8).
(3) Gastrulation. This is the process which effects a reorientation of the presumptive organ-forming areas and brings about their axiation antero-posteriorly in relation to the notochordal axis and the future embryonic body (Chap. 9). During gastrulation the major organ-forming areas are subdivided into minor areas or fields, each field being restricted to the development of a particular organ or part. (Pp. 378, 446, 447.
(4) Following gastrulation, the next step in the development of embryonic body form is tubulation and extension of the major organ-forming areas (Chap. 10).
(5) As tubulation and extension of the organ-forming areas is effected, the basic or fundamental conditions of the future organ systems are established, resulting in the development of primitive body form. As the development of various vertebrate embryos is strikingly similar up to this point, the primitive embryonic body forms of all vertebrates resemble each other (Chap. II).
In the drawings presented in Part III, the following scheme for designating the major organ-forming areas existing within the three germ layers is adhered to:
Cleavage (Segmentation) and Blastulation
6. Cleavage (Segmentation) and Blastulation
A. General considerations
1. Definitions
2. Early history of the cleavage (cell-division) concept
3. Importance of the cleavage-blastular period of development
a. Morphological relationships of the blastula
b. Physiological relationships of the blastula
1 ) Hybrid crosses
2) Artificial parthenogenesis
3) Oxygen-block studies
4. Geometrical relations of early cleavage
a. Meridional plane
b. Vertical plane
c. Equatorial plane
d. Latitudinal plane
5. Some fundamental factors involved in the early cleavage of the egg
a. Mechanisms associated with mitosis or cell division
b. Influence of cytoplasmic substance and egg organization upon cleavage
1) Yolk
2) Organization of the egg
c. Influence of first cleavage amphiaster on polyspermy
d. Viscosity changes during cleavage
e. Cleavage laws
1 ) Sach’s rules
2) Hertwig’s laws
6. Relation of early cleavage planes to the antero-posterior axis of the embryo
B. Types of cleavage in the phylum Chordata
1. Typical holoblastic cleavage
a. Amphioxus
b. Frog (Rana pipiens and R. sylvatica)
c. Cyclostomata
2. Atypical types of holoblastic cleavage
a. Holoblastic cleavage in the egg of the metatherian and eutherian mammals
1 ) General considerations
2) Early development of the rabbit egg
a) Two-cell stage
b) Four-cell stage
c) Eight-cell stage
d) Sixteen-cell stage
e) Morula stage
f) Early blastocyst
3) Types of mammalian blastocysts (blastulae)
b. Holoblastic cleavage of the transitional or intermediate type
1) Amhystoma maculatum (punctatum)
2) Lepidosiren paradoxa
3) Necturus maculosus
4) Acipenser sturio
5) Amia calva
6) Lepisosteus (Lepidosteus) osseus
7) Gymnophionan amphibia 3. Meroblastic cleavage
a. Egg of the common fowl
1 ) Early cleavages
2) Formation of the periblast tissue
3) Morphological characteristics of the primary blastula
4) Polyspermy and fate of the accessory sperm nuclei
b. Elasmobranch fishes
1 ) Cleavage and formation of the early blastula
2) Problem of the periblast tissue in elasmobranch fishes
c. Teleost fishes
1) Cleavage and early blastula formation
2) Origin of the periblast tissue in teleost fishes
d. Prototherian Mammalia
e. Cleavage in the California hagfish, Polistotrema (Bdellostorna) stouti
C. What is the force which causes the blastomeres to adhere together during early cleavage?
D. Progressive cytoplasmic inequality and nuclear equality of the cleavage blastomeres
1. Cytoplasmic inequality of the early blastomeres
2. Nuclear equality of the early blastomeres
E. Quantitative and qualitative cleavages and their influence upon later development
The Chordate Blastula and Its Significance
7. The Chordate Blastula and Its Significance
A. Introduction
1. Blastulae without auxiliary tissue
2. Blastulae with auxiliary or trophoblast tissue
3. Comparison of the two main blastular types
B. History of the concept of specific, organ-forming areas
C. Theory of epigenesis and the germ-layer concept of development
D. Introduction of the words ectoderm, mesoderm, endoderm
E. Importance of the blastular stage in Haeckel's theory of The Biogenetic Law of Embryonic Recapitulation
F. Importance of the blastular stage in embryonic development
G. Description of the various types of chordate blastulae with an outline of their organforming areas
1. Protochordate blastula
2. Amphibian blastula
3. Mature blastula in birds
4. Primary and secondary reptilian blastulae
5. Formation of the late mammalian blastocyst (blastula)
a. Prototherian mammal, Echidna
b. Metatherian mammal, Didelphys
c. Eutherian mammals
6. Blastulae of teleost and elasmobranch fishes
7. Blastulae of gymnophionan amphibia
Late Blastula in Relation to Certain Innate Physiological Conditions: Twinning
8. The Late Blastula in Relation to Certain Innate Physiological Conditions: Twinning
A. Introduction
B. Problem of differentiation
1. Definition of differentiation; kinds of differentiation
2. Self-differentiation and dependent differentiation
C. Concept of potency in relation to differentiation
1. Definition of potency
2. Some terms used to describe different states of potency
a. Totipotency and harmonious totipotency
b. Determination and potency limitation
c. Prospective potency and prospective fate
d. Autonomous potency c. Competence
D. The blastula in relation to twinning
1. Some definitions
a. Dizygotic or fraternal twins
b. Monozygotic or identical twins
c. Polyembryony •
2. Basis of true or identical twinning
3. Some experimentally produced, twinning conditions
E. Importance of the organization center of the late blastula
Gastrulation
A. Some definitions and concepts
1. Gastrulation
2. Primitive vertebrate body plan in relation to the process of gastrulation
a. Fundamental body plan of the vertebrate animal
b. The gastrula in relation to the primitive body plan
c. Chart of blastula, gastrula, and primitive, body-form relationships (fig. 188)
B. General processes involved in gastrulation
C. Morphogenetic movement of cells
1. Importance of cell movements during development and in gastrulation
2. Types of cell movement during gastrulation
a. Epiboly
b. Emboly
3. Description of the processes concerned with epiboly
4. Description of the processes involved in emboly
a. Involution and convergence
b. Invagination
c. Concrescence
d. Cell proliferation
e. Polyinvagination
f. Ingression
g. Delamination
h. Divergence
i. Extension
D. The organization center and its relation to the gastrulative process
1. The organization center and the primary organizer
2. Divisions of the primary organizer
E. Chemodifferentiation and the gastrulative process
F. Gastrulation in various Chordata 1. Amphioxus
a. Orientation
b. Gastrulative movements
1 ) Emboly
2) Epiboly
3) Antero-posterior extension of the gastrula and dorsal convergence of the mesodermal cells
4) Closure of the blastopore
c. Resume of cell movements and processes involved in gastrulation of Amphioxus
1 ) Emboly
2) Epiboly
2. Gastrulation in Amphibia with particular reference to the frog
a. Introduction
1) Orientation
2) Physiological changes which occur in the presumptive, organ-forming areas of the late blastula and early gastrula as gastrulation progresses
b. Gastrulation
1) Emboly
2) Epiboly
3) Embryo produced by the gastrulative processes
4) Position occupied by the pre -chordal plate material
c. Closure of the blastopore and formation of the neurenteric canal
d. Summary of morphogenetic movements of cells during gastrulation in the frog and other Amphibia
1) Emboly
2) Epiboly
3. Gastrulation in reptiles
a. Orientation
b. Gastrulation
4. Gastrulation in the chick
a. Orientation
b. Gastrulative changes
1) Development of primitive streak as viewed from the surface of stained blastoderms
2) Cell movements in the epiblast involved in primitive-streak formation as indicated by carbon-particle marking and vital-staining experiments
3) Cell movements in the hypoblast and the importance of these movements in primitive-streak formation
4) Primitive pit notochordal canal
5) Resume of morphogenetic movements of cells during gastrulation in the chick
5. Gastrulation in mammals
a. Orientation
b. Gastrulation in the pig embryo
c. Gastrulation in other mammals
6. Gastrulation in teleost and elasmobranch fishes
a. Orientation
b. Gastrulation in teleost fishes
1) Emboly
2) Epiboly
3) Summary of the gastrulative processes in teleost fishes
a) Emboly
b) Epiboly
4) Developmental potencies of the germ ring of teleost fishes
c. Gastrulation in elasmobranch fishes
7. Intermediate types of gastrulative behavior
G. The late gastrula as a mosaic of specific, organ-forming territories
H. Autonomous theory of gastrulative movements
I. Exogastrulation
J. Pre-chordal plate and cephalic projection in various chordates
K. Blastoporal and primitive-streak comparisons
Development of Primitive Body Form
10. Tubulation and Extension of the Major Organ-forming Areas: Development of Primitive Body Form
A. Introduction
1. Some of the developmental problems faced by the embryo after gastrulation
a. Tabulation
b. Increase in size and antero-posteri(*)r extension of the tubulated, major organforming areas
c. Regional modifications of the tubulated areas
2. Common, vertebrate, embryonic body form
3. Starting point for tabulation
4. Developmental processes which accomplish tabulation
a. Immediate processes
b. Auxiliary processes
5. Blastocoelic space and body-form development
6. Primitive circulatory tubes or blood vessels
7. Extra-embryonic membranes
B. Tabulation of the neural, epidermal, entodermal, and mesodermal, organ-forming areas in the vertebrate group
1. Neuralization or the tabulation of the neural plate area
a. Definition
b. Neuralizative processes in the Vertebrata
1) Thickened keel method
2) Neural fold method
c. Closure of the blastopore in rounded gastrulae, such as that of the frog
d. Anterior and posterior neuropores; neurenteric canal
2. Epidermal tabulation
a. Development of the epidermal tube in Amphibia
b. Tabulation of the epidermal area in flat blastoderms
3. Formation of the primitive gut tube (enteric tabulation)
a. Regions of primitive gut tube or early metenteron
b. Formation of the primitive metenteron in the frog
c. Formation of the tubular metenteron in flat blastoderms
4. Tabulation (coelom formation) and other features involved in the early differentiation of the mesodermal areas
a. Early changes in the mesodermal areas
1) Epimere; formation of the somites
2) Mesomere
3) Hypomere
b. Tabulation of the mesodermal areas
C. Notochordal area
D. Lateral constrictive movements
E. Tubulation of the neural, epidermal, entodermal, and mesodermal, organ-forming areas in Amphioxus
1. Comparison of the problems of tubulation in the embryo of Amphioxus with that of the embryos in the subphylum Vertebrata
a. End-bud growth
b. Position occupied by the notochord and mesoderm at the end of gastrulation
2. Neuralization and the closure of the blastopore
3. Epidermal tubulation
4. Tubulation of the entodermal area
a. Segregation of the entoderm from the chordamesoderm and the formation of the primitive metenteric tube
b. Formation of the mouth, anus, and other specialized structures of the metenteron
5. Tubulation of the mesoderm
6. Later differentiation of the myotomic (dorsal) area of the somite
7. Notochord
F. Early development of the rudiments of vertebrate paired appendages
G. The limb bud as an illustration of the field concept of development in relation to the gastrula and the tubulated embryo
H. Cephalic flexion and general body bending and rotation in vertebrate embryos
I. Influences which play a part in tubulation and organization of body form
J. Basic similarity of body-form development in the vertebrate group of chordate animals
delete
A. Introduction
1. Some of the Developmental Problems Faced by the Embryo After Gastrulation
a. Tubulation
One of the main problems, confronting the embryo immediately following gastrulation, is the tubulation of the major organ-forming areas, namely, epidermal, neural, entodermal, and the two, laterally placed, mesodermal areas. The epidermal, neural, and entodermal areas eventually form elongated, rounded tubes, whereas the mesodermal tubes are flattened. The epidermal and neural tubes extend the entire length of the developing embryo (fig. 217A-C), while the entodermal tube normally terminates at the beginning of the tail (fig. 21 7B, C), although in some instances it may extend even to the tail’s end (fig. 217A). Anteriorly, the entodermal tube ends along the ventral aspect of the developing head (fig. 217A, C). The two mesodermal tabulations are confined mainly to the trunk region of the embryo, but in the early embryo of the shark they continue forward into the head almost to the posterior limits of the developing eyes (fig. 217D). The condition of the mesodermal tubes in the Amphibia resembles to a degree that in the shark embryo (fig. 217B, E).
An important concept to grasp is that the tubulations of the respective areas occur synchronously or nearly so. It is true that the initial stages of the epidermal and entodermal tubulations slightly precede the other tubulations in
Fig. 217. Primary tubes (tubulations) of the primitive vertebrate body. (A) Schematic representation of epidermal, neural, and entodermal tubes in the early embryo of
the shark. Observe that a well-developed, post-anal or tail gut continues to the end of
the tail. (B) Gut, neural, and epidermal tubes in the amphibian type. (C) Gut,
neural, and epidermal tubes in the chick and mammal type. (D) Mesodermal tube in
the shark embryo. (E) Mesodermal tube in the amphibian embryo. (F) Mesodermal
condition in the early bird and mammal embryo. (G) Transverse section of shark
embryo, showing tubulations of major or^an-forming areas and primary coelomic conditions. (H) Transverse section of frog ^embryo shortly after closure of neural tube,
showing the five fundamental body tubes oriented around the notochord.
456
Amphioxus, in the frog, and in forms having rounded gastrulae, while in the chick the neural area is precocious. Viewed in their totality, however, the tubulations of all of the major organ-forming areas are simultaneous processes with the exception of the notochord which does not become tubulated but continues as an elongated rod of cells.
b. Increase in Size and Antero-posterior Extension of the Tubulated, Major Organ-forming Areas
Another goal to be achieved by the embryo during the immediate, postgastrular period is an increase in size, together with an antero-posterior extension of the major organ-forming areas. These changes are associated with tubulation, and they aid in producing the elongated, cylindrical form typical of the chordate body,
c. Regional Modifications of the Tubulated Areas
As tubulation of the various major organ-forming areas progresses, specific, organ-forming areas or fields (see end of chapter), located along the respective primitive body tubes, begin to express themselves and develop in a specialized manner. Thus, regional differentiation of the major organ-forming areas; comprising each primitive body tube, is another feature of the postgastrular period. As a result, localized areas along each of the body tubes show changes in shape, and specific, individualized structures begin to make their appearance. For example, the neural tubulation develops the primitive parts of the brain at its anterior end, while the posterior portion of the neural tube, caudal to the brain area, begins to form the spinal cord. Thus, the primitive brain becomes a specific peculiarity of the head region. Also, the epidermal tubulation at its cranial end contributes definite structures peculiar to the head. In the pharyngeal region, special developmental features arise in the entodermal tube together with the epidermal tube and the mesoderm. In the trunk region, modifications of the entodermal and mesodermal tubes give origin to many of the structural conditions peculiar to this area, while in the tail, the neural and epidermal tubulations together with activities of the mesoderm account for the characterstic structures of the tail appendage. These special developmental features of the respective, tubulated, organ-forming areas, which arise in specific areas along the antero-posterior axis of the embryo, occur in much the same way throughout the vertebrate group with the result that common or generalized structural conditions of the tubulated organ-forming areas appear in all vertebrate embryos. That is, the primitive brains of all vertebrate embryos up to a certain stage of development resemble each other in a striking manner; the contributions of the epidermal tubulation to the head also resemble each other, ind the early development of the pharyngeal and trunk regions is similar. As a result, the early morphogenesis
INTRODUCTION
459
organ systems conform to generalized, basic plans. After the generalized plan
of a particular system is established, it is modified in later development to fit
the requirements of the habitat in which the particular species lives. In the
cephalochordate, Amphioxus, a similar body form also develops, although it
is considerably modified.
The common, generalized, primitive embryonic body form of all vertebrate embryos possesses the following characteristics:
( 1 ) It is an elongated structure, cylindrical in shape, and somewhat compressed laterally.
(2) It is composed of five, basic, organ-forming tubes, oriented around a primitive axis, the notochord (fig. 217).
(3) It possesses the following regions: (a) head, (b) pharyngeal area, (c) trunk, and (d) tail (figs. 217, 226, 227, 230, 238, 244, 246).
In Chapter 1 1 and the following chapters, various details of these common regions and other features will be considered. In this chapter, we are concerned mainly with tabulation and antero-posterior extension of the major organ-forming areas in relation to body-form development.
3. Starting Point for Tubulation
The starting point for tubulation of the major organ-forming areas and subsequent, primitive, body formation is the gastrula; which, as observed in Chapter 9, exists in two forms, namely, rounded and the flattened gastrulae (figs. 219, 232). Many heavily yolked embryos, such as the embryo of Necturns maculosus, although they form a rounded gastrula, are faced with some of the problems of the flattened gastrulae (fig. 227). The rounded gastrulae, found in the frog, Amphioxus, etc., differ from the flattened gastrulae present in the bird, reptile, mammal, and teleost and elasmobranch fishes, mainly by the fact that, at the beginning of tubulation and body formation, the epidermal and gut areas already are partially tubulated in the rounded gastrulae. That is, in the rounded blastoderm, the initial stages of tubulation occur in these two major organ-forming areas during gastrulation. This means that the ventral portion of the trunk area in rounded gastrulae is circumscribed by intact cellular layers of the embryonic trunk region, with yolk material contained within the cell layers, while, in flattened gastrulae, the ventro-lateral portions of the trunk region are spread out flat, the yolk not being surrounded by the future, ventro-lateral walls of the embryonic trunk region. These conditions are illustrated in figures 219B and C and 234A-F.
The developmental problems faced by these two groups of gastrulae, therefore, are somewhat different. Moreover, tubulation of the organ-forming areas and the development of body form in Amphioxus varies considerably from that of the rounded gastrulae of the vertebrate group. For this reason, tubulation in Amphioxus is considered separately.
460
DEVELOPMENT OF PRIMITIVE BODY FORM
Regardless of differences, however, all vertebrate gastnilae, rounded and
flattened, possess three fundamental or basic regions, to wit, ( 1 ) a cephalic
or head region, containing the rudiments of the future head and pharyngeal
structures, (2) a trunk region, wherein lie the undeveloped fundaments of
the trunk, and (3) an end-bud or tail rudiment, containing the possibilities
of the future tail.
4. Developmental Processes Which Accomplish Tubulation
a. Immediate Processes
The term, immediate processes, signifies the events which actually produce the hollow tubular condition. In the case of the epidermal, enteric, and neural tubulations, the immediate process is mainly one of folding the particular,
BRAIN AREA
HEAD REGION
SENSORY PLATE
GILL - PLATE
AREA
TRUNK REGION
NEURAL FOLD
TAIL REGION
PRE-CHOROAL PLATE
NEURAL ECTODERM EPIDERMAL
ECTODERM
- S ODE R M \
NOTOCHORD \ D.
COELOMIC SPACE ENTODERM
NOTO CHORD NEURAL ECTODERM
VENTRAL
MESODERM
Fig. 219. Relationships of the major presumptive organ-forming areas at the end of
gastrulation in the anuran amphibia. (A) External view of gastrula, showing the ectodermal layer composed of presumptive epidermis (white) and presumptive neural plate
(black), as viewed from the dorsal aspect. (B) Diagrammatic median sagittal section
of condition shown in (A). (C) Same as (B), showing major organ-forming areas.
(D) Section through middorsal area of conditions (B) and (C), a short distance caudal to foregut and pre-chordal plate region. Observe that the notochord occupies the middorsal area of the gut roof.
INTRODUCTION
461
organ-forming area into a hollow tubular affair. With respect to the mesodermal areas, the immediate process is an internal splitting (de lamination),
whereby the mesodermal area separates into an outer and an inner layer
with a space or cavity appearing between the two layers. In the case of the
teleost fishes, a process of internal separation of cells appears to play a part
also in the neural tubulation.
b. Auxiliary Processes
Aiding the above activities which produce tubulation are those procedures which extend the tubulated areas into elongated structures. These auxiliary processes are as follows:
( 1 ) The cephalic or head rudiment, with its contained fundaments of the developing head region, grows forward as a distinct outgrowth. This anterior protrusion is known as the cephalic or head outgrowth (figs. 223A, B; 2321-L).
(2) The trunk rudiments enlarge and the trunk region as a whole undergoes antero-posterior extension (figs. 225 A; 233).
(3) The tail-bud area progresses caudally as the tail outgrowth and forms the various rudimentary structures associated with the tail (figs. 225; 230F; 238).
(4) A dorsal upgrowth (arching) movement occurs, most noticeable in the trunk area. It serves to lift the dorsal or axial portion of the trunk up above the yolk-laden area below, and the developing body tubes and primitive body are projected dorsalward (figs. 221, 224, 241).
(5) In embryos developing from rounded gastrulae, a ventral contraction and reshaping of the entire ventro-lateral areas of the primitive trunk region are effected as the yolk is used up in development. This results in a gradual retraction of this area which eventually brings the ventrolateral region of the trunk into line with the growing head and tail regions (cf. figs. 220, 223, 225 on the development of the frog, and 227 on the development of Necturus).
