Book - Developmental Anatomy 1924-2

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Arey LB. Developmental Anatomy. (1924) W.B. Saunders Company, Philadelphia.

Developmental Anatomy: Chapter I. - The Germ Cells and Fertilization | Chapter II. - Cleavage and the Origin of the Germ Layers | Chapter III. - Implantation and Fetal Membranes | Chapter IV. - Age, Body Form and Growth Changes | Chapter V. - The Digestive System | Chapter VI. - The Respiratory System | Chapter VII. - The Mesenteries and Coelom | Chapter VIII. - The Urogenital System | Chapter IX. - The Vascular System | Chapter X. - The Skeletal System | Chapter XI. - The Muscular System | Chapter XII. - The Integumentary System | Chapter XIII. - The Central Nervous System | Chapter XIV. - The Peripheral Nervous System | Chapter XV. - The Sense Organs | Chapter XVI. - The Study of Chick Embryos | Chapter XVII. - The Study of Pig Embryos | Figures
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Chapter II Cleavage and the Origin of the Germ Layers


The fertilized ovum promptly begins to form the new, multicellular individual by a process termed cleavage, or segmentation . This comprises orderly and rapid successions of mitoses which result in an aggregate of smaller cells, called blastomercs. Every blastomere receives the full assortment of chromosomes, half from each parent (Fig. 17 F-J).

The abundance and distribution of yolk in the egg so influences mitosis as to allow the following classification of cleavage:

(A) Total. Entire ovum divides; holoblastic ova.

  1. Equal. In isolecithal ova; blastomeres are of equal size; e.g., amphioxus and mammals.
  2. Unequal. In moderately telolecithal ova; yolk accumulated at vegetal pole retards mitosis, and fewer but larger blastomeres form there; e.g., lower fishes and amphibia.

(B) Partial. Protoplasmic regions alone cleave; meroblastic ova.

  1. Discoidal. In highly telolecithal ova; mitosis restricted to anim^d ]Jole; e.g., higher fishes, reptiles, and birds.
  2. Superficial. In centrolecithal ova; mitosis restricted to the peripheral cytoplasmic investment ; arthropods.

Cleavage in Amphioxus

The early processes of development are easily understood in a primitive, fish-like form, Amphioxus. About one hour after fertilization, its essentially isolecithal ovum divides vertically into two nearly equal blastomeres (Fig. 18, 2). Within the next hour the daughter cells again cleave in the vertical plane, at right angles to the first division, thus forming four cells (3). Fifteen minutes later a third division takes place in a horizontal plane (4). As the yolk is somewhat more abundant at the vegetal poles of the four cells, the mitotic spindles lie nearer the animal pole. Consequently, in the eight-celled stage the upper tier of four cells is slightly smaller than the lower four. By successive cleavages, first in the vertical, then in the horizontal ]3lane, a 16- and 3 2 -celled embryo is formed (5, 6). The upper two tiers are now smaller, and a cavity, the blastocode, is enclosed by the cells. The embryo at this stage is sometimes called a morula because of its resemblance to a mulberry. In subsequent cleavages, as development proceeds, the size of the cells is diminished, while the cavity enlarges (7, 8). The embryo is now a blastnla, nearly spherical in form and about four hours old. The cleavage of the holoblastic Amphioxus ovum is thus total and nearly equal.

Fig. 18. Cleavage in Amphioxus, viewed laterally (Hatschek). X 200. 1. Mature egg, with one polar body (P. 5 .) ; the other missing. 2. Ovum partly divided into two blastomeres. 3. Four blastomeres. 4. Eight blastomeres. 5. Sixteen blastomeres. 6. Thirty-two blastomeres, hemisected to show the blastocoele, B. 7, 8. Total and hemisected blastula.

Cleavage in Lower Fishes and Amphibia

These ova contain enough yolk so that the nucleus and most of the cytoplasm lie nearer the upper, or animal pole. The first cleavage spindle appears eccentrically in this cytoplasm. The first two cleavage planes are vertical and at right angles, and the four resulting cells are equal. The spindles for the third cleavage are located near the animal pole, and the division takes place in a horizontal plane. As a result, the upper four cells are much smaller than the lower four (Fig. ig A). The large, yolk-laden cells divide more slowly than the upper, small cells (B-D). At the blastula stage, the cavity is small, and the cells of the vegetal pole are many times larger than those of the animal pole {E, F). The cleavage is thus total but unequal vertical but the inert yolk does not cleave. The segmentation is thus partial and discoidal. In the bird's ovum, the cytoplasm is divided by successive vertical furrows into a mosaic of cells, which, as it increases in size, forms a cap-like structure upon the surface of the yolk (Fig. 20 A). These cells are separated from the yolk beneath by horizontal cleavage.

