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

| 9. 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

Basic Features of Vertebrate Morphogenesis

11. Basic Features of Vertebrate Morphogenesis

A. Introduction

1. Purpose of This Chapter

2. Definitions

a. Morphogenesis and Related Terms

b. Primitive, Larval, and Definitive Body Forms (see fig. 255)

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

(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.


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 (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.)


Bibliography


Adelmann, H. B. 1925. The development of the neural folds and cranial ganglia of the rat. J. Comp. Neurol. 39:19.

. 1927. The development of the eye

muscles of the chick. J. Morphol. 44:29.

. 1932. The development of the

prechordal plate and mesoderm of Ambly stoma piinctatum. J. Morphol. 54:1.

Baer, K. E. von. 1828-1837. liber Entwickelungsgeschichte der Thiere. Beobachtung und Reflexion. Erster Theil, 1828; Zweiter Theil, 1837. Konigsberg, Borntriiger.

Balfour, F. M. 1878. Monograph on the development of elasmobranch fishes. Republished in 1885 in The Works of Francis Maitland Balfour, edited by M. Foster and A. Sedgwick, vol. 1. The Macmillan Co., London.

Delsman, H. C. 1922. The Ancestry of Vertebrates. Valkoff & Co., Amersfoort, Holland.

Goodrich, E. S. 1918. On the development of the segments of the head of Scy Ilium. Quart. J. Micr. Sc. 63:1.

Hill, J. P. and Tribe, M. 1924. The early development of the cat {Felis dornestica). Quart. J. Micr. Sc. 68:513.


Huxley, T. H. 1858. The Croonian lecture — on the theory of the vertebrate skull. Proc. Roy. Soc., London, s.B. 9:381.

Kingsbury, B. F. 1915. The development of the human pharynx. 1. Pharyngeal derivatives. Am. J. Anat. 18:329.

. 1924. The significance of the so called law of cephalocaudal differential growth. Anat. Rec, 27:305.

. 1926. Branchiomerism and the

theory of head segmentation. J. Morphol. 42:83.

and Adelmann, H. B. 1924. The

morphological plan of the head. Quart. J. Micr, Sc. 68:239.

Kyle, H. M. 1926. The Biology of Fishes. Sidgwick and Jackson, Ltd., London.

Landacre, F. L. 1921. The fate of the neural crest in the head of urodeles. J. Comp. Neurol. 33:1.

Lewis, W. H. 1910. Chapter 12. The development of the muscular system in Manual of Human Embryology, edited by F. Keibel and F. P. Mall. J. B. Lippincott Co., Philadelphia.

Locy, W. A. 1895. Contribution to the structure and development of the vertebrate head. J. Morphol. 11:497.


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BASIC FEATURES OF VERTEBRATE MORPHOGENESIS


Newth, D. R. 1951. Experiments on the neural crest of the lamprey embryo. J. Exper. Biol. 28:17.

Owen, R. 1848. On the archetype and homologies of the vertebrate skeleton. John Van Voorst, London.

Raven, C. P. 1933a. Zur Entwicklung der Ganglienleiste. I. Die Kinematik der Ganglienleistenentwicklung bei den Urodelen. Arch. f. Entwlngsmech. d. Organ. 125:210.

. 1933b. Zur Entwicklung der Ganglienleiste. III. Die Induktionsfahigkeit des Kopfganglienleistenmaterials von Rana fusca.


Stone, L. S. 1922. Experiments on the development of the cranial ganglia and the lateral line sense organs in Amblystoma pimctatum. J. Exper. Zool. 35:421.

. 1926. Further experiments on the

extirpation and transplantation of mesectoderm in Amhlystorna punctatum. J. Exper. Zool. 44:95.

. 1929. Experiments showing the

role of migrating neural crest (mesectoderm) in the formation of head skeleton and loose connective tissue in Rana paliistris. Arch. f. Entwicklngsmech. d. Organ. 118:40.

Tait, J. 1928. Homology, analogy and plasis. Quart. Rev. Biol. Ill: 151.