(6) In embryos developing from flattened gastrulae, a constriction of the ventral region of the developing trunk comes to pass. This constriction is produced by an ingrowth toward the median line of entodermal, mesodermal, and epidermal cellular layers in the form of folds, the lateral body folds. Upon reaching the midline, the cellular layers fuse as follows: The entodermal layer from one side fuses with the entodermal layer of the other; the mesodermal layers fuse similarly; and, finally, the epidermal layer from one side fuses with the epidermal layer of the opposite side. The result is a general fusion of the respective body layers from cither side, as shown in figure 24 1C and D, which establishes the ventral region of the trunk. A complete fusion throughout jLhe extent of the ventral body wall does not take place
462
DEVELOPMENT OF PRIMITIVE BODY FORM
NEURAL PLATE
.A.B. C. D. E.
NERVOUS LAYER OF
/\ EPIDERMIS NOTOCHORD
DORSAL
DIVERTICULUM
OF
HINDGUT
BRAIN AREA
NEUROCOEL
NEURENTERIC CANAL
DORSAL PROJECTION U
^ OF HINDGUT
CLOSING BLASTOPORE HINDGUT PROCTOOAEUM
ORAL'^
VENTRAL DIVERTlCULUf
DIVERTICULUM OF HINDGUT
, VENTRAL
_ _ DIVERTICULUM
MESENCHYME 7" - OF HINDGUT
LIVER DIVERTICULUM
Fig. 220. Beginning neural fold stage of frog embryo from prepared material. (A)
Beginning neural fold stage as seen from dorsal view. (B) Sagittal section near median
plane of embryo similar to that shown in (A). (C) Same as (B), showing organ
forming areas. (D) Midsagittal section of caudal end of frog embryo slightly younger
than that shown in fig. 223 B. Observe that the blastopore practically is closed, while the
dorsal diverticulum of the hindgut connects with the neurocoel to form the neurenteric
canal. Observe, also, ventral diverticulum of hindgut.
until later in development, and, as a result, a small opening remains,
the umbilicus, where the embryonic and extra-embryonic tissues are
continuous. This discontinuity of the embryonic layers permits the
blood vessels to pass from the embryonic to the extra-embryonic regions. (Note: In the teleost fishes, although a typical, flattened, gastrular form is present, the formation of the ventral body wall of the
trunk through a general retraction of tissues resembles that of the
rounded gastrulae mentioned above.)
5. Blastocoelic Space and Body-form Development
During the terminal phases of gastrulation in such forms as Amphioxus and the frog, the blastocoel, as a spacious cavity, disappears for the most part. Its general area is occupied by cells which migrated into the blastocoel
INTRODUCTION
463
during gastrulation. However, the disappearance of the blastocoelic space
is more apparent than real. For, while most of the original blastocoelic space
is thus occupied and obliterated, a part of the original blastocoel does remain
as an extremely thin, potential area between the outside ectoderm and the
mesoderm-entoderm complex of cells. In flattened blastoderms, as in the
chick, the actual space between the ectoderm, mesoderm, and entoderm is
considerable (fig. 234E, F). To sum up: Though the blastocoelic space appears to disappear during the terminal phases of gastrulation, a residual or
potential space remains between the three germ layers, more pronounced in
some species than in others. This residual space gradually increases during
the tubulation processes of the major organ-forming areas. In doing so, it
permits not only the tubulation of these areas within the outside ectoderm,
but it allows important cell migrations to occur between the various body tubes.
6. Primitive Circulatory Tubes or Blood Vessels
Accompanying the tubulations of the epidermal, neural, entodermal, and the two mesodermal areas on either side of the notochord, is the formation
BRAIN AREA OF NEURAL
DORSAL
DIVERTICULUM
OF HINOGUT
VENTRAL
DIVERTICULUM
OF HINDGuT
liver diverticulum
CLOSING BLASTOPORE
Fig. 221. Transverse sections through early neural fold embryo of the frog as shown in fig. 220A and B. (A-J) Sections are indicated in fig. 220B by lines A-J, respectively. Observe that the dorsal arching (dorsal upgrowth) movement of the dorsally situated tissues accompanies neural tube formation.
464
DEVELOPMENT OF PRIMITIVE BODY FORM
Fig. 222. Neural crest cells in Amhystoma punctatum. (A and B from Johnston:
Nervous System of Vertebrates, Philadelphia, Blakiston, ’06; C-F from Stone: J. Exper.
Zool., ’35.) (A) Transverse section of early neural tube of Am by stoma, neural crest
cells located dorsally and darkly shaded. (B) Later stage than (A), showing relation of neural crest cells, epidermis, and neural tube. (C-F) Neural crest cells stippled, placodes of special lateral line sense organs and cranial nerve ganglia shown in black. The neural crest cells arise from dorsal portion of neural tube at points of fusion of neural folds and migrate extensively. A considerable portion of neural crest cells descends upon the mesoderm of visceral arches as indicated in (D-F) and contributes mesodermal cells to these arches, where they later form cartilaginous tissue.
of a delicate system of ve.ssels which function for the transport of the circulatory fluid or blood. The formation of these blood vessels begins below the
forming entodermal tube as two, subenteric (subintestinal) tubes or capillaries.
These capillaries grow forward below the anterior portion of the forming
digestive tube. Near the anterior end of the latter, they separate and pass
upward on either side around the gut tube to the dorsal area, where they come
together again below the notochord and join to form the rudiments of the
dorsal aortae. The latter are two delicate supraenteric capillaries which extend from the forming head area caudally toward the trunk region. In the
TUBULATION OF ORGAN-FORMING AREAS
465
latter region, each rudiment of the dorsal aorta sends a small, vitelline blood
vessel laterally into that portion of the gut tube or yolk area containing the
yolk or other nutritional source. In the yolk area, each joins a plexus of
small capillaries extending over the surface of the yolk substance. These
capillaries in turn connect with other capillaries which join ultimately each of
the original subintestinal blood capillaries. Below the anterior or foregut portion of the entodermal tube, the two subintestinal blood vessels fuse and thus
form the beginnings of the future heart (figs. 234-237; 332). The further
development of this system of primitive vessels is described in Chapter 17.
7. Extra-embryonic Membranes
Associated with the development of body form and tubulation of the major, organ-forming areas, is the elaboration of the very important extra-embryonic membranes. As the essential purpose at this time is to gain knowledge of the changes concerned with tubulation of the major organ-forming areas and the development of primitive body form, consideration of these membranes is deferred until Chapter 22. The latter chapter is concerned with various activities relating to the care and nutrition of developing embryos of various vertebrate species.
B. Tubulation of the Neural, Epidermal, Entodermal, and Mesodermal, Organ-forming Areas in the Vertebrate Group
1. Neuralization or the Tubulation of the Neural Plate Area
a. Definition
The separation of the neural plate material from the skin ectoderm, its migration inward, and its formation into a hollow tube, together with the segregation of the accompanying neural crest cells, is called neuralization.
b. Neuralizative Processes in the Vertebrata
Neuralization is effected by two general procedures in the vertebrate subphylum.
1) Thickened Keel Method. In tcleost, ganoid, and cyclostomatous fishes, the neural plate material becomes aggregated in the form of a thickened, elongated ridge or keel along the middorsal axis of the embryo (figs. 21 OF; 218C). This keel separates from, and sinks below, the overlying skin ectoderm (fig. 218A). Eventually the keel of neural cells develops a lumen within its central area and thus gradually becomes transformed into an elongated tube, coincident with the tubulations of the other major organ-forming areas (fig. 218B). In the cyclostomatous fish, Petromyzon planeri, although neuralization closely resembles the condition in teleost fishes, in certain respects the behavior of the neuralizative changes represents an intermediate condition
466
DEVELOPMENT OF PRIMITIVE BODY FORM
Fig. 223. Early neural tube stage of the frog, Rana pipiens, 2Vi to 3 mm. in length.
(A) Dorsal view, (B) Midsagittal section of embryo similar to (A). (C) Same as
(B) , showing organ-forming areas. Abbreviations: V. HD. = ventral hindgut divertic ulum; D. HD, = dorsal hindgut diverticulum; PHAR. ~ pharyngeal diverticulum of foregut. (D) Later view of (A). (E) Sec fig. 224.
between the keel method of the teleost and neural fold method of other vertebrates described below (Selys-Longchamp.s, ’10).
2) Neural Fold Method* In the majority of vertebrates, the neural (medullary) plate area folds inward (i.e., downward) to form a neural groove. This neural groove formation is associated with an upward and median movement of the epidermal layers, attached to the lateral margins of the neural plate, as these margins fold inward to form the neural folds. A change of position in the mesoderm also occurs at this time, for the upper part which forms the somites shijts late rad from the notochordal area to a position between the forming neural tube and the outside epidermis. This mesodermal migration permits the neural tube to invaginate downward to contact the notochordal area. Also, this change in position of the somitic mesoderm is a most important factor in neuralization and neural tube development as mentioned at the end of this chapter. {Note: In this stage of development, the embryo is often de
468
DEVELOPMENT OF PRIMITIVE BODY FORM
RHOMBENCEPHALON MESENCEPHALON PROSENCEPHALON
NEURAL TUBE
EPIPHYSIS
^ HEART RUDIMENT INFUNDIBULUM^^ ORAL EVAGINATION ORAL SUCKER NEURAL TUBE SUBN OTOCHORDAL HEAD GUT
(3VrOCT0DAEUM
I'^ANAL OPENING
RECTUM
VENTRAL MESODERM
NOTOCHORD
FOREGUT’
DIVERTICULUM
Fig. 225. Structure of 3’/2- to 4-mm. embryo of Rana pipiens (about eight pairs of
somites are present). (See fig. 226A and B for comparable external views of lateral and
ventral aspects of 5-mm., .yy/v6i//ca embryo.) (A) External dorsal view. (B) Midsagittal view. (C) Same, showing major organ-forming areas.
scribed as a neurula, especially in the Amphibia. However, in the bird and the mammal, the embryo during this period is described in terms of the number of somitic pairs present, and this stage in these embryos is referred to as the somite stage.) Each lateral neural fold continues to move dorsad and mesad until it meets the corresponding fold from the other side. When the two neural folds meet, they fuse to form the hollow neural tube and also complete the middorsal area of the epidermal tube (cf. figs. 221, 224, 233, 234, 236, 237, 242, 245A). As a general rule, the two neural folds begin to fuse in the anterior trunk and caudal hindbrain area. The fusion spreads anteriad and posteriad from this point (figs. 223, 229, 233, 235, 242, 245A). It is important to observe that there are two aspects to the middorsal fusion process:
(a) The lateral edges of the neural plate fuse to form the neural tube; and
(b) the epidermal layer from either side fuses to complete the epidermal layer above the newly formed neural tube.
Associated with the fusion phenomena of the epidermis and of the neural tube, neural crest cells are given off or segregated on either side of the neural tube at the point where the neural tube ectoderm separates from the skin
TUBULATION OF ORGAN-FORMING AREAS
469
ectoderm (figs. 221C-E; 23 4B; 236B). The neural crest material forms a
longitudinal strip of cells lying along either side of the dorsal portion of the
neural tube. As such, it forms the neural or ganglionic crest. In some vertebrate embryos, as in the elasmobranch fish, Torpedo, and in the urodele,
Ambystoma, the cells of the neural crest are derived from the middorsal part
of the neural tube immediately after the tube has separated from the skin
ectoderm (epidermis). (See fig. 222A, B.) In other vertebrates, such as the
frog, chick, and human, the neural crest material arises from the general area
of junction of neural plate and skin ectoderm as fusion of the neural folds is
consummated (fig. 234B).
The neural crest gives origin to ganglionic cells of the dorsal root ganglia of the spinal nerves and the ganglia of cranial or cephalic nerves as described in Chapter 19. Pigment cells also arise from neural crest material and migrate extensively within the body, particularly to the forming derma or skin, peritoneal cavity, etc., as set forth in Chapter 12. A considerable part of the mesoderm of the head and branchial area arises from neural crest material (fig. 222C-F). (See Chapters 11 and 15.)
As the neural plate becomes transformed into the neural tube, it undergoes extension and growth. Anteriorly, it grows forward into the cephalic outgrowth, in the trunk region it elongates coincident with the developing trunk, while posteriorly it increases in length and forms a part of the tail outgrowth.
f. Closure of the Blastopore in Rounded Gastrulae, such as that of
the Frog
Neuralization and the infolding of the neural plate cells begins in the frog and other amphibia before the last vestiges of the entoderm and mesoderm have completed their migration to the inside. As mentioned above, the neural folds begin, and fusion of the neural tube is initiated in the anterior trunk region. From this point, completion of the neural tube continues anteriad and posteriad. As the neural tube proceeds in its development caudally, it reaches ultimately the dorsal lip of the now very small blastopore. As the neural tube sinks inward at the dorsal blastoporal lip, the epidermal attachments to the sides of the infolding neural tube fuse in a fashion similar to the fusion of the edges of the neural tube to complete the dorsal epidermal roof. Associated with this epidermal fusion at the dorsal lip of the blastopore is the fusion of the epidermal edges of the very small blastopore. The extreme caudal end of the archenteron or blastoporal canal in this manner is closed off from the outside (fig. 220D), and the posterior end of the archenteron (the future hindgut area), instead of opening to the outside through the blastoporal canal, now opens into the caudal end of the neural tube. In this way, a canal is formed connecting the caudal end of the future hindgut with the neural tube. This neurenteric union is known as the neurenteric canal.
It is to be observed in connection with the closure of the blastopore and
Fig. 226. External views of embryos of Rana sylvatica and Rana pi pie ns. (A to J
after Pollister and Moore: Anat. Rec., 68; K and L after Shumway: Anat. Rec., 78.)
(A, B) Lateral and ventral views of 5-mm. stage. Muscular movement is evident at this
stage, expressed by simple unilateral flexure; tail is about one-fifth body length. (Pollister
and Moore, stage 18.) (C, D) Lateral and ventral views of 6-rnm. stage. Primitive
heart has developed and begins to beat; tail equals one-third length of body. (Pollister and Moore, stage 19.) (E, F) Similar views of 7-mm. stage. Gill circulation is established; hatches; swims; tail equals one-half length of body. (Pollister and Moore, stage 20.) (G, H) Ten-mm. stage, lateral and dorsal views. Gills elongate; tail fin is well developed and circulation is established within; trunk is asymmetrical coincident with posterior bend in the gut tube; cornea of eyes is transparent; epidermis is becoming transparent. (Pollister and Moore, stage 22.) (1, J) Eleven-mm. stage, true tadpole shape. Oper cular fold is beginning to develop and gradually growing back over gills. (K, L) Eleven-mm. stage of R. pipiens embryo. Observe that opercular folds have grown back over external gills and developing limb buds; opercular chamber opens on left side of body only. Indicated in fig. 257B.
470
TUBULATION OF ORGAN-FORMING AREAS
471
the formation of the neurenteric canal that two important changes occur in
the future hindgut area of the archenteron at this time, namely, the posterior
dorsal end of the archenteron projects dorso-caudally to unite with the neural
tube (fig. 220D), while the posterior ventral end of the archenteron moves
ventrad toward the epidermis where it meets the epidermal invagination, the
proctodaeum (fig. 220D).
d. Anterior and Posterior Neuropores; Neurenteric Canal
The fusion of the neural folds in the middorsal area proceeds anteriad and posteriad from the anterior somitic and hindbrain region as described above. At the anterior end of the forebrain when fusion is still incomplete, an opening from the exterior to the inside of the neural canal is present; it forms the anterior neuropore (figs. 229D; 23 IL; 235B; 242E-G; 245B). When fusion is complete, this opening is obliterated. The caudal end of the neural tube closes m a similar manner, and a posterior neuropore is formed (figs. 242E, G; 245). In the chick, as in the mammal, the posterior neuropore at first is a wide, rhomboidal-shaped trough, known as the rhomboidal sinus. The anterior end of the primitive streak is included within the floor of this sinus rhomboidalis (fig. 235A, B). The point of posterior neuroporal closure is at the base of the future tail in most vertebrates (fig. 245B), but, in the elasmobranch fishes, this closure is effected after the tail rudiments have grown caudally for some distance (fig. 229B-E).
The vertebrate tail arises from a mass of tissue, known variously as the tail bud, caudal bud, or end bud, and the posterior end of the neural tube comes to lie in the end-bud tissues (figs. 225, 238C). The end bud grows caudally and progressively gives origin to the tail. It consists of the following:
(a) the epidermal tube (i.e., the ectodermal covering of the end bud); within this epidermal layer are
(b) the caudal end of the neural tube;
(c) the caudal end of the notochord;
(d) mesoderm in the form of a mass of rather compact mesenchyme surrounding the growing caudal ends of the notochord and neural tube; and
(e) a caudal growth from the primitive intestine or gut.
This extension of the gut tube into the tail is called, variously, the tail gut, caudal gut or post-anal gut. It varies in length and extent of development in embryos of different vertebrate species. In some species it is joined to the neural tube; in others it is not so united. For example, the tail gut is as long as the trunk portion of the gut in the young shark embryo of 8 to 10 mm. in length, and at the caudal extremity it is confluent with the neural tube (figs. 21 7A; 229F). The confluent terminal portions of the neural and gut tubes form the neurenteric canal. This well-developed neurenteric canal extends
TUBULATION OF ORGAN-FORMING AREAS
473
around the caudal end or base of the notochord. In the developing frog on the
other hand, the confluence between the neural and gut tubes is present only during the initial stages of tail formation, and it thus represents a transient relationship (fig. 223B, C). Consequently, as the tail bud in the frog embryo grows
caudally, the neurenteric connection is obliterated and the tail gut disappears.
On the other hand, in the European frog, Bombinator, the condition is intermediate between frog and shark embryos (fig. 228). True neurenteric canals
within the developing tail are never formed in the reptile, chick, or mammal,
although a tail or post-anal gut, much abbreviated, develops in these forms.
(See paragraph below.) In teleost fishes, Kupffer’s vesicle possibly represents
a small and transient attempt to form a neurenteric canal (fig. 210G). However, the tail gut here, with the exception of the terminally placed Kupffer’s
Fig. 227. Stages of normal development of Necturus maculosus. (Slightly modified
from Eycleshymer and Wilson, aided by C. O. Whitman; Chap. 1 1 in Entwicklungsgeschichte cl. Wirheltiere, by F. Keibel, ’10.) (A) Stage 15, 14 days, 19 hours after
fertilization. Blastopore is circular and reduced; neural groove is indicated in center of figure. (B) Stage 18, 17 days, 2 hours old. Blastopore is an elongated, narrow aperture between caudal ends of neural folds; neural folds prominent and neural groove is deeper. (C) Stage 21, 18 days, 15 hours old, 3 or 4 pairs of somites. Neural folds are widely separated in head region, narrower in trunk, and coalesced in tail area. (D) Stage 22, 20 days, 10 hours, 6 pairs of somites, length about 6 mm. Observe head has three longitudinal ridges, the middle one represents developing brain, while lateral ones are common anlagen of optic vesicles and branchial arches. (E) Stage 23, 21 days, 2 hours, 10 to 12 pairs of somites, 7 mm. long. Head projects forward slightly above egg contour; end of tail is prominent; large optic vesicles protrude laterally from head area; branchial arch region is caudal to optic vesicle enlargement; anus is below tip of tail. (F) Stage 24, 22 days, 17 hours, 16 to 18 pairs of somites, 8 mm. long. Anterior half of head is free from egg contour; optic vesicles and mandibular visceral arch are well defined. (G) Stage 25, 23 days, 10 hours, 20 to 22 pairs of somites, 9 mm. long. Head is free from egg surface; tail outgrowth is becoming free; mandibular, hyoid, first branchial and common rudiment of second and third branchial arches are visible. Otic vesicle lies above hyoid arch and cleft between hyoid and first branchial arches. (H) Stage 26, 24 days, 22 hours, 23 to 24 pairs of somites, length-^10 mm. Head and caudal outgrowths are free from egg surface; heart rudiment is shown as darkened area below branchial arches; cephalic flexure of brain is prominent. (1) Stage 27, 26 days, 26 to 27 myotomes, length — 1 1 mm. Outline of body is straighter; nasal pits and mouth are well defined, mandibular arches are long; heart is prominent below branchial arches; anterior limb buds are indicated; faint outlines of posterior limb buds are evident. (J) Stage 28, 30 days, 8 hours, 30 to 31 myotomes, length — 13 mm. Trunk of embryo is straight, head and tail are depressed; surface of yolk is covered by dense network of capillaries; vitelline veins are prominent; pigment appears below epidermis; anterior limb bud projects dorsally; nuchal or neck flexure is prominent above heart and limb-bud area. (K) Stage 29, 36 days, 16 hours, 36 to 38 myotomes, length — 16 mm. Mandibular arches are forming lower jaw; nuchal and tail flexures are straightening; eye and lens are well defined; anlagen of gill filament are present on gill bars; pigment cells are evident on head areas; vitelline veins are prominent; yolk-laden, ventro-lateral portion of trunk is becoming elongated and contracted toward dorsal region of embryo. (L) Stage 30, 40 days, 20 hours, 44 to 46 myotomes, length — 18 mm. Fore and hind limb buds are prominent; nasal openings are small. (M) Stage 31, larva 49 days, 21 mm. (N) Stage 32, larva 61 days, 25 mm. (O) Stage 33, larva 70 days, 28 mm. (P) Stage 34, larva 97 days, 34 mm. (Q) Stage 35, young adult form, 126 days, 39 mm.