Fig. 20. Cleavage of the pigeon - s ovum (redrawn from Blount). A, Blastoderm in surface view; B, in vertical section.

Fig. 19. Cleavage and gastrulation in the frog. X 12. A-D, Cleavage stages; E, blastula; F, hemisection of E; G, early gastrula; u, hemisection of G. an., Animal cells; arch., archenteron; b'c., blastocoele; b - p., blastopore; ect., ectoderm; ent., entoderm; v - g., vegetal cells.

Cleavage in Higher Fishes, Reptiles and Birds

The ova of these vertebrates contain a large amount of yolk. There is very little pure cytoplasm except at the animal pole, and here the nucleus is located (Fig. 6). When segmentation begins, the first plane of separation is furrows, and successive horizontal cleavages give rise to several layers of cells (Fig. 20 B). The space between cells and yolk mass may be compared to the blastula cavity of Amphioxus and the frog (Fig. 22). The cellular cap is termed the germinal disc, or blastoderm. The yolk mass, which forms the floor of the blastula cavity and the greater part of the ovum, may be compared to the large, yolk-laden cells at the vegetal pole of the frog - s blastula. The main yolk mass never divides but is gradually used up in supplying nutriment to the embryo which is developed from the cells of the germinal disc. At the periphery of the blastoderm, new cells form progressively until they enclose the yolk (Fig. 22 C).

Fig. 21. Diagrams of cleavage ami the blastodermic vesicle in the rabbit (Thomson, after van Beneden). X 200.

Cleavage in Mammals

The ovum of all the higher mammals, including man, is isolecithal and nearly microscopic in size. Its cleavage has been studied in several forms, but the rabbit - s ovum will serve as an example. The cleavage is complete and nearly equal (Fig. 21), a cluster of approximately uniform cells being formed within the zona pellucida. This corresponds to the morula stage of Amphioxus. Next, an inner mass of cells is formed that is equivalent to the germinal disc, or blastoderm of the chick embryo. The inner cell mass is overgrown by an outer layer which is termed the trophectoderm, because it later supplies nutriment to the embryo from the uterine wall. Fluid then appears between the outer layer and the inner cell mass, thereby separating the two except at the animal pole. As the fluid increases in amount, a hollow blastodermic vesicle results, its walls composed of the single-layered trophectoderm, except where this is in contact with the inner cell mass. It is usually spherical or ovoid in form, as in the rabbit, and probably such is the form of the human ovum at this stage. In the rabbit, the vesicle is 4.5 mm. long before it becomes embedded in the wall of the uterus; among ungulates, or hoofed animals, the vesicle is greatly elongated and attains a length of several centimeters, as in the pig.

Fig. 22 Diagrams of blastula homologies (Prentiss). A, Amphioxus; B, frog; C, chick; D, mammal.

Comparing the mammalian blastodermic vesicle with the blastula stages of Amphioxus, the frog, and the bird, it will be seen that it is to be homologized with the bird - s blastula, not with that of Amphioxus (Fig. 22). In each case there is an inner cell mass of the germinal disc. The trophectoderm of the mammal represents a ])recocious development of cells, which, in the bird, later enveloji the yolk. The cavity of the vesicle is to be compared, not with the blastula cavity of Amphioxus and the frog, but with the yolk mass pins the cleft-like blastocoele of the bird's ovum. The higher mammalian ovum, although almost devoid of yolk, thus develops a - blastula - resembling that attained by the yolk-laden ova of reptiles and birds. That this similarity has an evolutionary significance is attested by discoidal cleavage in the highly telolecithal eggs of present-day monotreme mammals.

In the low primate Tarsius, cleavage and the blastodermic vesicle are well known. A four-celled Macacus ovum, with blastomeres nearly equal and oval in form, is the only cleavage stage yet observed among higher jirimates. In all placental mammals, segmentation of the ovum occurs during its passage down the uterine tube.

The Formation of Ectoderm and Entoderm (Gastrulation)

The blastula and early blastodermic vesicle show no differentiation into layers. Such differentiation next takes place, giving rise first to the ectoderm and entoderm, and finally to the mesoderm. From these three primary germ layers all tissues and organs of the body are derived.

The processes of gastridation, by which ectoderm and entoderm arise, and of mesoderm formation will be treated separately.

Amphioxus and Amphibia. - The larger cells at the vegetal pole of the Amphioxus blastula fold inward (Fig. 23 A, B). Eventually, these invaginating cells obliterate the blastula cavity and come in contact with the outer layer (Fig. 23 C). The new cavity, thus formed, is the primitive gut, or archenteron, and its narrowed mouth is the blastopore. The outer layer of cells is the ectoderm, the inner, newly formed layer is the entoderm. The entodermal cells are henceforth concerned in the nutrition of the body. The embryo is now termed a gastrula (little stomach).

In amphibia, invagination begins at the junction of animal and vegetal cells (Fig. 19 G). Externally, the blastopore appears as a crescentic groove. Since the vegetal cells are large and the blastocoele is relatively small, simple invagination fails. Hence, archenteron formation is aided by a lip-like overgrowth of rapidly dividing cells from the animal pole (Fig. 19 H).

Fig. 23. Gastrulation in Amphioxus. X 200.

Reptiles and Birds

The germinal disc, or blastoderm, in these animals lies like a cap on the surface of inert yolk (Fig. 6). Since the enormous amount of yolk makes gastrulation as in Amphioxus and amphibians impossible, the process exhibits marked modifications.

There appears caudally on the blastoderm of reptiles a pit-like depression. From this invagination, a proliferation of cells forms a layer which spreads beneath the ectoderm. The inner layer, originating in this manner, is the entoderm, and the region of the pit, where ectoderm and entoderm are continuous, is the blastopore. In Fig. 27 A these changes are complete.

Fig. 24. Gastrulation in the pigeon, as shown by a longitudinal section of the blastoderm (redrawn after Patterson). X 50.

In birds, the caudal portion of the blastoderm is rolled or tucked under, the inner layer formed in this way constituting the entoderm (Fig. 24). The marginal region, where ectoderm and entoderm meet, bounds the blastopore, while the space between entoderm and yolk is the archenteron.


Cells on the under surface of the inner cell mass become arranged in a definite sheet, the entoderm (Fig. 2^ A). It is usually said to arise by splitting, or delamination, although there are attempts to prove ingrowth from a - blastopore. - In most mammals, the entoderm spreads rapidly and lines the blastodermic vesicle (Fig. 38) but in Tarsius, the entoderm forms a much smaller sac (Fig. 25 B, C). The youngest human embryos known (Fig. 40) indicate a previous origin of entoderm much as in Tarsius.

Fig 23. Gastrulation in the low primate, Tarsius, as demonstrated by sections of the blastodermic vesicle (redrawn after Hubrecht). X 260.

Origin of the Mesoderm, Notochord and Neural Tube

Amphioxus and Amphibia

The dorsal portion of the inner sheet, which forms the roof of the archenteron in Amphioxus, gives rise to paired, lateral diverticula, the ccdonuc pouches (Fig. 26). These separate both from a mid-dorsal plate of cells (the future notochord), and from the entoderm of the gut, and become the primary mesoderm. The mesodermal pouches grow ventrad and their cavities form the coelom, or body cavity. Their outer layers, with the ectoderm, constitute the body wall, or somatopleure; their inner layers, with the gut entoderm, form the intestinal wall, or splanchnopleure. In the meantime, a dorsal plate, cut off from the ectoderm, folds into the neural tube (anlage of the nervous system), and the notochordal plate becomes a cord, or cylinder, of cells (axial skeleton) extending the length of the embryo. In this simple fashion the ground plan of the chordate body is attained.

Fig. 26. Origin of the mesoderm in Amphioxus (Hatschek). X 425. a/, Lumen of gut; r//., notochord : ai\, coelom; crrl.p., coelomic pouch; ect., ectoderm; ent., entoderm; n.c., neural canal; n.g., neural groove.

Fig. 27. Longitudinal sections of the snake's blastoderm, at various stages, to show the origin of the notochordal plate (adapted after Hertwig).

In amphibia, solid mesodermal plates arise in a similar location and extend laterally between the ectoderm and entoderm. Later, these plates split into two layers and the cavity so formed is the coelom (cf .3S) The notochord also originates as in Amphioxus.