474
DEVELOPMENT OF PRIMITIVE BODY FORM
Fig. 228. Sagittal section, showing organ-forming areas of Bomhinator embryo. (After O. Hertwig: Lehrhuch der Entwicklungsgeschkhte des Menschen und der Wirbeltiere. 1890. Jena, G. Fischer.) Observe elongated tail gut.
vesicle, is a solid mass of cells. Thus, the shark and Bomhinator embryos, on the one hand, and the frog, chick, or mammal embryo, on the other, represent two extremes in the development of the tail gut in the vertebrate group.
In the reptiles, also in some birds, such as the duck, in the human embryo, and certain other mammals, a transient notochordal-neural canal is present which connects the enteron or gut tube with the caudal area of the forming neural tube (figs. 200B, E; 207B; 23 IG-K). This canal is occasionally referred to as a neurenteric canal. However, it is best to view this condition as a special type of development within the above group, for it is not strictly comparable to the neurenteric canal formed in the developing tail of the embryos of the frog, shark, etc., where the neurenteric canal is formed by a definite union between neural and taihgut tubes as they project caudalward into the tail rudiment.
2. Epidermal Tubulation
The formation of the external, epidermal, tubular layer of the vertebrate body is a complex procedure. Its development differs considerably in the rounded type of gastrula of the Amphibia from that in the flattened gastrula of the chick or mammal.
a. Development of the Epidermal Tube in Amphibia
In the frog and other Amphibia, tubulation of the epidermal area of the blastula begins during gastrulation. At the end of gastrulation, the changes involved in epiboly have transformed the ectodermal area of the blastula into an oval-shaped structure, surrounding the internally placed mesoderm and entoderm (fig. 219). The neural plate material occupies the middorsal area of this oval-shaped, ectodermal layer, while the future epidermal area forms the remainder. Following gastrulation, the anterior end of this oval-shaped structure, in harmony with the forming neural tube, begins to elongate and
TUBULATION OF ORGAN-FORMING AREAS
475
grows forward as the head outgrowth (figs. 220, 223, 225). A cylindrical,
epidermal covering for the entire head, in this manner, is produced as the
cranial or brain portion of the neural plate folds inward (invaginates). A
similar outgrowth in the tail area proceeds posteriorly, although here the
neural tube grows caudally by proliferative activity within the epidermal tube
instead of folding into the epidermal tube as it does in the cephalic outgrowth
(figs. 223, 225). Coincident with these two outgrowths, the trunk area, with
its ventral, yolk-filled, entodermal cells, elongates antero-posteriorly as the
neural plate folds inward. It also grows larger in harmony with the head and
tail outgrowths. VAs these activities continue, yolk substance is used up, and
Fig. 229. Early stages of tubulation of neural and epidermal organ-forming areas with resultant body-form development in the shark, Squaliis acanthias (drawn from prepared slides). Neural area shown in black; epidermal area is stippled white; neural folds are outlined in white around edges of black area. (Consult also fig. 230.) (A) Embryonic
area is raised upward; neural plate is flattened; bilateral tail outgrowths are indicated. (B) Embryo is considerably elevated from extra-embryonic blastoderm; brain area is much expanded; trunk region of neural groove is pronounced. (C) Neuralization is considerably advanced; tail rudiments are converging. (D) Neural and epidermal areas are well tubulated; tail rudiments are fusing. (E) Young Squalus embryo, lying on left side; tail rudiments are fused into single caudal outgrowth. The body now consists of a flexed cephalic outgrowth, trunk region, and tail outgrowth. (F) Squalus embryo of about 10 mm. in length.
476
DEVELOPMENT OF PRIMITIVE BODY FORM
the ventro-lateral region of the trunk is retracted. A cylindrical shape of the
trunk region thus is established, bringing the trunk area into harmony with
the head and tail outgrowths. (Study particularly fig. 227.) The epidermal
area of the late gastrula thus becomes converted into an elongated, epidermal
tube which forms the external covering or primitive skin (see Chap. 12) for
the developing body. In Amphibia, this primitive epidermal tube is two layered,
consisting of an outer epidermal ectoderm and an inner neural ectoderm (figs.
221, 224). (See Chap. 12.) In the newly hatched larva, the epidermis is
extensively ciliated in all anuran and urodele Amphibia.
b. Tubulation of the Epidermal Area in Flat Blastoderms
In the flat blastoderms of the elasmobranch fish, chick, reptile, and mammal, the formation of the external body tube involves processes more complicated than that of the frog type. The following steps are involved:
( 1 ) A head fold produces a cephalic epidermal extension above the general tissues of the blastoderm. This rudimentary fold of the epidermis contains within it a similar fold of the entodermal layer, together with the invaginating, neural plate material. The notochordal rod lies between the forming entodermal fold and developing neural tube (figs. 213F; 230A; 232I-L; 242B, C). Shortly, the primitive head fold becomes converted into a cylindrical head outgrowth of the epidermal and entodermal layers, associated with the forming neural tube and notochord (figs. 229C, D; 230C; 233). The general process is similar to that in the frog, but it is more complicated in that the head rudiment first must fold or project itself up above the extra-embryonic areas, before initiating the outgrowth process.
(2) A second procedure involved in epidermal tubulation in flattened blastoderms is the dorsal upgrowth movement of epidermal, mesodermal, and entodermal tissues. This activity lifts the trunk region of the embryo up above the general blastodermic tissues (figs. 213H-J; 234B; 241 ). In some forms, such as the chick, the dorsal upgrowth movement is more pronounced in the anterior trunk area at first, gradually extending caudad to the trunk region later (figs. 233, 235). However, in the pig, human, and shark embryos, the dorsal elevation extends along the entire trunk area, coincident with the head outgrowth, and thus quickly lifts the embryonic body as a whole up above the extra-embryonic tissues (figs. 229, 230, 242, 245).
(3) The tail outgrowth, in reptiles, birds, and mammals, begins in a manner similar to that of the head region, and a tail fold first is developed which later becomes a cylindrical projection, bounded externally with epidermal cells, within which are found the notochord, tail mesoderm, and tail portions of neural and gut tubes (figs. 238C; 239K, L; 245B).
B.
X / Gill pouches I ANO II
INFUNOiBULUM-OOk'y PRE-ORAL GUT
PRE-SOMITE MESODERM FIRST GILL CLEFT NOTOCHORD
TBirPMINAL CREST \ FACIAL ACOUSTIC CREST
X. V \ / GLOSSOPHARYNGEAL CREST S U B N 0 T 0 C H 0 R D A L ROD
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Fig. 230. Sagittal sections of early elasmobranch embryos. (Slightly modified from
Scammon. See Chap. 12 in Entwicklungsgesclnchte d. Wirheltiere, by F. Keibel. ) (A)
Graphic reconstruction from sagittal sections of embryo of 2 mm., seen from left side (condition roughly comparable to stage between fig. 229A and B). Observe that neural plate is broad and flattened with slight elevation of neural folds. (B) Reconstruction of embryo of 2.7 mm., viewed from left side, showing mesoderm, forming gut, neural tubes, etc. (Consult (C) below.) (C) Same as (B) with mesoderm removed. Observe primitive gut and neural tubes. Note: (B) and (C) are comparable to stage shown in surface view in fig. 229C. (D, E) Same as (B) and (C), embryo 3.5 mm. in length.
(This embryo is comparable to fig. 229D.) (F) Same as (D) with mesoderm removed,
showing primitive vascular tubes and neural crest cells.
FOURT M CLE AVAGE
EIGHT-CELL STAGE^
'Tight-cell stage following third cleavage,
EGG INTACT Blastoderm removed from egg MARGINAL CELLS CENTRAL CELLS^^.
FIFTH CLEAVAGE
N l) T 0 CmOH D AL CANAL EPIMERIC MESODERM ep'permal Tube head outgrowth
( EC TO DERM 1 /
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Fici. 231. Series of diagrams, showing stages in the development of the turtle. (A~F)
Cleavage stages after Agassiz. (G J ) Stages of gastrulation, drawn from slide preparations. (K T) Stages during development of body fiirm. (P, Q, T from Agassiz; the
others are original.) (See L. Agassiz, 1857, Cont. Nat. Hist, of U. S. A., Vol. 11.)
479
Fig. 232. Early post-gastrular development in the chick. (A-H represent a late
head-process stage-— stage 5 of Hamburger and Hamilton, ’51. Compare with figure
203D I-L show the beginnings of the head fold — intermediate condition between stages
7 and 8 of Hamburger and Hamilton, ’51.) (A) Surface view, showing primitive streak,
neural plate, and epidermal areas. (B-F) Cross sections of A at levels indicated on G. (G) Median sagittal section of (A). (H) Same, showing presumptive, organ forming areas of entoderm notochord, pre-chordal plate, neural plate, and primitive-streak mesoderm. (1) Surface view, demonstrating a marked antero-posterior extension of the neural plate area and beginnings of neural folds. Observe shortening of primitive streak. (J) Drawing of stained specimen. (K) Median sagittal section of (J). (L) Same,
showing major organ-forming areas. In (G) and (H) the entoderm, notochord, and overlying neural ectoderm are drawn as separate layers. Actually, however, at this stage, the three layers are intimately associated.
480
TUBULATION OF ORGAN-FORMING AREAS
481
Fig. 233, Early body-form development in chick of 3 to 4 pairs of somites. (Approximately comparable to Hamburger and Hamilton, ’51, stage 8, 26 to 29 hours of incubation.) (A) Surface view, unstained specimen. (B) Stained, transparent preparation. Observe blood islands in caudal part of blastoderm. (C) Median sagittal section. (D) Same as (C), showing organ-forming layers.
direction of the notochord is much more pronounced in the flattened blastoderms than in the rounded blastoderms of the frog, salamander, etc. (cf. figs. 224; 237). {Note: Associated with the dorsal invagination of the roof of the midgut in the frog, is the detachment of a median rod of entodermal cells from the middorsal area of the gut. This median rod of cells comes to lie between the notochord and the roof of the midgut. It is known as the subnotochordal rod (fig. 225C). (See Chapter 15.)
The development of the rudimentary hindgut is consummated by caudal
482
DEVELOPMENT OF PRIMITIVE BODY FORM
growth and extension of the posterior or tail region of the primitive archenteron of the late gastrula. These changes result in an extension of the
archenteron in the direction of the developing tail and the area ventral to the
tail (compare fig. 220B-D with figs. 223B, C; 225B, C).
Three general areas of the primitive gut are thus established:
(a) a tubular enlargement and outgrowth into the developing head, the primitive foregut,
(b) a tubular extension and growth in the caudal region toward the tail, the primitive hindgut, and
(c) a midgut area whose ventral wall is filled with yolk substance, while its roof or dorsal wall assumes a trough-like form extending below the notochord (figs. 223, 224, 225).
The foregut and hindgut areas at this time present the following special features:
( 1 ) Two terminal diverticula or evaginations evolve at the extreme anterior portion of the foregut; and
(2) at the extreme caudal end of the hindgut, similar evaginations occur.
In the foregut region, one of these evaginations projects toward the brain and anterior end of the notochord, while the second diverticulum, more pronounced than the dorsal evagination, moves ventrad toward the epidermis underlying the developing brain. The dorsal evagination represents the preoral or head gut. In the frog it is much abbreviated (figs. 220B, C; 225B, C). On the other hand, the antero-ventrally directed, oral, or pharyngeal, evagination is relatively large and projects toward the ectoderm underlying the brain where it forms the future pharyngeal area of the foregut (figs. 220; 223; 225B, C). Ultimately an invagination from the epidermis, the stomodaeum, becomes intimately associated with the anterior end of the pharyngeal evagination (see Chap. 13). In the hindgut region, the diverticulum which projects dorsally into the tail is the tail gut, whereas the ventral evagination toward the epidermis below the tail represents the future rectal and cloacal areas of the hindgut (figs. 220; 223; 225B, C). It shortly becomes associated with an invagination of the epidermis, the proctodaeum (fig. 223B, C). As previously mentioned, the tail gut may be well developed, as in the European frog, Bombinator (fig. 228), or quite reduced, as in the frog, Rana (fig. 225).
c. Formation of the Tubular Metenteron in Flat Blastoderms
The development of the cylindrical gut tube in those vertebrate embryos which possess flattened gastrulae is an involved, complicated affair. The developmental mechanics are not clearly understood. For example, it is not clear whether the embryonic layers, lying in front of the head fold in figure 23 2G and H, are folded slightly backward in figures 232K and L and still farther
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Fig. 234. Transverse sections of chick embryo with five pairs of somites. (This embryo is slightly older than that shown in fig. 233; a topographical sketch of this developmental stage is shown at the bottom of the figure with level of sections indicated.) Observe that a dorsal arching (dorsal upgrowth) movement of the dorsal tissues is associated with neural tube formation. See A and B.
483
484
DEVELOPMENT OF PRIMITIVE BODY FORM
caudad in figure 23 3C and D by autonomous activities within this tissue, or
whether the actively growing head outgrowth proceeds so rapidly that it
mechanically causes the area in front of the head fold to rotate backward
under the developing foregut and thus contribute to the foregut floor. It is
obvious, however, that the entodermal material, lying in front of the head
fold of the embryo, is folded backward, at least slightly, and thus becomes
a part of the floor of the foregut. The extent, however, varies considerably in
different species. It appears to be greater in the mammal (fig. 242C) than in
the chick. Another example suggesting the integration of different movements
of cellular layers is presented in the formation of the floor of the hindgut of
the developing pig embryo. In figure 242C, the rudiments of the fore gut and
hindgut areas are established. However, in figure 242G, it is difficult to evaluate how much of the floor of the hindgut in this figure is formed by actual
ingrowth forward from point “a†and to what extent the floor is formed by
the rapid extension of tissues and backward growth of the caudal region of
the embryo as a whole, including the allantoic diverticulum.
Special processes also aid the formation of foregut and hindgut in many instances. For example, in the chick, the floor of the foregut is established in part by a medial or inward growth and fusion of the entodermal folds along the sides of the anterior intestinal portal, as indicated by the arrows in figure 234C. A similar ingrowth of entoderm occurs in the shark embryo (fig. 213J). although here the entoderm grows in as a solid layer from either side and is not present in the form of a lateral fold, as in the chick. However, it should be observed that the formation of the hindgut in the shark embryo arises by a most interesting and extraordinary method. In the flattened gastrulae of reptiles, birds, and mammals, the hindgut is established by the formation of tail folds, involving entodermal and epidermal layers. In the shark embryo, on the other hand, an enteric groove with enteric folds is formed, and the folds eventually move ventrad and fuse to form a hollow tube beneath the notochord of the developing tail.
Though the rudimentary foregut and hindgut areas of the metenteron arise almost simultaneously in mammalian embryos, such as in the pig and human embryos, in the chick a different sequence of procedure is present. In the latter species the foregut begins its development immediately following gastrulation when the first pairs of somites are present (fig. 233). The hindgut, on the other hand, begins its development at a considerably later period when the embryo has attained many pairs of somites (fig. 238).
Once the rudimentary, pouch-like, foregut and hindgut areas have been established in embryos developing from flattened gastrulae, their further development assumes morphogenetic features similar to those in the frog embryo. For example, the foregut possesses an antero-dorsal prolongation toward the brain, the pre-oral or head gut, while slightly posterior to the pre-oral gut, the future pharyngeal area makes contact ventrally with the stomodaeal in
TUBULATION OF ORGAN-FORMING AREAS
485
vagination from the epidermal (ectodermal) tube (fig. 242G). Similarly, the
caudal region of the hindgut rudiment contacts the proctodaeal invagination
of the epidermal tube, while a tail gut extension continues into the tail (fig.
217).
The formation of definitive walls of the midgut area in embryos developing from the flattened gastrular condition (including the higher mammals which do not possess large amounts of yolk substance) occurs as follows:
(1) Where the entoderm of the midgut terminates on either side of the notochord at the end of gastrulation, it grows mesad from either side
Fig. 235. Chick embryo of 9 to 10 pairs of somites. (Approximating Hamburger and Hamilton, ’51, stage 10; 33 to 38 hours of incubation.) (A) Surface view, unstained. (B) Stained preparation. (C) Median sagittal section. Observe the following: heart is bent slightly to the right; three primary brain vesicles are indicated; foregut touches infundibular outgrowth of prosencephalon; first indication of downward bending of the head outgrowth, i.e., the cephalic (cranial) flexure is evident. (D) Same, showing major organ-forming areas.
486
DEVELOPMENT OF PRIMITIVE BODY FORM
Fig. 236. Transverse sections through chick embryo of about 12 to 13 pairs of somites,
about 38 hours of incubation. (Approximately between stages 10 to 11 of Hamburger
and Hamilton, ’51, slightly older than that shown in fig. 235.) Observe that the optic
vesicles are constricting at their bases; heart is bent slightly to the right; anterior neuropore
is evident. (A) Optic vesicles. (B) Stomodaeal area. (C) Anterior end of developing heart. (D) Caudal extremity of forming heart. (E) Anterior intestinal portal
and forming caudal portion of the heart. (F) Well-developed somites. (G) Open
neural groove.
below the notochord to complete the roof of the midgut (figs. 201 D; 209C; 21 OF; 213). This process is similar to that which occurs in the Amphibia (cf. fig. 219D).
(2) A dorsal arching or evagination of the entoderm toward the notochordal area, comparable to that found in the frog and other Amphibia, is present also. A study of figures 213H-J; 217G; 23 4B; 237E-G; 241B-D demonstrates the marked dorsal upgrowth of all the forming body layers in the trunk area. {Note: In the elasmobranch fishes, a subnotochordah rod of cells of entodermal origin is formed similar to that in the frog and other Amphibia.)
( 3 ) The ventro-lateral walls of the midgut area, in contrast to those found in the frog, are established largely by actual ingrowth of the entoderm, mesoderm, and ectoderm with subsequent fusion in the median line
Fig. 237. Chick embryo of 17 to 19 pairs of somites. (Approximating Hamburger
and Hamilton, ’51, stage 13, 48 to 52 hours of incubation, sections indicated on outline
drawing.) Head lies partly on left side; auditory pits are deep; cervical flexure is evident
in region of rhombencephalon; cephalic flexure is marked; stomodaeum is a deep indentation touching foregut between the first pair of aortal arches; head fold of amnion
reaches back to anterior part of rhombencephalon (hindbrain). (A) Anterior (telencephalic) portion of prosencephalon, showing closed neuropore; amnion is indicated.
(B) Optic vesicles. (C) Anterior end of foregut, showing anterior extremity of stomodaeal invagination and first (mandibular) pair of aortal arches; notochord ends and
pre -chordal plate area begins at about this section. (D) Anterior end of heart (ventral
aorta); observe thin roof plate of neural tube, characteristic of the later myelencephalic
(medulla) portion of rhombencephalon or hindbrain. (E) Otic (auditory) pits and
anterior region of ventricular portion of heart. (F) Caudal limits of forming heart,
dorsal mesocardium, neural crest cells. (G) Caudal end of heart, showing converging
(vitelline) veins of the heart, sclerotome given off to notochordal area, lateral mesocardium forming. (H) Anterior trunk area, showing differentiation of somite and
typically flattened condition of ectoderm, mesoderm, and entoderm. (I) Caudal trunk
area, showing undifferentiated somite (epimeric mesoderm), intermediate mesoderm
(mesomere), and lateral plate mesoderm (hypomere). (J) Similar to (I). (K) Caudal
trunk region, showing closing neural tube. (L) Area of Hensen’s node. (M) Primitive streak.
487
488
DEVELOPMENT OF PRIMITIVE BODY FORM
in elasmobranch fishes, reptiles, birds, and mammals. This process involves the formation of lateral body folds which fold mesially toward
the median plane. (Study fig. 241 A-D.) In teleost fishes the process
is different, for in this group the entoderm and mesoderm grow outward beneath the primitive epidermis (ectoderm) and soon envelop
the yolk. Thus, the end result in teleosts is much the same as in the
frog and Necturus, It is well to observe, at this point, that a complete
retraction of the ventro-lateral walls of the midgut and body-wall
tissues surrounding the yolk or yolk-sac area, as in the frog and
Necturus (fig. 227), does not occur in the higher vertebrates, although
in the elasmobranch and teleost fishes such retraction does occur.
Fig. 238. Chick embryo of about 27 to 28 pairs of somites. (Corresponding approximately to Hamburger and Hamilton, ’51, stage 16, 51 to 56 hours of incubation.) Forebrain (prosencephalon) is divided into telencephalon and diencephalon; epiphysis is appearing on roof of diencephalon; cephalic and cervical flexures are pronounced; tail bud is short; anterior part of body is rotated to the left back to about the thirteenth pair of somites; amnion now covers anterior three fifths of body; heart shows strong ventricular loop; three pairs of aortal arches can be seen. (A) External view. (B) Transparent wholemount." (C) Sagittal section, diagrammatic.