The same pocket-like depression in the caudal portion of the blastoderm, that gave rise to the cells of the entodermal layer, now invaginates more extensively and forms a pouch which pushes forward between ectoderm and entoderm (Fig. 27 A and B). The size of the invagination cavity varies in different species; in some it is elongate and narrow, lieing confined to the middle line of the blastoderm. The floor of this pouch soon fuses with the underlying entoderm, and the two thin, rupture, and disappear, thus putting the cavity of the pouch temporarily in communication with the space (archenteron) beneath the entoderm (Fig. 27 C). The cells of the roof persist as the notochordal plate, which later liccomes the notochord. The neural folds arise before the mouth of the pouch (blastopore) closes, and, fusing to form the neural tube, incorporate the blastopore into its floor. This temporary communication between the neural tube and the primitive enteric cavity is the neurenteric canal (cf. Fig. 27 C) it is found in all the vertebrate groups (cf. Fig. 58). A transverse section through the invaginated pouch, at the time of rupture of its floor, and through the underlying entoderm will make clear the lateral extent of these changes (Fig. 28).

Fig. 28. Transverse section of a snake's blastoderm, at a level corresponding to the middle of (adapted after Hertwig).

From about the blastopore, and from the walls of the pouch, mesodermal plates arise and extend like wings between the ectoderm and entoderm (Fig. 28). As in amphibia, they later separate into outer (somatic) and inner (splanchnic) layers enclosing the Primitive groove coelom. The relation between notochordal plate, mesoderm, and entoderm, shown in Fig. 28, resembles strikingly the conditions in Amphioxus (Fig. 26 A).


Due to the modified gastrulation in reptiles, birds, and mammals through the influence of yolk, a structure known as the primitive streak becomes important. An account of its formation and significance, based on conditions found in the bird, may be introduced conveniently at this place.

Shortly after the formation of entoderm, an opaque band appears in the median line at the more caudal portion of the blastoderm (Fig. 29).

Fig. 29. BlaStoderm of a chick cmliryo at the stage of the primitive streak. X 20.

Along this primitive streak, which is at first merely a linear ectodermal thickening, there forms a shallow primitive groove, and at its forward end the streak ends in a knob, the primitive knot, or node (of Hensen). The primitive streak becomes highly significant when interpreted in the light of the theory of concrescence, a theory of general application in vertebrate development. It will be remembered that the entoderm of birds arises by a rolling under of the outer layer along the caudal margin of the blastoderm. As the blastoderm expands, it is believed that a middle point on this margin remains fixed (Fig. 30 A) while the edges of the margin on eaeh side are carried caudad and brought together (B, C). Thus, a crescentic margin is transformed into a longitudinal slit. Since this marginal lip originally bounded the blastopore (p. 35), the longitudinal slit must also be an elongated blastopore whose direction has merely been changed. The lips of the slit fuse, forming the primitive streak (D). The teachings of comparative embryology support these conclusions, for the neurenteric canal arises at the cranial end of the primitive streak, the anus at its caudal end, while the primary germ layers fuse in its substance. All these relations exist at the blastopore of the lower animals.

Fig. 30. Diagrams to illustrate the formation of the primitive streak according to the theorjof concrescence. The expanding blastoderm is indicated by dotted circles.

Fig. 31. Median longitudinal section of a chick embryo at the stage of the primitive streak and head process. X 100.

From the thickened ectoderm of the primitive streak a proliferation of cells takes place, and there grows out laterally and caudally between the ectoderm and entoderm a solid plate of mesoderm which soon splits into somatic and splanchnic layers (Fig. 316). An axial growth, the head process, or notochordal plate, likewise extends forward from the primitive knot and fuses at once with the entoderm (Figs. 31 and 317). Since the primitive streak represents a modified blastopore, it is evident that this cranial extension, the head process, corresponds to the pouch-like invagination concerned in the formation of notochord and mesoderm in reptiles. In birds, the fusion of the head process with the entoderm, the relation of mesodermal sheets to it laterally, the formation of the notochord from its tissue and the occasional traces in it of a cavity continuous with the primitive pit (that is, a notochordal canal), all recall the conditions described for the less modified invagination in reptiles. The primitive groove is the visible result of mesoderm proliferation from the tissue of the streak.

Fig. 32. A , Embryonic disc of the Mateer human embryo, at the stage of the primitive streak (after Streeter). X 50. B, Embryonic disc of the Ingalls human embryo, with primitive streak and head process. X 26.


A typical primitive streak appears on the blastoderm of mammals (Fig. 32 A). The under side of its ectodermal thickening proliferates mesodermal cells which grow laterally and caudally (Fig. 33). All three germ layers fuse in the primitive knot and from it a head process soon extends forward (Fig. 32 B).