TUBULATION OF ORGAN-FORMING AREAS
489
MESENCHYME OF
IDERMAL
(ECTODERM AL) TUBE ANTERIOR SEROSA fifl." S * L
INTftA* EMBRYONIC COELOM
NOTOCHORD parietal RECESS OF HIS)
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endocardium
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COMMON CARDINAL VE ---=^'^^-i:-‘^SlNUS VENOSUS
DORSAL ^OHTA LATERAL MESOCAROlUM O MPHALOMESENTFRIC
notochord
FUSED DORSAL AQRTAI pharyngeal (BRANCHIAL) POUCH in
Fig. 239. Sections through chick embryo of age indicated in fig. 238. Level of sections
is shown on diagram.
(See Chap. 22.) In the elasmobranch fishes, this retraction of tissues contributes little to the formation of the wall of the enteron or to that of the body. However, in teleosts such contribution is considerable.
At this point reference should be made to figures 23 8C on the chick, 242C and G on the pig, and 245 B on the early human embryo to gain a visual image of the developing foregut, midgut, and hindgut areas of the primitive metenteron. Compare with the frog (fig. 225C).
490
DEVELOPMENT OF PRIMITIVE BODY FORM
4. Tubulation (Coelom Formation) and Other Features
Involved in the Early Differentiation of the
Mesodermal Areas
The differentiation of the mesodermal areas is an all-important feature of embryonic development, for the mesoderm contributes much to the substance of the developing body. (See Chaps. 11 and 15.) While the neural, enteric, and epidermal tubes are being established, radical changes occur within the two mesodermal layers on either side of the notochord as follows:
a. Early Changes in the Mesodermal Areas
1) Epimere; Formation of the Somites. The longitudinal mass of paraxial mesoderm which lies along the side of the notochord forms the epimere (figs. 221F, G; 234E, F). The two epimeres, one on either side of the notochord, represent the future somitic mesoderm of the trunk area. In the early post-gastrula, the epimeric mesoderm, together with the notochord, lies immediately below the neural plate. However, as neuralization is effected^ the
Fig. 240. Chick embryo of about 72 to 75 hours of incubation, about stage 20 of Hamburger and Hamilton, ’51.
492
DEVELOPMENT OF PRIMITIVE BODY FORM
area of the anterior trunk and posterior hindbrain region of the embryo. In
the chick embryo (see Patterson, ’07), the most anterior segment forms first,
and later segmentation progresses in a caudal direction. This probably holds
true for most other vertebrates. However, in elasmobranch fishes, segmentation of the epimeric mesoderm also extends forward from the hindbrain
area into the head region presenting a continuous series of somites from the
eye region caudally into the tail (fig. 217D). (Study figs. 217D, 230D.) Segmentation of epimeric mesoderm appears in the head region of Amphibia.
In many higher vertebrates, three pairs of somitic condensations appear in
the area just caudal to the eye but at a slightly later period of development
than that of the elasmobranch fishes (fig. 217D-F).
2 ) Mesomere. The narrow longitudinal band of mesoderm, adjoining the lateral border of the epimere, is the mesomere (figs. 22 IF, G; 230D; 234E, F) . This mesoderm ultimately gives origin to much of the excretory (kidney) tissue and ducts and to certain of the reproductive ducts of many vertebrates. (See Chap. 18.) Because of the origin of nephric tissue from its substance, this longitudinal band of mesoderm generally is referred to as the urogenital or nephrotomic mesoderm. Synonymous terms often used are intermediate mesoderm or intermediate cell mass. The mesomere undergoes a segmentation similar to the epimeric area in its more anterior portion where the pronephric kidney develops in higher vertebrates, while in lower vertebrates, such as the shark embryo, it may be more extensively segmented.
3) Hypomere. The remainder of the mesoderm which extends lateroventrally from the mesomere forms the hypomere or hypomeric mesoderm. It also is called the lateral plate mesoderm or lateral plate mesoblast. This portion of the mesoderm does not become segmented in present-day vertebrates. (Compare with the condition in Amphioxus described on p. 505.)
b. Tabulation of the Mesodermal Areas
Coincident with the formation of the somites, a cavity begins to appear within the mesoderm. This cavity or primitive coelomic space separates the mesoderm into two layers, an outer layer near the ectoderm and an inner layer close to the neural, notochordal, and entodermal cells. This hollowing process within the mesodermal layer is known as coelom formation or tubulation of the mesoderm. In many embryos of the lower vertebrates, there is a strong tendency for the coelomic space to form throughout the entire lateral mass of mesoderm from the epimeric area ventrad into the lateral plate mesoderm. For example, in elasmobranch (shark) embryos of about 3 to 4 mm. in length and also in many early post-gastrular amphibia, the following features of the primitive coelom are found in the trunk region of each mesodermal mass:
(1) The mesoderm possesses a cavity, continuous dorso^ventrally from the epimere into the lateral plate (figs. 217G, H; 221 E). When the epimere (and to some extent the nephrotomic region as well) under
LATERAL CONSTRICTIVE MOVEMENTS
493
goes segmentation, the coelomic space within these areas becomes
segregated within the segments and, thus, is present in a discontinuous
condition.
(2) The early coelomic cavity in the shark and amphibian embryo, therefore, may be divided into three parts: (a) the myocoelic portion within the epimeric mesoderm, (b) the nephrocoel within the nephrotomic mesoderm, and (c) the splanchnocoel contained within the hypomeric or lateral plate mesoderm. While the myocoelic and nephrocoelic regions of the primitive coelom may become segmented and discontinuous, that within the splanchnocoel is continuous antero-posteriorly in the trunk region.
The coelomic cavities contained within the somites of the shark and amphibian embryo are soon lost. The coelomic cavity or nephrocoel within the nephrotome is concerned with the development of the lumen within the tubules and ducts of the excretory (urinary) system, while the splanchnocoels give origin to the coelomic cavity proper of the adult. The lateral wall of the splanchnocoel near the primitive epidermis is known as the somatopleural mesoderm, and the inner or medial wall associated with the gut tube and developing heart tissues constitutes the splanchnopleural layer. The epidermis and somatopleural mesoderm together form the somatopleure, while the entoderm and splanchnopleural mesoderm form the splanchnopleure.
In the embryos of higher vertebrates, the coelomic space of the somitic portion of the primitive coelom (i.e., the myocoels) is less pronounced and appears somewhat later in development than in the shark and amphibian embryo, but it does tend to appear. This is true also of the nephrocoel or coelomic cavity within the nephrotome. (See Chap. 18.) The coelomic condition or splanchnocoel within the hypomere forms similarly in all vertebrates. These matters will be described more in detail in Chapter 20.
C. Notochordal Area
The notochord is the elongated, median band of cells of the gastrula which lies between the two mesodermal areas. The notochord thus may be regarded as a specialized, median portion of the middle germ layer of mesodermal tissue. During gastrulation and shortly after, there may be a tendency for the notochordal material in certain forms to canalize or tubulate. Later, the notochordal material becomes converted into a definite rod of notochordal cells which represents the primitive skeletal axis of the embryo. The notochord and its relation to the early skeletal system are discussed in Chapter 15.
D. Lateral Constrictive Movements
While the neural, epidermal, and entodermal tabulations are in progress, a lateral constriction or invagination of the body wall occurs on either side in all vertebrate embryos from the fishes to the mammals. These constrictions
494
DEVELOPMENT OF PRIMITIVE BODY FORM
are effected at the level of the notochord and lower margin of the somitic
area from the anterior trunk region caudally into the tail. As a result, a
transverse section of the early vertebrate body appears pyriform or pear
shaped, with the neck of the pear directed dorsally (fig. 241 C). The constriction line is shown typically in the developing embryo of Necturus (fig.
227 ) where it extends from the lower aspect of the head outgrowth along the
lower boundary of the somitic area to the base of the tail. A line, drawn
across the body from the general area of the two lateral constrictions and
passing through the notochord, divides the embryonic body into an upper or
epaxial (epiaxial) region above the level of the notochord and a lower or
hypaxial (hypoaxial) region below the level of the notochord.
£. Tubulation of the Neural, Epidermal, Entodermal, and Mesodermal, Organ-forming Areas in Amphioxus
1. Comparison of the Problems of Tubulation in the Embryo OF Amphioxus with that of the Embryos in the Sub PHYLUM Vertebrata
a. End-bud Growth
In Amphioxus, the procedures involved in tubulation of the major organforming areas and development of primitive body form differ from those in the vertebrate group. For example, in the latter group, the basic rudiments of the head, pharyngeal, trunk, and tail regions appear to be well established at the end of gastrulation. During tubulation of the major organ-forming areas, these subregions become extended in an antero-posterior direction and the rudiments of specific structures begin to express themselves. This is especially true of the head, pharyngeal, and trunk regions. The vertebrate tail, however, arises from an end-bud tissue which progressively lays down the various parts of the tail by means of a proliferative growth in the caudal direction. On the other hand, in Amphioxus, only a small portion of the anterior end of the future body is laid down during gastrulation. Further development of the epidermal, neural, enteric, and mesodermal cellular areas together with the notochord are dependent upon cell proliferation at the caudal end of the late gastrula and later embryo. Much of the body of Amphioxus, therefore, is formed by a caudal proliferative growth of end-bud cells, somewhat comparable to the end-bud growth of the tail in the vertebrate group.
b. Position Occupied by the Notochord and Mesoderm at the End of Gastrulation
A second feature of difference in the developing embryo of Amphioxus from that of the vertebrate embryo lies in the arrangement of the notochordmesoderm complex of cells in the late gastrula. In the late gastrula of
TUBULATION OF ORGAN-FORMING AREAS IN AMPHIOXUS
495
Amphioxus, this potential, third germ layer forms a part of the entodermal
roof, although the studies of Conklin (’32) have demonstrated that notochord
and mesoderm are distinct cellular entities even in the blastula. In contrast
to this condition, the notochord and the mesoderm already are segregated as
a middle germ layer between the ectoderm and the entoderm in the late
vertebrate gastrula. The gastrula of Amphioxus, therefore, has the added
problem of segregating the notochordal and mesodermal cells from the entoderm during tubulation of the major organ-forming areas.
2. Neuralization and the Closure of the Blastopore
In the late gastrula of Amphioxus, a longitudinal middorsal plate of cells, the neural plate, elaborated by cell division and extension during gastrulation, represents the future central nervous system (fig. 247E). As the period of gastrulation comes to its end, the blastopore decreases greatly in size (fig. 247A-D). The archenteric opening also moves dorsally, coincident with a shifting of the caudal end of the archenteron in such a way that it projects in a dorso-caudal direction (figs. 189G, H; 247H). This movement of the archenteron is associated with the migration of the mass of mesodermal cells from the two lateral areas of the blastoporal lips (fig. 247A, B) to the dorsomedial portion of the blastopore (fig. 247C), where the mesoderm comes to lie on either side of the notochord below the neural plate (fig. 247C). As these changes occur, the dorsal area of the gastrula near the blastopore becomes flattened with a subsequent depression of the neural plate (fig. 247C, D). In sagittal section, the gastrula now appears oval in shape and considerably elongated in the antero-posterior direction (fig. 189G, H); in transverse view, it is triangular, especially at the caudal end (fig. 247D).
As the above changes are brought about, the ectoderm of the ventral lip of the blastopore grows dorsad, while that of the lateral lips grows mediad. In this way, the opening of the blastopore is closed by the coming together and fusion of these ectodermal (epidermal) growths (fig. 247D-F). However, the archenteron does not lose its connection, at this time, with the outside environment of the embryo for two reasons:
( 1 ) As observed above, the caudal end of the archenteron previously had shifted in such a manner that it now projects dorso-caudally; and
(2) synchronized with the epidermal growth which closes the blastoporal opening (fig. 248A), the neural plate sinks downward, becoming detached along its margin from the epidermal area (fig. 248B-D).
The downward sinking of the neural plate and its detachment from the epidermal layer begins at the dorsal lip of the blastopore and spreads anteriad. (Compare fig. 248D with 248B and C.) Consequently, as the epidermal growth along the lateral lips of the blastopore reaches the area of the sinking neural
Fig. 242. Early development of the pig embryo (B, C, and G from Patten: Embryology
of the Pig, Philadelphia, Blakiston; A is from Streeter: Carnegie Inst. Publ. No. 380;
Contrib. to Embryol. 100; D, E, and F from Heuser and Streeter: Carnegie Inst. Publ.
No. 394, Contrib. to Embryol. 109. All figures have been modified), (A) Early, neural
groove stage. Neural area is shown in black; amnion is cut away as indicated. (B)
Four-somite stage. (C) Median sagittal section, approximating the stage of development shown in (B). Observe foregut, midgut, and hindgut areas. (D) Embryo of about
six pairs of somites. (E) Embryo of about 7 to 8 pairs of somites. (F) Eighteen
pairs of somites. (G) Sagittal .sectional diagram of embryo slightly younger than (F),
showing neural and gut tubes, amnion, allantois, and forming heart.
496
TUBULATION OF ORGAN-FORMING AREAS IN AMPHIOXUS
497
plate in the region of the dorsal blastoporal lip, it continues forward along the
epidermal margins of the insinking neural plate, growing mesad and fusing in
the midline over the neural plate (fig. 247E-G). In this way, the epidermal
growth forms a covering for the neural plate. It follows, therefore, that the posterior end of the archenteron will now open into the space between the neural
plate and its epidermal covering. This new passageway between the epidermalneural plate cavity and the archenteron is the beginning of the neurenteric
canal (figs. 247H; 248A).
The flattened neural plate, canopied by the epidermal overgrowth, then begins to fold itself into the form of a tube. In doing so, its lateral edges swing gradually toward the middorsal line, as shown in figure 195. The actual grooving and tubulation of the neural plate starts at a point about midway along the embryo at the stage of development shown in figure 247F. It proceeds anteriorly and posteriorly from this point. At its extreme anterior end, the neural tube remains open to the surface as the anterior neuropore (figs. 247H; 249A-D). Eventually the caudal end of the neural plate becomes tubulated, and a definite canal is formed, connecting neural and enteric tubes. This canal is the neurenteric canal. The neurenteric canal disappears between the stage of development shown in figure 249C and that shown in figure 249D. The continued caudal growth of the neural tube is accomplished by cell proliferation from the posterior end of the tube and neurenteric canal area.
Fig. 243. Sections of pig embryo of about stage shown in fig. 242 (B) and (C). (Modified from Patten: Embryology of the Pig, 3d Ed., Philadelphia, Blakiston, ’48.) (A) Line 1, fig. 242C. (B) Line 2, fig. 242C. (C) Line 3, fig. 242C. (D) Line 4,
fig. 242C.
498
DEVELOPMENT OF PRIMITIVE BODY FORM
MAXILLARY PROCESS
ANDI BULAR
ARCH
HYOID ARCH
Fig. 244. Development of body form in the pig embryo. (A and B from Keibel: Normentafel zur Entwicklungsgeschichte des Schweines (Sus scrofa domesticus). 1897. Jena, G. Fischer. C, D, and E slightly modified from Keibel, previous reference, and from Minot: A Laboratory Text-book of Embryology. 1903. Philadelphia, P. Blakiston’s Son & Co.) (A) About 4 to 5 mm. (B) About 6 mm. (C) Ten mm. (crown-rump measurement). (D) Fifteen mm. (E) Twenty mm.
3. Epidermal Tubulation
After the neural plate sinks downward and becomes separated from the outside epidermis, the medial growth of the epidermis over the neural plate completes the middorsal area of the primitive epidermal tube (fig. 247 E-H). It then comes to enclose the entire complex of growing and elongating neural,
Fig. 245. Human embryo of ten somites. (After G. W. Corner: Contrib. to Embryol Carnegie Inst., Washington, Publ. No. 394, 112.) (A) Dorsal view. (B) Median
sagittal section of model.
500
DEVELOPMENT OF PRIMITIVE BODY FORM
Fig. 246. Development of body form in human embryo. (C from Keibel and Mall: Manual of Human Embryology, Vol. I, 1910. Philadelphia and London, Lippincott. A, B, D, and E from Keibel and Elze: Normentafel zur Entwicklungsgeschichte des Menschen. Jena, 1908. G. Fischer.) (A) Early neural fold stage. Somites are beginning to form; notochordal canal is evident. (B) About nine pairs of somites. (C) His’s embryo M. (D) About 23 pairs of somites, 4-5 mm. long. (E) About 35 pairs of trunk somites, 12 mm. long.
mesodermal, and entodermal tubes and with them it continues to grow in length principally by rapid cell proliferation at the caudal end of the embryo.
4, Tubulation of the Entodermal Area
The primitive metenteron of Amphioxus is derived from the archenteron of the late gastrula as follows.
a. Segregation of the Entoderm from the Chordamesoderm and the Formation of the Primitive Metenteric Tube
The mesoderm and notochord which occupy the roof of the archenteron of the gastrula evaginate dorsally at the anterior end of the embryo and, thus, become separated from the entoderm. (Compare fig. 195 with fig. 250A.) This separation of notochord and mesoderm by dorsal evagination from the
TUBULATION OF ORGAN-FORMING AREAS IN AMPHIOXUS
501
entoderm continues slowly in a caudal direction from the anterior end until
an embryonic condition is reached approximating about 13 to 14 pairs of
mesodermal segments. At this level, the notochord and mesoderm become
completely separated from the entoderm. As a result, the enteric or gut tube
from this point in its growth posteriad is a separate entity. (See tabulation
of mesoderm on p. 505. Anterior to the fourteenth somite, after the notochord
and mesoderm separate from the entoderm, the latter grows medially from
either side to complete the entodermal roof below the evaginated notochord
and mesoderm (fig. 250A). A primitive metenteric tube thus is formed, as
shown in figure 249C, whose only opening is that which leads by way of the
neurenteric canal (fig. 249 A, C) into the neurocoel of the neural tube and
from thence to the outside through the anterior neuropore.
NEURAL PLATE CELLS
Fig. 247. Closure of the blastopore and epidermal overgrowth of neural plate in Amphioxus (original diagrams, based on data supplied by Conklin, ’32). (A) Vegetal
pole view of early stage of gastrulation, showing general areas occupied by notochordal, entodermal, and mesodermal cells. (B) Same view of gastrula, one hour later, showing triangular form of blastopore, (C) Posterior view of late gastrula. Blastopore is now ovoid in shape and dorsally placed. Gastrula is triangular in transverse section with dorsal surface flattened. (D) Same view, later. Slight epidermal upgrowth, indicated by arrows (a and a') merges with ingrowing epidermal edges along lateral lips of blastopore (b and b') which spreads along epidermal edges of neural plate. (E) Dorsal view a brief period later than (D). Epidermal ingrowth from lateral blastoporal lips is now closing the blastoporal opening, shown in broken lines, and also is proceeding craniad along edges of sinking neural plate. (See fig. 248.) (F, G) Later stages of
epidermal overgrowth of neural plate. (H) Sagittal section of (G).
502
DEVELOPMENT OF PRIMITIVE BODY FORM
Fig. 248. Sinking of neural plate and epidermal overgrowth of neural plate in Amphioxus. (Slightly modified from Conklin, ’32.) (A) Sagittal section of embryo comparable
to that shown in fig. 247F. (B, C, D) Sections through embryo as shown by lines B,
C, D, respectively, on (A). Observe that the neural plate begins to sink downward from region of closed blastopore and proceeds forward from this point.
b. Formation of the Mouth, Anus, and Other Specialized Structures of the Metenteron
At the anterior end of the metenteron, a broad, dorsal outgrowth occurs which continues up on either side of the notochord and becomes divided into right and left dorsal diverticula (fig. 249B, H). The left diverticulum remains small and thick-walled and later fuses with an ectodermal invagination to form the pre-oral pit, described as a sense organ. The right diverticulum, however, increases greatly in size, becomes thin-walled, and gives origin to the so-called head cavity.
The mouth develops at a time when the larva acquires about 16 to 18 pairs of mesodermal segments or somites (fig. 249D). It appears when the overlying epidermis about halfway up on the left side of the body fuses with the entoderm, a fusion which occurs just posterior to the forming pre-oral pit (left diverticulum). (See black oval fig. 249D, and fig. 249F.)
At the time that the mouth forms, the entoderm opposite the first pair of somites pushes ventrally and fuses with the ectoderm. This area of fusion finally perforates and forms the first gill slit. The gill slit, once formed, moves up on the right side of the body (fig. 249E). The entodermal area from which the first and later gill slits make their appearance is known as the branchial rudiment (fig. 249D).
At the caudal end of the larva, following the degeneration of the neurenteric canal, a small area of entoderm fuses with the ectoderm and forms the anal opening. The anus is first ventral in position, but later moves up to the left side as the caudal fin develops (fig. 249E, G).
TUBULATION OF ORGAN*FORMING AREAS IN AMPHIOXUS
503
5. Tubulation of the Mesoderm
Tubulation of the mesoderm and the formation of a continuous anteroposterior coelom in Amphioxus differs considerably from that found in the subphylum Vertebrata. This fact becomes evident in tracing the history of the mesoderm from the time of its segregation from the entoderm of the late
Fig. 249. Various stages of development of Amphioxus. (A from Kellicott, ’13, and Conklin, ’32; B from Kellicott, ’13, slightly modified; C-I, slightly modified from Conklin, ’32.) (A) Six -somite stage, comparable to fig. 247G and H. The animal hatches about
the time that two pairs of somites are present. (B) Nine-somite stage. The larva at this stage swims by means of cilia which clothe the entire ectodermal surface. (C) About fourteen pairs of somites are present at this stage. Neurenteric canal is still patent. (D) About 16 to 18 pairs of somites. Neurenteric canal is degenerating; mouth is formed. (E) About 20 to 22 pairs of somites. Anal opening is established between this stage and that shown in (D). (F) Transverse section, showing oral opening, looking from anterior
end of animal. (G) Same through anal area. (H) Frontal section of a 24-hour larva near dorsal side showing notochord, somites (S-1, S-8, etc.) and undifferentiated tissue at caudal end. Neural tube shown at anterior end. Nine pairs of somites are present. (I) Frontal section of a 38-hour larva at the level of the notochord showing section through the neural tube at the anterior and posterior ends, i.e., in region where larva bends ventralwards. Thirteen pairs of somites are present with muscle fibrillae along the mesial borders of the somites.
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DEVELOPMENT OF PRIMITIVE BODY FORM
gastrula and later embryo to the stage where a continuous antero-posterior
coelomic space is formed, comparable to that found in the vertebrates.
The mesoderm of the late gastrula of Amphioxus is present as a dorsomedian band of cells on either side of the notochord, and together with the notochord, occupies the dorsal area or roof of the archenteron as mentioned previously. In the region of the blastopore, the two mesodermal bands diverge ventrally and occupy the inner aspect of the lateral walls of the blastopore (fig. 190F, G; 247B). At about the time of blastoporal closure, the two mesodermal masses of cells, located along the lateral lips of the blastopore, are retracted dorsally, where they come to lie on either side of the notochord (fig. 247C). In this position the two bands of mesoderm and the notochord continue to form the dorsal region or roof of the archenteron until approximately the time when the embryo is composed of 13 to 14 pairs of mesodermal segments or somites (fig. 249C). (See Hatschek, 1893, pp. 131, 132; Willey, 1894, p. 115; Conklin, ’32, p. 106.) When the embryo reaches a stage of development wherein 15 to 16 pairs of somites are present, the notochord and mesoderm have separated entirely from the entoderm (fig. 249D). At about this period the neurenteric canal between the metenteron and the neural tube disappears (fig. 249C, D).
ENTEROCOEL
DORSAL FIN-RAY CAVITY
SPLANCMNOCOEL SPLANCHNOCOELS ^FUSE
I'’
HORIZONTAL SEPTUM
Fig. 250. Differentiation of somites in Amphioxus. (A and B from Conklin, ’32; C,
E, and F after Hatschek, 1888 and 1893; D from MacBride, 1898; all figures are modified.) (A) Somites shortly after separation from entoderm. (B) Later stage, the
somites grow ventrally. (C) Semitic wall begins to differentiate into a thickened, dorsal,
myotomic area, located near notochord and neural tube, and thinner somatic and visceral
areas. (D) Horizontal septum formed which separates dorso-myotomic portion of somite
from splanchnocoelic area below. (E, F) Later stages in differentiation of myotome and
myocoelic diverticulum. (See text.)
TUBULATION OF ORGAN-FORMING AREAS IN AMPHIOXUS
505
The formation of a continuous, antero-posterior, coelomic cavity in Amphioxus may be described as follows. The mesodermal bands on either side
of the notochord of the post-gastrular embryo become converted into mesodermal grooves as each mesodermal band folds inwards or evaginates into
the residual blastocoelic space between the archenteron and the outside ectoderm (fig. 195). Beginning at the anterior end, these longitudinal grooves
of mesoderm soon become divided into distinct segments or somites by the
appearance of transverse divisions (fig. 249 A, B, H). The first and second
pairs of somites are formed at the anterior ends of the mesodermal grooves
at about the time that the embryo hatches and swims about by means of
ciliary action.
Eventually each somite becomes entirely constricted from the notochord and entoderm. In this segregated condition the somite forms a rounded structure retaining within itself a portion of the original archenteric cavity (fig. 250A). Hence, the cavity within the somite is called an enterocoel and represents the beginnings of the coelomic cavity of later development, at least in the anterior 13 or 14 pairs of somites. (Note: It is to be observed in this connection that the primitive somite in Amphioxus is not comparable to the primitive somite of the vertebrate embryo. In the latter, the somite represents merely a segment of the epimeric mesoderm, whereas in Amphioxus it is the entire mesoderm in each half of a particular segment of the embryo.)
After hatching, the mesodermal bands continue to form into grooves as the embryo elongates, and, synchronously, successive pairs of somites are formed. At about the time 8 to 10 pairs of somites are present (fig. 249B, H), the enterocoels of the first two pairs of somites have become entirely separated from the archenteron. The enterocoels of the following six pairs of somites are small and are not as evident at first as those of the first two pairs. Ultimately a definite enterocoel is found, however, in each somite.
Posterior to the eighth or ninth pairs of somites, the forming mesodermal grooves do not show the enterocoelic pouches as plainly as the more anterior somites. Slit-like mesodermal grooves tend to be present, however, and, when the somite is entirely free from the archenteron, this slit-like cavity expands into the enterocoelic space of the somite. As the region of the fourteenth pair of somites is approached, the slit-like mesodermal groove becomes more and more indefinite. Posterior to the fourteenth or fifteenth pair of somites, the somites originate from a solid mesodermal band on either side of the notochord. An enterocoelic origin of the cavity within each somite, therefore, is not possible caudal to this area, and the coelomic space arises by a hollowing-out process similar to coelomic cavity formation in the vertebrate group.
At about the time when eight pairs of somites are established, a shift of
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DEVELOPMENT OF PRIMITIVE BODY FORM
the mesoderm on either side of the embryo produces a condition wherein the
somites of either side may be slightly intersegmental in relation to the somites
on the other side (fig. 249H).
During its later development, each somite grows ventrally (fig. 250B). That portion of the somite contiguous to the notochord and neural tube thickens and forms the myotome. The region of the somite near the epidermal ectoderm is called the somatic or parietal mesoderm, while that associated with the entoderm forms the visceral or splanchnic mesoderm (fig. 25 OC).
As the myotome enlarges, the coelomic space becomes more and more displaced ventrally, and most of it comes to lie on either side of the enteron (metenteron). (See fig. 250D.) This ventral coelomic space forms the splanchnocoel, while the dorsal space, lateral to the myotome, is known as the myocoel. Eventually, the splanchnocoels of each pair of somites push ventrally to the lower portion of the enteron, where they ultimately fuse (fig. 250D-F). Gradually the splanchnocoels of each segment fuse anteroposteriorly and in this way a continuous, antero-posterior, splanchnocoelic space below and around the gut tube is formed. Tubulation or the formation of a continuous, antero-posterior, coelomic cavity thus is effected by fusion of the splanchnocoels of the respective somites on either side (fig. 25 OF). A horizontal septum, the intercoelomic membrane also appears, separating the myocoels above from the splanchnocoelic cavity below (fig. 250D).
6. Later Differentiation of the Myotomic (Dorsal) Area OF the Somite
While the above events are taking place in the ventral portion of the somite, the upper, myotomic region undergoes profound modification.
As shown in figure 250D, the myotomic portion of the somite has two unequally developed areas;
( 1 ) a medial muscular portion, the myotome and
(2) the laterally placed, thin-walled, parietal part which surrounds the coelomic space, or myocoel.
The muscular portion enlarges rapidly and, as seen in figure 25 OE and F, forms the muscle plate or myotome of the adult. These muscle plates very early assume the typical > shape characteristic of the adult. On the other hand, the myocoelic portion contributes important connective or skeletal tissue to the framework of the body. In each segment, the wall of the myocoel gives origin to three diverticula as follows:
(a) a lower sclerotomic diverticulum,
(b) a ventral diverticulum, and
(c) a dorsal sclerotomic diverticulum.
TUBULATION OF ORGAN-FORMING AREAS IN AMPHIOXUS
507
The lower sclerotomic diverticulum (fig. 250D, E) extends up between the
myotome and the medially placed notochord and nerve cord, as diagrammed
in figure 250F. Its walls differentiate into two parts:
( 1 ) an inner layer which, together with a similar contribution from the somite on the opposite side, wraps around the notochord and nerve cord and, subsequently, gives origin to a skeletogenous sheath of connective tissue which enswathes these structures; and
(2) an outer layer which covers the mesial (inner) aspect of the myotome with a fascia or connective tissue covering.
The outer surface of the myotome does not have a covering of fascia.
The ventral diverticulum extends between the lateral wall of the splanchnococl and the epidermal layer of the body wall (fig. 250E, F) and separates the parietal wall of the splanchnocoel from the epidermal wall (fig. 250F). This ventral diverticulum or dermatomic fold, together with the external or parietal wall of the myocoel above, forms the dermatome. The inner and outer layers of the ventral diverticulum gradually fuse to form the cutis or dermal layer of the integument or skin in the ventro-lateral portion of the body, whereas the parietal wall of the myocoel above gives origin to the same dermal layer in the body region lateral to the myotome. The dorsal sclerotomic diverticula form the fin-ray cavities in the dorsal fin. These cavities become entirely isolated from the rest of the myocoelic spaces. Several fin-ray cavities occupy the breadth of a single myotome. The dorsal myotomic portion of the somite thus differentiates into three main structural parts:
(a) the muscular myotome,
(b) the mesial sclerotome or skeletogenous tissue, and
(c) the latero- ventral dermatome or dermal tissue of the skin.
7. Notochord
The notochord arises as a middorsal evagination of the primitive archenteron up to about the stage of about 13 to 14 pairs of somites (fig. 195). Posterior to this region it takes its origin by proliferative growth from a separate mass of notochordal tissue, lying above the gut and between the two mesodermal masses of cells. Its origin posterior to the general area of the thirteenth to fourteenth body segments, therefore, has no relation to the entoderm. It rapidly develops into a conspicuous skeletal rod, lying below the neural tube and between the mesodermal somites and resting in a slight depression along the dorsal aspect of the metenteron or entodermal tubulation (fig. 249E, H). It continues forward in the head region, anterior to the brain portion of the neural tube (fig. 249E).
(The student is referred to the following references for further details relative to the early development of Amphioxus: Cerfontaine, ’06; Conklin, ’32;
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DEVELOPMENT OF PRIMITIVE BODY FORM
Hatschek, 1893; Kellicott, ’13; MacBride, 1898, ’00, ’10; Morgan and Hazen,
’00; and Willey, 1894.)
F. Early Development of the Rudiments of Vertebrate Paired Appendages
Two pairs of appendages, placed at the anterior (pectoral) and posterior (pelvic) extremities of the trunk, are common to all vertebrate groups. However, all vertebrates do not possess two pairs of paired appendages. Certain lizards of the genera Pygopus and Pseudopus have only a posterior pair of appendages, while in certain other vertebrates the opposite condition is found, the anterior pair being present without posterior appendages. The latter condition is found in certain teleost and ganoid fishes; the amphibian. Siren lacertina; the lizard, Chirotes; and among the mammals, the Sirenia and Cetacea. Again, some vertebrates are entirely apodal, e.g., cyclostomatous fishes and most snakes, although the boa constrictors and pythons possess a pair of rudimentary posterior appendages embedded in the skin and body wall. Some have rudimentary appendages only in the embryo, as the legless amphibians of the order Gymnophiona, and certain lizards. Consequently, the presence of embryonic rudiments of the paired appendages is a variable feature when the entire group of vertebrates is considered.
The rudiments of the paired appendages also are variable, relative to the time of their appearance in the vertebrate group as a whole. They are more constant in the Amniota, i.e., reptiles, birds, and mammals, in time of appearance than in the Anarnniota, i.e., fishes and amphibia. In the reptiles, birds, and mammals, the limb buds arise when primitive body form is being evolved. In the anuran amphibia, the anterior rudiments may appear and go on to a high degree of differentiation before the appearance of the posterior pair of appendages. For example, in the frog, Rana pipiens, the posterior limb buds first make their appearance a brief period before the beginning of metamorphosis of the tadpole into the adult form. However, the anterior limb buds differentiate earlier but remain concealed beneath the operculum until they become visible during the later stages of metamorphosis. In urodele amphibia, the fore limb bud is not covered by an operculum, and it is visible at the time of its initial appearance which occurs before the hind limb rudiment arises (fig. 227J-L).
In the majority of vertebrates, the limb rudiment first makes its appearance as an elongated, dorso-ventrally flattened fold of the epidermis, containing a mass of mesodermal cells within, as shown, for example, in the chick and mammalian embryos (figs. 240, 244, 246). The contained mesodermal cells may be in the form of epithelial muscle buds derived directly from the myotomes (e.g., sharks) or as a mass of mesenchyme (chick, pig, human). (See Chap. 16.) The early limb-bud fold may be greatly exaggerated in certain elasmobranch fishes, as in the rays, where the anterior and posterior fin folds
LIMB BUD AN ILLUSTRATION OF FIELD CONCEPT OF DEVELOPMENT
509
fuse together for a time, forming one continuous lateral body fold. On the
other hand, in the lungfishes (the Dipnoi) and in amphibia (the Anwa and
Urodela), the appendage makes its first appearance, not as an elongated fold
of the lateral body wall, flattened dorso-ventrally, but as a rounded, knob-like
projection of the lateral body surface (fig. 227K-M).
G. The Limb Bud as an Illustration of the Field Concept of Development in Relation to the Gastrula and the Tubulated Embryo
In Chapter 9 it was observed that the major presumptive organ-forming areas are subdivided into many local, organ-forming areas at the end of gastrulation. In the neural and epidermal areas, this subdivision occurs during gastrulation through influences associated with local inductive action. At the end of the gastrular period, therefore, each local area within the major organforming area possesses the tendency to give origin to a specific organ or a part of an organ. The restricted, localized areas within each major organforming area represent the individual, or specific, organ-forming fields. During tubulation, the major organ-forming areas with their individuated, organ-forming fields are molded into tubes, and, thus, the individual fields become arranged along each tube. Consequently, each tube possesses a series of individual, organ-forming areas or fields, distributed antero-posteriorly along the tube.
As a result of the close association of cells and substances during gastrulation and tubulation, many specific organ-forming fields are related to more than one of the body tubes. Specific organ-forming fields, therefore, may have intertubular relationships. For example, the lens field is located in the epidermal tube, but, in many species, its origin as a lens field is dependent upon influences emanating from the optic vesicle of the neural tube (see Chap. 19). Another example of an association between the parts of two contiguous tubes is the limb-bud field in the urodele, Amby stoma punctatum. As the limb-bud field in this species illustrates various aspects and properties of an organ-forming field, it will be described below in some detail.
The presumptive anterior limb disc or limb field of Amby stoma is determined as a specific limb-forming area in the middle gastrular stage (Detwiler, ’29, ’33). Later on in the embryo, it occupies a circular-shaped area within trunk segments three to six. According to Harrison (’18) and Swett (’23), its properties as a field mainly are resident in the cells of the somatic layer of the mesoderm in this area. If, for example, the somatic layer of mesoderm in this area is transplanted to another area, a well-developed limb will result. Also, the mesoderm of the dorsal half of the field forms a greater part of the limb than the other parts, with the anterior half of the limb disc next in importance. It appears, therefore, that the limb-forming potencies are greatest in the dorso-anterior half of the limb field and become less postero-ventrally. Moreover, not “all of the cells which are potentially limb forming go into
510
DEVELOPMENT OF PRIMITIVE BODY FORM
the limb†(Swett, ’23). As demonstrated by Harrison (’18) half discs (half
fields), left intact in the developing embryo or removed and transplanted to
other areas, develop into normal limbs.
The above experiments of Harrison, together with those of Detwiler (’29, ’33) suggest that while the limb field is irreversibly determined at an early stage to form limb tissue, the exact determination of the various parts within the field is absent at the earlier phases of development. One kind of precise determination is present, however, for the first digit-radial aspect (i.e., the pre-axial aspect) of the limb appears to arise only from the anterior end of the field, whether the field is allowed to develop intact or is split into two parts. That is, if it is split into two portions, the anterior extremity of the posterior portion, as well as the original anterior part of the limb field, develops the pre-axial aspect of the limb. This antero-posterior polarization is present from the first period of field determination. On the other hand, the dorso-ventral polarity is not so determined; for if the transplanted limb disc is rotated 180 degrees (i.e., if it is removed and reimplanted in its normal place dorsal side down) it will develop a limb with the dorsal side up but with the antero-posterior axis reversed (Harrison, ’21). In these cases the first digit-radial aspect will appear ventral in position. This result indicates that the pre-axial aspect of the limb becomes oriented always toward the ventral aspect of the limb. However, the experiments of Swett (’37, ’39, ’41) tend to show that the reversal of the dorso-ventral axis occurs only when implanted below the myotome s; for when the rotated limb field is implanted in the somitic (myotomic) area, it will remain inverted. Factors other than those resident within the limb field itself, probably factors in the flank area, appear thus to induce the normal dorso-ventral axis when the limb disc is implanted in its normal site.
In the descriptions given above, the importance of the somatic layer of mesoderm as the seat of the limb-forming factors is emphasized. It is obvious, however, that the epidermal covering of the limbs derived from the epidermal tubulation also is important in limb formation. For example, epidermal importance is suggested by the experiments of Saunders (’49) on the developing limb bud of the chick wherein it was found that the apical ridge of ectoderm, located at the apex of the early limb bud, is essential for normal limb development.
Individual, or specific, organ-forming fields which appear in the gastrula and early tubulated embryo thus are generalized areas determined to form individual organs. As development proceeds, two main limitations are imposed upon the field:
( 1 ) The cellular contribution of the field actually entering into the organ becomes restricted; and
(2) specific parts of the field become progressively determined to form specific parts of the organ. •
CEPHALIC FLEXION AND GENERAL BODY BENDING
511
It is obvious, therefore, that the fields of influence which govern the development of specific organs may be much more extensive in cellular area
than the actual cellular contributions which take part in the formation of
the specific organ structures. Experiments on the forming limb of Amby stoma
also have demonstrated that a particular area of the field is stronger in its
limb-forming potencies than other regions of the field. This property probably
is true of other fields as well.
(For a detailed discussion of the field concept in embryonic development, reference should be made to Huxley and DeBeer, ’34, Chaps. 8 and 9; Weiss, ’39, p. 289 ff.)
H. Cephalic Flexion and General Body Bending and Rotation in Vertebrate Embryos
The anterior end of the neural tubulation is prone to assume a bent or flexed contour whereby the anterior end of the neural tube is directed downward toward the ventral aspect of the embryo. This general behavior pattern is strong in vertebrate embryos with the exception of the teleost fishes. In teleost fishes this bending habit is slight. As the later development of the head progresses in other vertebrate embryos, the neural tube shows a pronounced cephalic (cranial) flexure in the region of the midbrain, in some species more than in others. (See Chap. 19.) An additional bending occurs in the posterior hindbrain area. The latter flexure is the cervical or nuchal flexure (figs. 231, 238, 240, 244, 246).
Aside from the acute bending which takes place in the formation of the cephalic and the nuchal flexures, there is a definite tendency for many vertebrate embryos to undergo a general body bending, with the result that the anterior part of the body and the caudal portion of the trunk and tail may be depressed in a ventral direction (figs. 222C-E; 227; 229F; 238; 240; 244; 246). In the frog embryo, at hatching, the opposite tendency may prevail for a brief period, and the dorsal trunk region may appear sagging or hollowed (fig. 226A, C).
In addition to these bending movements, in the embryos of higher vertebrates, a rotation or twisting (torsion) of the developing body along the antero-posterior axis is evident. In the chick embryo, for example, the head region begins to rotate toward the right at about 38 hours of incubation. Gradually this torsion continues caudally (figs. 237, 238, 239, 260). At about 70 to 75 hours, the rotational movement reaches the tail region, and the embryo then comes to lie on its left side throughout its length (fig. 240). In exceptional embryos, the rotational movement is toward the left, and the embryo comes to lie on its right side. Similar movements occur in the pig and other mammals.
This rotational movement is advantageous, particularly in long-bodied Amniota, such as the snakes, where it permits the developing embryo to coil
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DEVELOPMENT OF PRIMITIVE BODY FORM
in spiral form within the extra-embryonic membranes. The coiling tendency,
however, is not alone confined to the snake group, for the habits of general
body bending, referred to above, essentially is a coiling tendency. Viewed
thus, the rotation or torsion of the developing body along its median axis is
a generalized behavior pattern which permits and aids the coiling habit so
prevalent among the embryos of higher vertebrates. It may be observed further
that the coiling behavior is a common attitude during rest not only among
snakes but also among the adults of many higher vertebrates.
I. Influences Which Play a Part in Tubulation and Organization of
Body Form
In Chapter 9, it was pointed out that the pre-chordal plate material, that is, organizer material which invaginates first during gastrulation and which comes to lie in the future head region, induces the organization of certain head structures and itself may form a part of the pharyngeal wall and give origin to head mesoderm, etc. On the other hand, the trunk-organizer material (notochord and somitic mesoderm) which moves to the inside, following the pre-chordal plate material, organizes the trunk region. The following series of experiments based upon work by Spemann, ’31, sets forth the inductive properties of these two cellular areas:
Experiment
1. Head-organizer material, taken from one embryo and placed at head level of a
host embryo, will induce a secondary head, having eyes and ear vesicles
2. Head-organizer material, transplanted to trunk and tail levels in host embryos, induces a complete secondary embryo, including head
3. Trunk-organizer material (i.e., notochord and somitic mesoderm), placed at head level in host embryo, induces a complete secondary embryo, including the head structures
4. Trunk-organizer material, placed at future trunk or tail levels in host embryos, induces trunk and tail structures only
The many influences which play a part in the organization of the vertebrate
head and body constitute an involved and an unsolved problem. The extreme
difficulty of this general problem has long been recognized. (See Kingsbury
and Adelmann, ’24.) The above-mentioned work of Spemann represents a
beginning attempt to analyze this aspect of development and to understand
the factors involved. It demonstrates that the organization of the neural tube
and other axial areas is dependent upon specific cellular areas which migrate
inward during gastrulation. However, this is but one aspect of the problem.
As observed in the series of experiments above, trunk-organizer material
is able to organize a complete secondary embryo, including the head, when
TUBULATION AND ORGANIZATION OF BODY FORM
513
Fig. 251. Dependency of neural tube formation upon surrounding tissues. (A) Effect
of notochord without myotomes. (B) Effect of myotomes without notochord. (C)
Absence of notochord and myotomes.
placed at head level in the host but can only organize trunk and tail structures when placed in trunk and tail areas of the host. In other words, there exists a mutual relationship between the level of the host tissues and the transplanted organizer material of the trunk organizer in effecting tlie formation of a head at the head level.
Another forceful example of the interrelationship of developing parts and formative expression of body structures is shown by the work of Holtfreter (’33) on the development of the neural tube. This work demonstrates that the form of the neural tube is dependent upon influences in its environment, as shown in figure 251. The presence of the later developing notochord determines a thin ventral floor of the neural canal, whereas the contiguous myotome determines a thick wall of the neural tube. Normally, in development, the notochord lies below the neural tube, while the somites with their myotomie parts come to lie lateral to the tube. That is to say, the normal bilateral symmetry of the neural tube is dependent upon the relationship, in their normal positions, of the notochord and the myotomes.
The behavior of the developing neural tube, relative to the notochord and the myotomes, demonstrates the importance of the’ migration of the somitic mesoderm from a position contiguous and lateral to the notochord at the beginning of neuralization to one which is lateral to the forming neural tube as neuralization and differentiation of the neural tube progresses.
A further illustration of the probable influence of the notochordal area in morphogenesis and organization of body form is the behavior of the developing metenteron or enteric tube. As observed previously, the gut tubulation tends to invaginate or arch upward toward the notochord not only in embryos developing from flattened gastrulae but also in amphibia. The movement of the entoderm toward the notochord strikingly resembles the behavior of the neural plate ectoderm during the formation of the neural tube. This comparison becomes more striking when one considers the manner of enteron for
514
DEVELOPMENT OF PRIMITIVE BODY FORM
mation in the tail and hindgut regions in the shark embryo, Squalus acanthias,
already mentioned, p. 484. In this species the entoderm of the developing tail
actually invaginates dorsad and closes in a manner similar to the forming
neural tube. That is to say, in the developing tail of the shark, two invaginations toward the notochord are evident, one from the dorsal side, which involves the formation of the neural tube, and the other from the ventral side,
effecting the developing enteric tube.
The above facts suggest, therefore, that one of the main organizing influences at work during tubulation and primitive body formation emanates from the pre-chordal plate area, the notochord, and the epimeric portion of the mesoderm. From this general area or center, a chain of acting and interacting influences extends outward, one part acting upon another, to effect the formative expression of the various parts of the developing body.
J. Basic Similarity of Body-form Development in the Vertebrate Group of Chordate Animals
In the earlier portion of this chapter, differences in the general procedures concerned with tubulation and primitive body formation in round and flattened gastrulae were emphasized. However, basically all vertebrate embryos show the same tendency of the developing body to project itself upward and forward in the head region, dorsally in the trunk area and dorso-posteriad in the tail region. Literally, the embryonic body tends to lift itself up out of, and above, the area which contains the yolk and extra-embryonic tissues. This proneness to move upward and to protrude its developing head end forward and its caudal end backward is shown beautifully in the development of the embryos of the shark (figs. 229, 230), the mud puppy (fig. 227), the chick (fig. 235C), and the pig (fig. 242). The embryo struggles to be free from its bed of yolk and extra-embryonic tissue, as it were, and it reminds one of the superb imagery employed by the poet, John Milton, in his immortal poem, Paradise Lost, where he describes the development of the lion thus:
The grassy clods now calv’d; now half appear’d
The tawny lion, pawing to get free
His hinder parts, then springs as broke from bonds,
And rampant shakes his brinded mane.
In summary, therefore, although it appears that rounded and flattened gastrulae in the vertebrate group may have slightly different substrative conditions from which to start, they ail employ essentially similar processes in effecting tubulation of the respective, major organ-forming areas and in the development of primitive body form.
Bibliography
Cerfontaine, P. 1906. Recherches sur le
developpement de I’ Amphioxus. Arch,
biol., Paris. 22:229.
Conklin, E. G. 1932. The embryology of Amphioxus. J. Morphol. 54:69.
Dean, B. 1896. The early development of Amia. Quart. J. Micr. Sc. (New Series) 38:413.
Detwiler, S. R. 1929. Transplantation of anterior limb mesoderm from Amhlystonia embryos in the slit blastopore stage. J. Exper. Zool. 52:315.
. 1933. On the time of determination of the antero-posterior axis of the forelimb in Amhly stoma. J. Exper. Zool. 64:405.
Hamburger, V. and Hamilton, H. L. 1951. A series of normal stages in the development of the chick embryo. J. Morphol. 88:49.
Harrison, R. G. 1918. Experiments on the development of the forelimb of Ainblystorna, a self-differentiating equipotential system. J. Exper. Zool. 25:413.
. 1921. On relations of symmetry
in transplanted limbs. J. Exper. Zool. 32:1.
Hatschek, B. 1888. Uber den Schechtenbau von Amphioxus. Anat. Anz. 3:662.
Hatschek, B. 1893. The Amphioxus and its development. Translated by J. Tuckey. The Macmillan Co., New York.
Holtfreter, J. 1933. Der Einfluss von Wirtsalter und verschiedenen Organbezirken auf die Differenzierung von angelagertem Gastrulaektoderm. Arch. f. EntwickIngsmech. d. Organ. 127:619.
Huxley, J. S. and De Beer, G. R. 1934. The Elements of Experimental Embryology. Cambridge University Press, London.
Kcllicott, W. E. 1913. Outlines of Chordate Development. Henry Holt & Co., New York.
Kingsbury, B. F. and Adelmann, H. B. 1924. The morphological plan of the head. Quart. J. Micr. Sc. 68:239.
MacBride, E. W. 1898. The early development of Amphioxus. Quart. J. Micr. Sc. 40:589.
. 1900. Further remarks on the development of Amphioxus. Quart. J. Micr.
Sc. 43:351.
. 1910. The formation of the layers
in Amphioxus and its bearing on the interpretation of the early ontogenetic processes in other vertebrates. Quart. J. Micr. Sc. 54:279.
Morgan, T. H. and Hazen, A. P. 1900. The gastrulation of Amphioxus. J. Morphol. 16:569.
Needham, J. 1942. Biochemistry and Morphogenesis. Cambridge University Press, London.
Patterson, J. T. 1907. The order of appearance of the anterior somites in the chick. Biol. Bull. 13:121.
Saunders, J. W. 1949. An analysis of the role of the apical ridge of ectoderm in the development of the limb bud in the chick. Anat. Rec. 105:567.
Selys-Longchamps, M. de. 1910. Gastrulation et L)rmation des feuillets chez Petromyzon planeri. Arch, biol., Paris. 25:1.
Spemann, H. 1931. Uber den Anteil von Implantat und Wirtskeim an der Orienticrung und Beschaffenheit der induzierten Embryonalanlage. Arch. f. EntwickIngsmech. d. Organ. 123:389.
Swett, F. H. 1923. The prospective significance of the cells contained in the four quadrants of the primitive limb disc of Amhly stoma. J. Exper. Zool. 37:207.
. 1937. Experiments upon delayed
determination of the dorsoventral limb axis in Amhly stoma punctatum (Linn.). J. Exper. Zool. 75:143.
. 1939. Further experiments upon
the establishment and the reversal of prospective dorsoventral limb-axis polarity. J. Exper. Zool. 82:305.
. 1941. Establishment of definitive
polarity in the dorsoventral axis of the forelimb girdle in Amhly stoma punctatum (Linn.). J. Exper. Zool. 86:69.
Weiss, P. 1939. Principles of Development. Henry Holt & Co., New York.
Willey, A. 1894. Amphioxus and the Ancestry of the Vertebrates. The Macmillan Co., New York.
515
11
Basic Features of VerteLrate Morplio^enesis
A. Introduction
1. Purpose of this chapter
2. Definitions
a. Morphogenesis and related terms
b. Primitive, larval, and definitive body forms
1 ) Primitive body form
2) Larval body form
3) Definitive body form
3. Basic or fundamental tissues
B. Transformation of the primitive body tubes into the fundamental or basic condition of the various organ systems present in the primitive embryonic body
1. Processes involved in basic system formation
2. Fundamental similarity of early organ systems
C. Laws of von Baer
D. Contributions of the mesoderm to primitive body formation and later development
1. Types of mesodermal cells
2. Origin of the mesoderm of the head region
a. Head mesoderm derived from the anterior region of the trunk
b. Head mesoderm derived from the pre-chordal plate
c. Head mesoderm contributed by neural crest material
d. Head mesoderm originating from post-otic somites
3. Origin of the mesoderm of the tail
4. Contributions of the trunk mesoderm to the developing body
a. Early differentiation of the somites or epimere
b. Early differentiation of the mesomere (nephrotome)
c. Early differentiation and derivatives of the hypomere
1) Contributions of the hypomere (lateral plate mesoderm) to the developing pharyngeal area of the gut tube
2) Contributions of the hypomere (lateral plate mesoderm) to the formation of the gut tube and heart structures
3) Contributions of the hypomere (lateral plate mesoderm) to the external (ectodermal or epidermal) body tube
4) Contributions of the hypomere or lateral plate mesoderm to the dorsal body areas
5) Contributions of the lateral plate mesoderm to the walls of the coelomic cavity
5. Embryonic mesenchyme and its derivatives
516
INTRODUCTION
517
E. Summary of later derivatives of presumptive, major, organ-forming areas of the late
blastula and gastrula
1. Neural plate area (ectoderm)
2. Epidermal area (ectoderm)
3. Entodermal area
4. Notochordal area
5. Mesodermal areas
6. Germ-cell area
F. Metamerism
1. Fundamental metameric character of the trunk and tail regions of the vertebrate body
2. Metamerism and the basic morphology of the vertebrate head
G. Basic homology of the vertebrate organ systems
1. Definition
2. Basic homology of vertebrate blastulae, gastrulae, and tubulated embryos
Basic Features of Vertebrate Morphogenesis
A. Introduction
1. Purpose of This Chapter
In this chapter, the basic morphogenetic features which give origin to the later organ systems are emphasized. These features arise from the stream of morphogenetic phenomena which come down from the fertilized egg through the periods of cleavage, blastulation, gastrulation, and tabulation. This chapter thus serves to connect the developmental processes, outlined in Chapters 6 to 10, with those which follow in Chapters 12 to 21. As such, it emphasizes certain definitions and basic structural features involved in the later morphogenetic activities which mold the adult body form.
2. Definitions
a. Morphogenesis and Related Terms
The word morphogenesis means the development of form or shape. It involves the elaboration of structural relationships. The morphogenesis of a particular shape and structure of a cell is called cytomorphosis or cytogenesis and is synonymous with the term cellular differentiation, considered from the structural aspect. In the Metazoa, the body is composed of groups of cells, each cellular group possessing cells of similar form and function. That is, each cell group is similarly differentiated and specialized. A cellular group, composed of cells similar in form (structure) and function, is called a tissue. Histology is the study of tissues, and the word histogenesis relates to that phase of developmental morphology which deals with the genesis or development of tissues. An organ is an anatomical structure, produced by an association of different tissues which fulfills one or several specialized functions. For example, the esophagus, stomach, liver, etc., are organs of the body. During development, each of the major organ-forming areas, delineated in
518
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
Chapters 6, 7, 9 and 10, produce several specific organs. Organogenesis is
concerned with the formation of these specific organs. A group of organs
which are associated together to execute one general function form an organ
system. The digestive system, for example, has for its general function that
of obtaining nourishment for the body. It is composed of a series of o’-gans
integrated toward this end. The nervous system, similarly, is an assemblage
of specific organs devoted to the discharge of nervous functions. So it is with
the other systems of the organism. System development is concerned with
the genesis of such systems. The association of various systems, integrated
together for the maintenance of the body within a particular habitat, constitutes the organism. Finally, the organism acquires a particular body form
because of the form, structure, and activities assumed by its organ systems
as a result of their adaptation to the functional necessities of the particular
habitat in which the organism lives. It should be urged further that this nice
relationship between form and structure, on the one hand, and functional
requirements, on the other, is a fundamental principle of development from
the egg to the adult. It is a principle intimately associated with the morphogenesis of the organ systems described in Chapters 12 to 21.
During development from the egg to the adult form, three major types of body form are evolved in the majority of vertebrate species.
b. Primitive, Larval, and Definitive Body Forms (see fig. 255)
1) Primitive Body Form. The condition of primitive or generalized, embryonic body form is attained when the embryo reaches a state in which its developing organ systems resemble the respective developing organ systems in other vertebrate embryos at the same general period of development. (See p. 520.) Superficially, therefore, the general structure of the primitive embryonic body of one species resembles that of the primitive embryonic bodies of other vertebrate species. Such comparable conditions of primitive, body-form development are reached in the 10 to 15-mm. embryo of the shark, Squalus acanthias, of the frog embryo at about 5 to 7 mm., the chick at about 55 to 96 hrs. of incubation, the pig at 6 to 10 mm., and the human at 6 to 10 mm.
2) Larval Body Form. Following primitive body form, the embryo gradually transforms into a larval form. The larval form is present in the period between primitive body form and definitive body form. The larval period is that period during which the basic conditions of the various organ systems, present in primitive body form, undergo a metamorphosis in assuming the form and structure of the adult or definitive body form. In other words, during the larval period, the basic or generalized conditions of the various organ systems are changed into the adult form of the systems, and the larval period thus represents a period of transition. Embryos which develop in the water (most fishes, amphibia) tend to accentuate the larval condition, whereas those which develop within the body of the mother (viviparous teleosts,
INTRODUCTION
519
sharks, mammals) or within well-protected egg membranes (turtle, chick)
slur over the larval condition.
The larval stage in non-viviparous fishes (see Kyle, ’26, pp. 74-82) and in the majority of amphibia is a highly differentiated condition in which the organs of the body are adapted to a free-living, watery existence. The tadpole of the frog, Rana pipiens, from the 6-mm. stage to the 11 -mm. stage, presents a period during which the primitive embryonic condition, present at the time of hatching (i.e., about 5 mm.), is transformed into a well-developed larval stage capable of coping with the external environment. From this time on to metamorphosis, the little tadpole possesses free-living larval features. Another example of a well-developed, free-living, larval stage among vertebrates is that of the eel, Anguilla rostrata. Spawning occurs in the ocean depths around the West Indies and Bermuda. Following the early embryonic stage in which primitive body form is attained, the young transforms into a form very unlike the adult. This form is called the Leptocephalus. The Leptocephalus was formerly classified as a distinct species of pelagic fishes. After many months in the larval stage, it transforms into the adult form of the eel. The latter migrates into fresh-water streams, the American eel into streams east of the Rockies and the European eel into the European streams (Kyle, ’26, pp. 54-58). The larval stages in most fishes conform more nearly to the adult form of the fish.
The embryo of Squalus acanthias at 20 to 35 mm. in length, the chick embryo at 5 to 8 days of incubation, the pig embryo of 12- to 18-mm. length, and the human embryo of 12 to 20-mm. length may be regarded as being in the stage of larval transition. The young opossum, when it is born, is in a late larval state. It gradually metamorphoses into the adult body form within the marsupium of the mother (Chap. 22).
3) Definitive Body Form. The general form and appearance of the adult constitute definitive body form. The young embryo of Squalus acanthias, at about 40 mm. in length, assumes the general appearance of the adult shark; the frog young, after metamorphosis, resembles the adult frog (Chap. 21), the chick of 8 to 13 days of incubation begins to simulate the form of the adult bird; the pig embryo of 20 to 35 mm. gradually takes on the body features of a pig, and the human fetus, during the third month of pregnancy, assumes the appearance of a human being. The transformation of the larval form into the body form of the adult is discussed further in Chapter 21 in relation to the endocrine system.
3. Basic or Fundamental Tissues
Through the stages of development to the period when the primitive or generalized, embryonic body form is attained, most of the cells which take part in development are closely associated. In the primitive embryonic body, this condition is found in all the five primitive body tubes and in the notochord. These closely arranged cells form the primitive epithelium. In the de
520
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
veloping head and tail regions, however, mesoderm is present in the form of
loosely aggregated cells, known as mesenchyme. While the cells of the epithelial variety are rounded or cuboidal in shape with little intercellular substance or space between the cells, mesenchymal cells tend to assume stellate
forms and to have a large amount of intercellular substance between them.
The primitive vascular or blood tubes are composed of epithelium in the sense
that the cells are closely arranged. However, as these cells are flattened and
show specific peculiarities of structure, this tissue is referred to as endothelium.
Also, while the cells of the early neural tube show the typical epithelial features, they soon undergo marked changes characteristic of developing neural
tissue. The primitive or generalized, embryonic body thus is composed of
four fundamental tissues, viz., epithelial, mesenchymal, endothelial, and neural
tissues.
B. Transformation of the Primitive Body Tubes into the Fundamental or Basic Condition of the Various Organ Systems Present in the Primitive Embryonic Body
1. Processes Involved in Basic System Formation
As the primitive body tubes (epidermal, neural, enteric, and mesodermal) are established, they are modified gradually to form the basis for the various organ systems. While the notochordal axis is not in the form of a tube, it also undergoes changes during this period. The morphological alterations, which transform the primitive body tubes into the basic or fundamental structural conditions of the systems, consist of the following:
(a) extension and growth of the body tubes,
(b) saccular outgrowths (evaginations) and ingrowths (invaginations) from restricted areas of the tubes,
(c) cellular migrations away from the primitive tubes fo other tubes and to the spaces between the tubes, and
(d) unequal growth of different areas along the tubes.
As a result of these changes, the primitive neural, epidermal, enteric, and mesodermal tubes, together with the capillaries or blood tubes and the notochord, experience a state of gradual differentiation which is directed toward the production of the particular adult system to be derived from these respective basic structures. The primitive body tubes, the primitive blood capillaries, and the notochord thus come to form the basic morphological conditions of the future or gut ^ systems. The basic structural conditions of the various systems are described in Chapters 12 to 21.
2. Fundamental Similarity of Early Organ Systems
The general form and structure of each primitive embryonic system, as it begins to develop in one vertebrate species, exhibits a striking resemblance
LAWS OF VON BAER
521
to the same system in other vertebrate species. This statement is particularly
true of the gnathostomous vertebrates (i.e., vertebrates with jaws). Consequently, we may regard the initial generalized stages of the embryonic or rudimentary systems as fundamental or basic plans of the systems, morphologically
if not physiologically. The problem which confronts the embryo of each
species, once the basic conditions of the various systems have been established,
is to convert the generalized basic condition of each system into an adult
form which will enable that system to function to the advantage of the particular animal in the particular habitat in which it lives. The conversion of
the basic or primitive condition of the various systems into the adult form of
the systems constitutes the subject matter of Chapters 12 to 21.
The basic conditions of the various organ systems are shown in the structure of shark embryos from 10 to 20 mm. in length, frog embryos of 5 to 10 mm., chick embryos from 55 to 96 hrs., pig embryos from 6 to 10 mm., crownrump length, and human embryos of lengths corresponding to 6 to 10 mm. That is to say, the basic or generalized conditions of the organ systems are present when primitive or generalized embryonic body form is developed. It is impossible to segregate any particular length of embryo in the abovementioned series as the ideal or exact condition showing the basic condition of the systems, as certain systems in one species progress faster than those same systems in other species. However, a study of embryos of these designations serves to provide an understanding of the basic or fundamental conditions of the various systems (figs. 257-262; also fig. 347A).
C. Laws of von Baer
As indicated above, the species of the vertebrate group as a whole tend to follow strikingly similar (although not identical) plans of development during blastulation, gastrulation, tubulation, the development of the basic plan of the various systems and primitive body form. As observed in the chapters which follow, the fundamental or basic plan of any particular, organ-forming system, in the early embryo of one species, is comparable to the basic plan of that system in other species throughout the vertebrate group. However, after these basic parallelisms in early development are completed, divergences from the basic plan begin to appear during the formation of the various organ systems of a particular species.
The classical statements or laws of Karl Ernst von Baer (1792-1876) describe a tendency which appears to be inherent in the developmental procedure of any large group of animals. This developmental tendency is for generalized structural features to arise first, to be remodeled later and supplanted by features specific for each individual species. To interpret these laws in terms of the procedure principle mentioned in Chapter 7, it may be assumed that general, or common, developmental procedures first are utilized, followed by
522
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
specific developmental procedures which change the generalized conditions
into specific conditions.
The laws of von Baer ( 1 828-1837, Part I, p. 224) may be stated as follows:
(a) The general features of a large group of animals appear earlier in development than do the special features;
(b) after the more general structures are established, less general structures arise, and so on until the most special feature appears;
(c) each embryo of a given adult form of animal, instead of passing through or resembling the adult forms of lower members of the group, diverges from the adult forms, because
(d) the embryo of a higher animal species resembles only the embryo of the lower animal species, not the adult form of the lower species.
D. Contributions of the Mesoderm to Primitive Body Formation and Later Development
The mesoderm is most important to the developing architecture of the body. Because the mesoderm enters so extensively into the structure of the many organs of the developing embryo, it is well to point out further the sources of mesoderm and to delineate the structures and parts arising from this tissue.
1. Types of Mesodermal Cells
Most of the mesoderm of the early embryo exists in the form of epithelium (see p. 519). As development proceeds, much of the mesoderm loses the close arrangement characteristic of epithelium. In doing so, the cells separate and assume a loose connection. They also may change their shapes, appearing stellate, oval, or irregular, and may wander to distant parts of the body. This loosely aggregated condition of mesoderm forms the primitive mesenchyme. Though most of the mesoderm becomes transformed into mesenchyme, the inner layer of cells of the original hypomeric portion of the mesodermal tubes retains a flattened, cohesive pattern, described as mesothelium. Mesothelium comes to line the various body cavities, for these cavities are derived directly from the hypomeric areas of the mesodermal tubes (Chap. 20).
2. Origin of the Mesoderm of the Head Region
The primary cephalic outgrowth (Chap. 10), which later forms the head structures, contains two basic regions, namely, the head proper and the pharyngeal or branchial region. During its early development, the heart lies at the ventro-caudal extremity of the general head region; it recedes gradually backward as the head and branchial structures develop. The exact origin of the mesoderm which comes to occupy the head proper and pharyngeal areas varies in different gnathostomous vertebrates. The general sources of the head mesoderm may be described in the following manner.
CONTRIBUTIONS OF THE MESODERM TO PRIMITIVE BODY FORMATION
523
a. Head Mesoderm Derived from the Anterior Region of the Trunk
The mesoderm of the branchial area in lower vertebrates, such as the snarks and, to some degree, the amphibia, represents a direct anterior extension of the mesoderm of the trunk (figs. 217D, E; 230D; 252E) . It is divisible into two parts: (1) a ventro-lateral region, the hypomeric or lateral plate mesoderm, and (2) a dorsal or somitic portion. The latter represents a continuation into the head region of the epimeric (somitic) mesoderm of the trunk. That portion of the mesoderm of the branchial area which may be regarded specifically as part of the mesoderm of the head proper is the mesoderm associated with the mandibular and hyoid visceral arches, together with the hyoid and mandibular somites located at the upper or dorsal ends of the hyoid and mandibular visceral arches (fig. 217D, E).
In the higher vertebrates (reptiles, birds, and mammals), the mesoderm of the branchial region appears early, not as a continuous epithelium, as in the shark and amphibian embryo, but as a mass of mesenchyme which wanders into the branchial area from the anterior portion of the developing trunk region (figs. 217F; 23 3B; 234B). This mesenchyme assumes branchial region characteristics, for it later condenses to form the mandibular, hyoid, and more posteriorly located, visceral arches. Also, mesenchymal condensations appear which correspond to the pre-otic head somites formed in the early shark embryo. For example, in the chick, there is an abducent condensation, which corresponds to the hyoid somite of the shark embryo, and a superior oblique condensation corresponding probably to the mandibular somite of the shark embryo (cf. fig. 217D, F). (See also Adelmann, ’27, p. 42.) Both of these condensations give origin to eye muscles (Chap. 16). Somewhat similar condensations of mesenchyme which form the rudiments of eye muscles occur in other members of the higher vertebrate group.
b. Head Mesoderm Derived from the Pre-chordal Plate
The term pre-chordal plate mesoderm signifies that portion of the head mesoderm which derives from the pre-chordal plate area located at the anterior end of the foregut. The pre-chordal plate mesoderm is associated closely with the foregut entoderm and anterior extremity of the notochord in the late blastula and gastrula in the fishes and amphibia. However, in reptiles, birds, and mammals, this association is established secondarily with the foregut entoderm by means of the notochordal canal and primitive-pit invaginations during gastrulation. (See Chap. 9 and also Hill and Tribe, ’24.)
(Note: It is advisable to state that Adelmann, ’32, relative to the 19-somite embryo of the urodele Ambystoma pimctatum, distinguishes between a prechordal mesoderm, which forms the core of the mandibular visceral arch, and the pre-chordal plate mesoderm, which earlier in development is associated with the dorsal anterior portion of the foregut entoderm. See figure 252E.)
During the period when the major organ-forming areas are being tubulated.
NEURAL ECTODERM
.RANCHIAL POUCHBRANCHIAL GROOVE OR gill- SL 1 T AREA
HYPOMERICl
MESOOERMAI^
CONTRIBUTION ^
TO LATERAL
BODY WALL
MESENCHYMAL
CONTRIBUTION
FROM SPLANCHNIC
LAYER OF HYPOMERE
Fig. 252. Mesodermal contributions to developing body. (A-D) Sections through
developing chick of 48-52 hrs. of incubation. (A) Section through somites of caudal
trunk area showing primitive area of mesoderm and coelomic spaces. (B) Section
through anterior trunk area depicting early differentiation of somite. (C) Section
through trunk area posterior to heart revealing later stage of somite differentiation than
that shown in B. (D) Section through developing heart area. Observe dermomyotome,
sclerotomic mesenchyme, and mesenchymal contributions of hypomere to forming body
substance. (E) Mesodermal contributions to anterior end of developing embryo of
Ambystoma of about 19 somites. (Redrawn and modified from Adelmann: 1932, J.
Morphol. 54.) (F) Frontal section of early post-hatching larva of Rana pipiens show
ing mass of mesoderm lying between gut, epidermal and neural tubes, together with the
contributions of the mesoderm to the visceral arches.
524
CONTRIBUTIONS OF THE MESODERM TO PRIMITIVE BODY FORMATION
525
the pre-chordal plate mesoderm separates as a mass of mesenchyme from the
antero-dorsal aspect of the foregut, anterior to the cephalic terminus of the
notochord (fig. 232G, H). It migrates forward as two groups of mesenchyme
connected at first by an interconnecting bridge of mesenchyme. Eventually
these two mesenchymal masses become separated and each forms a dense
aggregation of mesodermal cells over the mandibular visceral arch and just
caudal to the eye (fig. 252E). In the shark embryo and in the chick it gives
origin to the pre-mandibular somites (condensations) which probably give
origin to the eye muscles innervated by the oculomotor or third cranial nerves.
In Ambystoma, Adelmann (’32, p. 52) describes the pre-chordal plate mesoderm as giving origin to “the eye muscles†and “probably much of the head
mesenchyme ahead of the level of the first (gill) pouch, but its caudal limit
cannot be exactly determined.†Thus it appears that a portion of the head
mesoderm in the region anterior to the notochordal termination is derived
from the pre-chordal plate mesoderm in all vertebrates.
c. Head Mesoderm Contributed by Neural Crest Material
A conspicuous phase of the development of the head region in vertebrate embryos is the extensive migration of neural crest cells which arise in the middorsal area as the neural tube is formed (Chap. 10; fig. 222C-F). Aside from contributing to the nervous system (Chap. 19), a portion of the neural crest material migrates extensively lateroventrally and comes to lie within the forming visceral (branchial) arches, contributing to the mesoderm in these areas (figs. 222C-F; 230D, F). Also, consult Landacre (’21); Stone (’22, ’26, and ’29); and Raven (’33a and b). On the other hand, Adelmann (’25) in the rat and Newth (’51 ) in the lamprey, Lampetra planeri, were not able to find evidence substantiating this view. However, pigment cells (melanophores) of the skin probably arise from neural crest cells in the head region of all vertebrate groups.
d. Head Mesoderm Originating from Post-otic Somites
There is good evidence that the musculature of the tongue takes its origin in the shark embryo and lower vertebrates from cells which arise from the somites of the trunk area, immediately posterior to the otic (ear) vesicle, from whence they migrate ventrad to the hypobranchial region and forward to the area of the developing tongue (fig. 253). In the human embryo, Kingsbury (’15) suggests this origin for the tongue and other hypobranchial musculature. However, Lewis (’10) maintains that, in the human, the tongue musculature arises from mesenchyme in situ.
3. Origin of the Mesoderm of the Tail
In the Amphibia, the tail mesoderm has been traced by means of the Vogt staining method to tail mesoderm in the late blastular and early gastrular
526
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
stages. At the time of tail-rudiment formation, this mesoderm forms two bilateral masses of cells located within the “tail bud†or “end bud.†These cellular
masses proliferate extensively as the tail bud grows caudally and give origin
to the mesoderm of the tail. Similarly, in other vertebrates, the mesoderm of
the future tail is present as mesenchyme in the terminal portion of the tail
bud. These mesenchymal cells proliferate, as the tail grows caudalward, and
leave behind the mesoderm, which gradually condenses into the epithelial
masses or segments (myotomes) along either side of the notochord and
neural tube.
4. Contributions of the Trunk Mesoderm to the Developing Body
The mesoderm of the trunk area contributes greatly to the development of the many body organs and systems in the trunk region. Details of this contribution will be described in the chapters which follow, but, at this point, it is well to survey the initial activities of the mesodermal tubes of the trunk area in producing the vertebrate body.
a. Early Differentiation of the Somites or Epimere
The somites (figs. 217, 237, 252) contribute much to the developing structure of the vertebrate body. This fact is indicated by their early growth and differentiation. For example, the ventro-mesial wall of the fully developed somite gradually separates from the rest of the somite and forms a mass of mesenchymal cells which migrates mesad around the notochord and also dorsad around the neural tube (fig. 252A-C). The mesenchyme which thus arises from the somite is known as the sclerotome. In the somite of the higher vertebrates just previous to the origin of the sclerotome, a small epithelial core of cells becomes evident in the myocoel; this core contributes to the sclerotomic material (fig. 252B). As a result of the segregation of the sclerotomic tissue and its migration mesad to occupy the areas around the notochord and nerve cord, the latter structures become enmeshed by a primitive skeletogenous mesenchyme. The notochord and sclerotomic mesenchyme are the foundation for the future axial skeleton of the adult, including the vertebral elements and the caudal part of the cranium as described in Chapter 15.
After the departure of sclerotomic material, myotomic and dermatomic portions of the somite soon rearrange themselves into a hollow structure (fig. 252C, D), in which the myotome forms the inner wall and the dermatome the outer aspect. This composite structure is the dermomyotome, and the cavity within, the secondary myocoei. In many vertebrates (fishes, amphibia, reptiles, and birds), the dermatome gives origin to cells which migrate into the region of the developing dermis (Chap. 12) and contributes to the formation of this layer of the skin.
CONTRIBUTIONS OF THE MESODERM TO PRIMITIVE BODY FORMATION
527
b. Early Differentiation of the Mesomere (Nephrotome)
The differentiation of the nephrotome or intermediate mesoderm will be considered later (Chap. 18) in connection with the urogenital system.
c. Early Differentiation and Derivatives of the Hypomere
The lateral-plate mesoderm (hypomere), figure 252A, performs an extremely important function in embryological development. The cavity of the hypomere (splanchnocoel) and the cellular offspring from the hypomeric mesoderm, which forms the wall of this cavity, give origin to much of the structural material and arrangement of the adult body.
1) Contributions of the Hypomere (I^ateral Plate Mesoderm) to the Developing Pharyngeal Area of the Gut Tube. The developing foregut (Chap. 13) may be divided into four main areas, namely, (1) head gut, (2) pharyngeal, (3) esophageal, and (4) stomach areas. The head gut is small and represents a pre-oral extension of the gut; the pharyngeal area is large and expansive and forms about half of the forming foregut in the early embryo; the esophageal segment is small and constricted; and the forming stomach region is enlarged. At this point, however, concern is given specifically to the developing foregut in relation to the early development of the pharyngeal region.
In the pharyngeal area the foregut expands laterally. Beginning at its anterior end, it sends outward a series of paired, pouch-like diverticula, known as the branchial (pharyngeal or visceral) pouches. These pouches push outward toward the ectodermal (epidermal) layer. In doing so, they separate the lateral plate mesoderm which synchronously has divided into columnar masses or cells (fig. 252E, F). Normally, about four to six pairs of branchial (pharyngeal) pouches are formed in gnathostomous vertebrates, although in the cyclostomatous fish, Petromyzon, eight pairs appear. In the embryo of the shark, Squalus acanthias, six pairs are formed, while in the amphibia, four to six pairs of pouches may appear (fig. 252F). In the chick, pig, and human, four pairs of pouches normally occur (figs. 259, 261). Also, invaginations or inpushings of the epidermal layer occur, the branchial grooves (visceral furrows); the latter meet the entodermal outpocketings (figs. 252F; 262B).
The end result of all these developmental movements in the branchial area is to produce elongated, dorso-ventral, paired columns of mesodermal cells (figs. 252E; 253), the visceral or branchial arches, which alternate with the branchial-groove-pouch or gill-slit areas (figs. 252F; 253). The most anterior pair of visceral arches forms the mandibular visceral arches; the second pair forms the hyoid visceral arches; and the succeeding pairs form the branchial (gill) arches (figs. 239C, D; 240; 244; 246; 252E; 253). The branchial arches with their mesodermal columns of cells will, together with the contributions from the neural crest cells referred to above, give origin to the connective, muscle, and blood-vessel-forming tissues in this area.
528
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
2) Contributions of the Hypomere (Lateral Plate Mesoderm) to the Formation of the Gut Tube and Heart Structures. Throughout the length of the
forming gut tube, from the oral area to the anal region, the lateral plate mesoderm (mesoblast) contributes much to the forming gut tube. This is occasioned to a great extent posterior to the pharyngeal area by the fact that the
inner or mesial walls of the two hypomeres enswathe the forming gut tube
as they fuse in the median plane (fig. 241), forming the dorsal and ventral
mesenteries of the gut. However, in the heart area, due to the dorsal displacement of the foregut, the dorsal mesentery is vestigial or absent while
the ventral mesentery is increased in extent. Each mesial wall of the hypomeric
mesoderm, forming the ventral mesentery in the region of the developing
heart, becomes cupped around the primitive blood capillaries, coursing anteriad in this area to form the rudiments of the developing heart. The ventral
mesentery in the heart area thus gives origin to the dorsal mesocardium, the
ventral mesocardium, and the rudimentary, cup-shaped, cpimyocardial structures around the fusing blood capillaries (figs. 236C-D; 254A). The primitive
blood capillaries soon unite to form the rudiment of the future endocardium
of the heart, while the enveloping epimyocardium establishes the rudiment of
the future muscle and connective tissues of the heart (Chap. 17).
On the other hand, in the region of the stomach and continuing posteriorly to the anal area of the gut, the movement mediad of the mesial walls of the two lateral plate (hypomeric) mesodermal areas occurs in such a way as to
Fig. 253. Diagram illustrating the basic plan of the vertebrate head based upon the shark, Scy Ilium canicula. (Modified from Goodrich: 1918, Quart. Jour. Micros. Science, 63.)
CONTRIBUTIONS OF THE MESODERM TO PRIMITIVE BODY FORMATION
529
the hypomeres to the developing heart and gut structures in reptiles, birds, and mammals. Sections are drawn through the following regions: (A) Through primitive tubular heart anterior to sinus venosus. (B) Through caudal end of sinus venosus and lateral meso* cardia. (C) Through liver region. (D) Through region posterior to liver. (E) Through posterior trunk in region of urinary bladder.
envelop or enclose the gut tube. This enclosure readily occurs because in this region of the trunk, the gut tube lies closer to the ventral aspect of the embryo than in the heart area. Consequently, a dorsal mesentery above and a ventral mesentery below the primitive gut tube are formed (fig. 25 4C). The dorsal and ventral mesenteries may not persist everywhere along the gut (fig. 254D). The degree of persistence varies in different vertebrates; these variations will be mentioned later (Chap. 20) when the coelomic cavities are discussed. However, there is a persistence of the ventral mesentery below the stomach and anterior intestinal area of all vertebrates, for here the ventral mesentery (i.e., the two medial walls of the lateral plate mesoderm below the gut) contributes to the development of the liver and the pancreas. These matters are discussed in Chapter 13.
Aside from the formation of the dorsal and ventral mesenteries by the inward movement and fusion of the medial walls of the lateral plate mesoderm above and below the primitive enteron or gut tube, that part of the medial walls of the lateral plate mesoderm which envelops the primitive gut itself is of great importance. This importance arises from the fact that the entoderm of the gut only forms the lining tissue of the future digestive tract and its various glands, such as the liver, pancreas, etc., whereas mesenchymal contributions from the medial wall of the lateral plate mesoderm around the
530
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
entodermal lining give origin to smooth muscle tissue, connective tissue, etc.
(figs. 254C, D; 258; 260; 262; 278C). It is apparent, therefore, that the gut
throughout its length is formed from two embryonic contributions, namely,
one from the entoderm and the other from the mesenchyme given off by the
medial walls of the lateral plate or hypomeric mesoderm.
{Note: The word splanchnic is an adjective and is derived from a Greek word meaning entrails or bowels. That is, it pertains to the soft structures within the body wall. The plural noun viscera (singular, viscus) is derived from the Latin and signifies the same structures, namely, the heart, liver, stomach, intestine, etc., which lie within the cavities of the body. It is fitting, therefore, to apply the adjective splanchnic to the medial portion of the hypomere because it has an intimate relationship with, and is contributory to, the development of the viscera. The somatic mesoderm, on the other hand, is the mesoderm of the lateral or body-wall portion of the hypomere. The word splanchnopleure is a noun and it designates the composite tissue of primitive entoderm and splanchnic mesoderm, while the word somatopleure is applied to the compound tissue formed by the primitive lateral wall of the hypomere (somatic mesoderm) plus the primitive ectoderm overlying it. The coelom proper or spianchnocoel is the space or cavity which lies between the splanchnic and somatic layers of the lateral plate or hypomeric mesoderm. During later development, it is the cavity in which the entrails lie.
3) Contributions of the Hypomere (Lateral Plate Mesoderm) to the External (Ectodermal or Epidermal) Body Tube. The somatopleural mesoderm gives origin to a mass of cellular material which migrates outward to lie along the inner aspect of the epidermal tube in the lateral and ventral portions of the developing body (fig. 252A, D). In the dorsal and dorso-lateral regions of the body, contributions from the sclerotome and dermatome apparently aid in forming this tissue layer. The layer immediately below the epidermis constitutes the embryonic rudiment of the dermis. (See Chap. 12.)
4) Contributions of the Hypomere or Lateral Plate Mesoderm to the Dorsal Body Areas. Many cells are given off both from splanchnic and somatic layers of the hypomeric mesoderm to the dorsal body areas above and along either side of the dorsal aorta (fig. 254), contributing to the mesenchymal “packing tissue†in the area between the notochord and differentiating somite, extending outward to the dermis.
5) Contributions of the Lateral Plate Mesoderm to the Walls of the Coelomic Cavities. The pericardial, pleural, and peritoneal cavities are lined, as stated above, by an epithelial type of tissue called mesothelium (fig. 254A-E). These coelomic spaces (see Chap. 20) are derived from the fusion of the two primitive splanchnocoels or cavities of the two hypomeres. External to the mesothelial lining of the coelomic spaces, there ultimately is developed a fibrous, connective tissue layer. Thus, mesothelium and connective tissue form.
Fig. 255. This figure illustrates different types of body form in various vertebrates
during embryonic development. A, D, H, M, and Q show primitive embryonic body
form in the developing shark, rock fish, frog, chick, and human. B, larval form of
shark; E and F, larval forms of rock fish; I and J, larval forms of frog; N and O, larval
forms of chick; R, larval form of human. C, G, K, L, P, and S represent definitive
body form in the above species. (Figures on rockfish development (Roccus saxatilis) redrawn from Pearson: 1938, Bull. Bureau of Fisheries, L). S. Dept, of Commerce, vol.
49; figures on chick redrawn from Hamburger and Hamilton: 1951, J. Morphol., vol.
88; figure Q, of developing human embryo, redrawn and modified from model based
upon Normentafeln of Keibel and Elze: 1908, vol. 8, G. Fischer, Jena; Dimensions of
human embryos in R and S, from Mall: Chap. 8, vol. 1, Human Embryology, by
F. Keibel and F. P. Mall, 1910, Lippincott, Philadelphia.)
531
532
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
in general, the walls of the coelomic spaces. These two tissues arise directly
from the hypomeric mesoderm.
5. Embryonic Mesenchyme and Its Derivatives
The mesenchymal cells given off from the mesodermal tubes of the trunk area, namely, (1) sclerotomic mesenchyme, (2) dermatomic mesenchyme, (3) mesenchymal contributions from the lateral plate mesoblast (hypomere) to the gut, skin, heart, and (4) the mesenchyme contributed to the general regions of the body lying between the epidermal tube, coelom, notochord, and neural tube, form, together with the head and tail mesoderm, the general packing tissue which lies between and surrounding the internal tubular structures of the embryo (fig. 254). Its cells may at times assume polymorphous or stellate shapes. This loose packing tissue of the embryo constitutes the embryonic mesenchyme. (See Chap. 15.)
This mesenchyme ultimately will contribute to the following structures of the body:
(a) Myocardium (cardiac musculature, etc.) and the epicardium or covering coelomic layer of the heart (Chap. 17),
(b) endothelium of blood vessels, blood cells (Chap. 17),
(c) smooth musculature and connective tissues of blood vessels (Chaps. 16 and 17),
(d) spleen, lymph glands, and lymph vessels (Chap. 17),
(e) connective tissues of voluntary and involuntary muscles (Chap. 16),
(f) connective tissues of soft organs, exclusive of the nerve system (Chap. 15),
(g) connective tissues in general, including bones and cartilage (Chap. 15),
(h) smooth musculature of the gut tissues and gut derivatives (Chap. 16),
(i) voluntary or striated muscles of the tail from tail-bud mesenchyme (Chap. 16),
(j) striated (voluntary) musculature of face, jaws, and throat, derived from the lateral plate mesoderm in the anterior pharyngeal region (Chap. 16),
(k) striated (voluntary) extrinsic musculature of the eye (Chap. 16),
(l) intrinsic, smooth musculature of the eye (Chap. 16),
(m) tongue and musculature of bilateral appendages, derived from somitic muscle buds (sharks) or from mesenchyme possibly of somitic origin (higher vertebrates) (Chap. 16), and
(n) chromatophores or pigment cells of the body from neural crest mesenchyme (Chap. 12).
SUMMARY OF DERIVATIVES OF ORGAN-FORMING AREAS
533
£. Summary of Later Derivatives of the Major Presumptive Organforming Areas of the Late Blastula and Gastrula
1. Neural Plate Area (Ectoderm)
This area gives origin to the following:
(a) Neural tube,
(b) optic nerves and retinae of eyes,
(c) peripheral nerves and ganglia,
(d) chromatophores and chromaffin tissue (i.e., various pigment cells of the skin, peritoneal cavity, etc., chromaffin cells of supra-renal gland),
(e) mesenchyme of the head, neuroglia, and
(f) smooth muscles of iris.
2. Epidermal Area (Ectoderm)
This area gives origin to:
(a) Epidermal tube and derived structures, such as scales, hair, nails, feathers, claws, etc.,
(b) lens of the eye, inner ear vesicles, olfactory sense area, general, cutaneous, sense organs of the peripheral area of the body,
(c) stomodaeum and its derivatives, oral cavity, anterior lobe of pituitary, enamel organs, and oral glands, and
(d) proctodaeum from which arises the lining tissue of the anal canal.
3. Entoderm AL Area
From this area the following arise:
(a) Epithelial lining of the primitive gut tube or metenteron, including: (1) epithelium of pharynx; epithelium pharyngeal pouches and their derivatives, such as auditory tube, middle-ear cavity, parathyroids, and thymus; (2) epithelium of thyroid gland; (3) epithelial lining tissue of larynx, trachea, and lungs, and (4) epithelium of gut tube and gut glands, including liver and pancreas,
(b) most of the lining tissue of the urinary bladder, vagina, urethra, and associated glands,
(c) Seessel’s pocket or head gut, and
(d) tail gut.
4. Notochordal Area
This area:
(a) Forms primitive antero-posterior skeletal axis of all chordate forms,
(b) aids in induction of central nerve tube.
534
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
(c) gives origin to adult notochord of Amphioxus and cyclostomatous fishes
and to notochordal portions of adult vertebral column of gnathostomous
fishes and water-living amphibia, and
(d) also, comprises the remains of the notochord in land vertebrates, such as “nucleus pulposus†in man.
5. Mesodermal Areas
These areas give origin to:
(a) Epimeric, mesomeric, and hypomeric areas of primitive mesodermal tube,
(b) epimeric portion also aids in induction of central nerve tube,
(c) muscle tissue, involuntary and voluntary,
(d) mesenchyme, connective tissues, including bone, cartilage,
(e) blood and lymphoid tissue,
(f) gonads with exception of germ cells, genital ducts, and glandular tissues of male and female reproductive ducts, and
(g) kidney, ureter, musculature and connective tissues of the bladder, uterus, vagina, and urethra.
6. Germ-cell Area
This area gives origin to:
(a) Primordial germ cells and probably to definitive germ cells of all vertebrates below mammals and
(b) primordial germ cells of mammals and possibly to definitive germ cells.
F. Metamerism
1. Fundamental Metameric Character of the Trunk and Tail Regions of the Vertebrate Body
Many animals, invertebrate as well as vertebrate, are characterized by the fact that their bodies are constructed of a longitudinal series of similar parts or metameres. As each metamere arises during development in a similar manner and from similar rudiments along the longitudinal or antero-posterior axis of the embryo, each metamere is homologous with each of the other metameres. This type of homology in which the homologous parts are arranged serially is known as serial homology. Metamerism is a characteristic feature of the primitive and later bodies of arthropods, annelids, cephalochordates, and vertebrates.
In the vertebrate group, the mesoderm of the trunk and tail exhibits a type of segmentation, particularly in the epimeric or somitic area. Each pair of somites, for example, denotes a primitive body segment. The nervous system
^OPTIC VESICLE LENS PLACODE .
^ nasal placode — —maxillary process
mandibular arch
branchial arch
nasal placode
ORAL OPENING
Laxillary PROCESstl^
.
mandibular ARCH
\ ^nasolateral
PROCESS
^ NaSOMEDIAL -*
process I naso-optic furrow 'maxillary process "mandibular arch
hyomandibular cleft
NASOMEDIAL
process
NASOLATERAL
process
naso-optic
furrow
'hyomandibular
CLEFT
tubercles around ^ hyomandibular CLEFT § fusing to form
f external EAR'
...»
NASOLATERAL PROCESS^
NASOMEDIAL PROCESSES
fusing to form PHILTRUM-. OF LIP
EXTERNAL EAR
ear tubercles around hyomandibular cleft
-hyoid bone REGlONr
ih j 1
F.O. 256. Developmental features of the human fac. Modified slightly from models by B. Ziegler, Freiburg, after Karl Peter.
535
536
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
also manifests various degrees of segmentation (Chap. 19), although the
origin and arrangement of the peripheral nerves in the form of pairs, each
pair innervating a pair of myotomic derivatives of the somites, is the most
constant feature.
In the cephalochordate, Amphioxus, the segmentation of the early mesoderm is more pronounced than that of the vertebrate group. As observed in Chapter 10, each pair of somites is distinct and entirely separate from other somitic pairs, and each pair represents all the mesoderm in the segment or metamere. That is, all the mesoderm is segmented in Amphioxus. However, in the vertebrate group, only the more dorsally situated mesoderm undergoes segmentation, the hypomeric portion remaining unsegmented.
2. Metamerism and the Basic Morphology of the Vertebrate Head
While the primitive, metameric (segmental) nature of the vertebrate trunk and tail areas cannot be gainsaid, the fundamental metamerism of the vertebrate head has been questioned. Probably the oldest theory supporting a concept of cephalic segmentation was the vertebral theory of the skull, propounded by Goethe, Oken, and Owen. This theory maintained that the basic structure of the skull demonstrated that it was composed of a number of modified vertebrae, the occipital area denoting one vertebra, the basisphenoidtemporo-parietal area signifying another, the presphenoid-orbitosphenoidfrontal area denoting a third vertebra, and the nasal region representing a fourth cranial vertebra. (Consult Owen, 1848.) This theory, as a serious consideration of vertebrate head morphology was demolished by the classic Croonian lecture given in 1858 by Huxley (1858) before the Royal Society of London. His most pointed argument against the theory rested upon the fact that embryological development failed to support the hypothesis that the bones of the cranium were formed from vertebral elements.
A factor which aroused a renewal of interest in a segmental interpretation of the vertebrate head was the observation by Balfour (1878) that the head of the elasmobranch fish, Scy Ilium, contained several pairs of pre-otic (prootic) somites (that is, somites in front of the otic or ear region). Since Balfour’s publication, a large number of studies and dissertations have appeared in an endeavor to substantiate the theory of head segmentation. The anterior portion of the central nervous system, cranial nerves, somites, branchial (visceral) arches and pouches, have all served either singly or in combination as proffered evidence in favor of an interpretation of the primitive segmental nature of the head region. However, it is upon the head somites that evidence for a cephalic segmentation mainly depends.
A second factor which stimulated discussion relative to head segmentation was the work of Locy (1895) who emphasized the importance of so-called neural segments or neuromcres (Chap. 19) as a means of determining the
ARROWS SHOW water CURRENTS
Fig. 257. Drawings of early frog tadpoles showing development of early systems.
(A) Frog tadpole (R. pipiens) of about 6 7 mm. It is difficult to determine the exact
number of vitelline arteries at this stage of development and the number given in the
figure is a diagrammatic representation. {A') Shows right and left ventral aortal divisions of bulbus cordis. (B) Anatomy of frog tadpole of about 10-18 mm. See also
figures 280 and 335.
537
540
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
primitive segmental structure of the vertebrate brain. It is to be observed that
the more conservative figure 253, taken from Goodrich, does not emphasize
neuromeres, for, as observed by Kingsbury (’26, p. 85), the evidence is overwhelmingly against such an interpretation. The association of the cranial nerves
with the gill (branchial) region and the head somites, shown in figure 253,
will be discussed further in Chapter 19.
A third factor which awakened curiosity, concerning the segmental theory of head development, is branchiomerism. The latter term is applied to the development of a series of homologous structures, segmentally arranged, in the branchial region; these structures are the visceral arches and branchial pouches referred to above. As mentioned there, the branchial pouches or outpocketings of the entoderm interrupt a non-segmented mass of lateral plate (hypomeric) mesoderm, and this mesoderm secondarily becomes segmented and located within the visceral arches. These arches when formed, other than possibly the mandibular and the hyoid arches (fig. 253), do not correspond with the dorsal somitic series. Consequently, “branchiomerism does not, therefore, coincide with somitic metamerism.†(See Kingsbury, ’26, p. 106.)
Undoubtedly, much so-called “evidence†has been accumulated to support a theory of head segmentation. A considerable portion of this evidence apparently is concerned more with segmentation as an end in itself than with a frank appraisal of actual developmental conditions present in the head (Kingsbury and Adelmann, ’24 and Kingsbury, ’26). However, the evidence which does resist critical scrutiny is the presence of the head somites which includes the pre-otic somites and the first three or four post-otic somites. While the pre-otic somites are somewhat blurred and slurred over in their development in many higher vertebrates, the fact of their presence in elasmobranch fishes is indisputable and consistent with a conception of primitive head segmentation.
Furthermore, aside from a possible relationship with head-segmentation phenomena, the appearance of the pre-otic and post-otic head somites coincides with basic developmental tendencies. As observed above, for example, there is a tendency for nature to use generalized developmental procedures in the early development of large groups of animals (see von Baer’s laws, p. 522, and also discussion relative to Haeckel’s biogenetic law in Chap. 7). Nature, in other words, is utilitarian, and one can be quite certain that if general developmental procedures are used, they will prove most efficient when all factors are considered. At the same time, while generalized procedures may be used, nature does not hesitate to mar or elide parts of procedures when needed to serve a particular end. The obliteration of developmental steps during development is shown in the early development of the mesoderm in the vertebrate group compared to that which occurs in Amphioxus. In the vertebrate embryo, as observed previously, the hypomeric mesoderm is unsegmented except in a secondary way and in a restricted area as occurs in branchiomerism. However, in Amphioxus, early segmentation of the meso
METAMERISM
541
derm is complete dorso-ventrally, including the hypomeric region of the
mesoderm. It becomes evident, therefore, that the suppression of segmentation
in the hypomeric area in the vertebrate embryo achieves a precocious result
which the embryo of Amphioxus reaches only at a later period of development. Presumably in the vertebrate embryo, segmentation of the epimeric
mesoderm is retained because it serves a definite end, whereas segmentation
of the hypomeric mesoderm is deleted because it also leads to a necessary end
result in a direct manner.
When applied to the developing head region, this procedure principle means this: A primitive type of segmentation does tend to appear in the pre-otic area as well as in the post-otic portion of the head, as indicated by the pre-otic and post-otic somites, and secondarily there is developed a branchial metam
GASSERIAN GANGLION I ME TENCEPHAUON
geniculate GANGLION OF NERVE Stt ACOUSTIC GANGLION OF NERVE :
MYf lencephalon OTIC VESICLE
SUPERIOR GANGLION OF NERVE H JUGULAR GANGLION OF NERVE X PETROSAL GANGLION OF NERVE IX ^
NERVE :
NOOOSE ganglion OF nerve::
NERVE
SPINAL CORO-^
pharyngeal pouch in-<: pharyngeal POUCHBC; thyroid BODY BUL0US COROIS
MESENCEPHALON
â– NERVE 33
NERVE m
infundibulum E’S POCKET SEESSEL'S POCKET CHOROID FISSURE OlENCEPHALON
DORSAL aorta NOTOCHORD stomach LIVER
ventral pancreasdorsal pancreas
gall blaode
MESONEPHROS- —
MIDGUT
AN DUCT
glomeruli
COLLECTING DUCT HINDGUT
SPINAL GANGLION
Fig. 259. Chick embryo reconstruction of about 100 hrs. of incubation with special
reference to the nervous and urinary systems. See also fig. 336D.
bation. Reference should
5
BASIC HOMOLOGY OF ORGAN SYSTEMS
545
erism (branchiomerism) . However, all these segmental structures serve a
definite end. In other areas, head development proceeds in a manner which
obscures segmentation, for the probable reason that segmentation does not fit
into the developmental pattern which must proceed directly and precociously
to gain a specific end dictated by problems peculiar to head development.
{Note: For a critical analysis of the supposed facts in favor of segmentation, together with a marshaling of evidence against such an interpretation, consult Kingsbury and Adelmann (’24) and for a favorable interpretation of the segmental nature of the head region, see Goodrich (’18) and Delsman (’22). Figure 253 is taken from Goodrich (’18), and the various structures which favor a segmental interpretation of the head region are shown.)
G. Basic Homology of the Vertebrate Organ Systems
1. Definition
Homology is the relationship of agreement between the structural parts of one organism and the structural parts of another organism. An agreeable relationship between two structures is established if:
( 1 ) the two parts occupy the same relative position in the body,
(2) they arise in the same way embryonically and from the same rudiments, and
(3) they have the same basic potencies.
By basic potency is meant the potency which governs the initial and fundamental development of the part; it should not be construed to mean the ability to produce the entire structure. To the basic potency, other less basic potencies and modifying factors may be added to produce the adult form of the structure.
2. Basic Homology of Vertebrate Blastulae, Gastrulae, and Tubulated Embryos
In Chapters 6 and 7, the basic conditions of the vertebrate blastula were surveyed, and it was observed that the formative portion of all vertebrate blastulae presents a basic pattern, composed of major presumptive organforming areas oriented around the notochordal area and a blastocoelic space. During gastrulation (Chap. 9), these areas are reoriented to form the basic pattern of the gastrula, and although round and flattened gastrulae exist, these form one, generalized, basic pattern, composed of three germ layers arranged around the central axis or primitive notochordal rod. Similarly, in Chapter 10, the major organ-forming areas are tubulated to form an elongated embryo, composed of head, pharyngeal, trunk, and tail regions. As tubulation is effected in much the same manner throughout the vertebrate series and as the pre-chordal plate mesoderm, foregut entoderm, notochord, and somitic meso
546
BASIC FEATURES OF VERTEBRATE MORPHOGENESIS
geniculate ganglion of seventh nerve
ACOUSTIC GANGLION OF EIGHTH NERVE AUDITORY VESICLE
JU^dLAR GANGLION
SUPERIOR GANGLION NINTH NERV ACCESSORY ganglion BASILAR ARTERY DORSAL ROOT GANGLION OP FIRST
cervical nerve aortal arch I
AORTAL ARCH II AORTAL ARCH III AORTAL ARCH IV AORTAL ARCH VT PULMONARY ARTERY TRACHEA NOTOCHORD RIGHT ATRIUM LUNG
SMALL
INTESTINE
hepatic
PORTAL VEIN DORSAL AORTA
OMPHALOMESENTERIC
ARTERY
(FUTURE SUPERIOR MESENTERIC ARTERY)
GLOMERULUS
MESONEPHRIC TUBULE
DORSAL AORTA
MESONEPHRIC DUCT
Fig. 261. Drawings of pig embryos of about 9.5 to 12 mm. (A) Reconstruction of about
9.5 to 10 mm. pig embryo with special emphasis on the arterial system.
derm appear to be the main organizing influence throughout the series (Chap. 10), the conclusion is inescapable that the tubulated embryos of all vertebrates are homologous basically, having the same relative parts, arising in the same manner, and possessing the same basic potencies within the parts. To this conclusion must be added a caution, namely, that, although the main segments or specific organ regions along each body tube of one species are homologous with similar segments along corresponding tubes of other species, variations may exist and non-homologous areas may be insinuated or homologous areas
BASIC HOMOLOGY OF ORGAN SYSTEMS
547
may be deleted along the respective tubes. Regardless of this possibility, a
basic homology, however, appears to exist.
During later development through larval and definitive body-form stages, a considerable amount of molding or plasis by environmental and intrinsic factors may occur. An example of plasis is given in the development of the forelimb rudiment of the fish, frog, bird, and pig. In the definitive form, these structures assume different appearances and are adapted for different func
METENCEPHALON
BASILAR ARTERY
NOTOCHORD
ROOT OF TONGUE THYROID GLAND developing epiglottis AORTIC ARCH III L ARYN X
ESOPH AGU S
VALVES OF
SINUS 'VENOSUS/ LUNG bud'
SPINAL CORD SINUS VENOSU;
GALL BLADDER
NOTOCHORDOORSAL AORTA
DEVELOPING VERTEBRAE
MESONEPHRIC KIDNE
MESENCEPHALON
TUBERCULUM
ju / POSTERIUS ~ — ^INFUNDIBULUM OIEUCEPHALON
rathke's pocket
SEESSEL'S POCKET — -OPTIC CHIASMA
-RECESSUS OPTICUS TELENCEPHALON AMINA TERMINALIS TONGUE BULBUS CORDIS
EXTRA-EMBRYONIC COELOM
UMBILICAL CORD
ALLANTOIC DIVERTICULUM
GENITAL EMINENCE
PROCTODAEUM
CLOACA
ALLANTOIC STALK
B.
metanephrogenous
TISSUE SPINAL GANGLION
Fig. 261 — (Continued} (B) Median sagittal section of 10 mm. embryo.
VEIN OF maxillary REGION (BRANCH OF INTERNAL JUGULAR)
OTIC VESICLE
VEIN OF
MANDIBULAR REGION BRANCH OF EXTERNAL JUGULAR)
INTERNAL JUGULAR VEIN DORSAL
jSEGMENTAL VEINS EXTERNAL JUGULAR VEIN
LEFT DUCT OF CUVIER RIGHT VITELLINE VEIN LIVER DUCTUS VENOSUS HEPATIC VEINS PORTAL VEIN
UMBILICAL
ARTERY
'TRANSVERSE ANASTOMOSIS
OF SITBCAROINALS
POSTERIOR CARDINAL
VEIN
PIG EMBRYO SHOWING RIGHT HALF
OF VENOUS SYSTEM
Fig. 261 — (Continued) (C) Lateral view of 12 mm. embryo showing venous system.
(C is redrawn and modified from Minot; 1903, A Laboratory Text-book of Embryology,
Blakiston, Philadelphia.)
548
Fig. 262. Sections and stereograms of 10 mm. pig embryo.
MCSCNCHYME^
Ibl— (Continued) Sections and stereograms of 10 mm. pig embryo
BIBLIOGRAPHY
551
tional purposes. Basically, however, these structures are homologous, although
plasis produces adult forms which appear to be different.
A further statement should be added, concerning that type of molding or plasis of a developing structure which produces similar structures from conditions which have had a different genetic history. For example, the bat’s fore limb rudiment is molded to produce a structure resembling superficially that of the bird, although modern bats and birds have arisen through different lines of descent. Similarly, the teeth of certain teleost fishes superficially resemble the teeth of certain mammals, an effect produced from widely diverging lines of genetic descent. These molding effects or homoplasy, which produce superficially similar structures as a result of adaptations to certain environmental conditions, are called convergence, parallelism, and analogy. An example of experimental homoplasy is the induction of eye lenses in the embryo by the transplantation of optic-cup material to a place in the epidermis which normally does not produce a lens.
{Note: For a discussion of homology, homogeny, plasis, convergence, etc., see Tait, ’28.)
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