Fig. 33. Transverse section through the primitive streak of the Mateer human embryo (Fig. 32 ,1 ) to show the origin of mesoderm (redrawn after Streeter). X 185.

The head process of many mammalian embryos contains a cavity {notochordal canal), which in some cases is of considerable size, opening at the primitive pit (Fig. 34). As in reptiles, the floor of this cavity fuses with the entoderm, and the two rupture and disappear. Portions of the floor, still persistent, are shown in Fig. 34. Thus a canal, later enclosed by the neural folds, and then known as the neurenteric canal, puts the dorsal surface of the blastoderm in communication with the enteric cavity beneath the entoderm (Figs. 57 and 58). The roof of the head process, or notochordal plate, is for a time associated closely with the lateral mesoderm (compare these relations in reptiles. Fig. 28), but eventually it becomes the notochord.

Fig. 34. Median sagittal section through the primitive knot and head process of the Ingalls human embryo (Fig. 32 5 ). X 200.

The mesoderm grows rapidly around the wall of the blastodermic vesicle, until Anally the two wings fuse ventrally. The single sheet then splits into two layers, the cavity between being the coelom, or body cavity (Fig. 35). The outer mesodermal layer (somatic), with the ectoderm, forms the somatopleure, or body wall; the inner splanchnic layer, with the entoderm, forms the intestinal wall, or splanchnoplcure. The neural tube having in the meantime arisen from the neural folds of the ectoderm, there is present the ground plan of the vertebrate body, the same in man as in Amphioxus (Fig. 35 A).

Fig. 35. Diagrammatic transverse sections of mammalian embryos. A , The origin and spread of mesoderm (Brjme); B, the further differentiation of mesoderm, and the body plan (Prentiss).

Mesoderm, but not a coelom, is already present in the youngest human embryo yet examined (Fig. 40 A). In Tarsius, a low primate, the mesoderm has two sources: (i) From the splitting of ectoderm at the caudal edge of the blastoderm; this constitutes the extra-embryonic mesoderm and takes no part in forming the body of the embryo. (2) The intra-embryonic mesodertu, which gives rise to body tissues, takes its origin from the primitive streak as in the chick and lower mammals. The origin in the human embryo is probably much the same as in Tarsius.

Homologies of Mesoderm and Notochord

In Amphioxus and amphibia, transverse sections (Fig. 26) apparently show that the mesoderm and notochord are folded directly from dorsal gut-entoderm. Yet such is illusory, for the roof of the archenteron grows from the dorsal lip of the blastopore. Longitudinal sections prove that as the embryo elongates, this caudal, formative region progressively adds to the roof of the primitive gut. Hence, both notochord and mesoderm originate from the indifferent tissue at the blastopore where ectoderm and entoderm meet. In reptiles, birds, and mammals the mesoderm arises as lateral proliferations from the primitive streak, whereas the notochordal plate (head process) is a - growth - from its anterior end (cf. p. 40). But, as the primitive streak is a modified, fused blastopore (p. 39), their origin is fundamentally like that in Amphioxus and amphibia. From its external position and developmental relations the parent blastoporic tissue is often styled ectoderm; especially in embryos with a primitive streak this is convenient and unobjectionable. It will be evident, therefore, that although the ultimate source of both mesoderm and notochord is from an indifferent - ectoderm, - the notochord, once formed, is true mesoderm.

The Notochord or Chorda Dorsalis

As the primitive streak recedes caudad during development, the head process is progressively lengthened at its expense. Ultimately, the primitive streak becomes restricted to the tail region and serves as a growth zone there, whereas the entire remainder of the body is built around the head process as an axis. The original position of the primitive knot corresponds to the junction of head and neck in the future body. In later stages, the rod-like notochord extends from head to tail in the midplane (Fig. 91). It becomes enclosed in the centra of the vertebrae and in the base of the cranium, and eventually degenerates. In Amphioxus, the notochord forms the only axial skeleton, and it is persistent in the vertebrae of fishes and amphibians. In adult man, traces are found as - pulpy nuclei - in the intervertebral discs.


Usually but one human ovum is produced and fertilized at coitus. The simultaneous development of two or more embryos is due commonly to the ripening, expulsion, and subsequent fertilization of an equal number of ova. In such cases ordinary, or fraternal livins, triplets, and so on, of the same or opposite sex result; properly speaking, they are not twins at all. Identical, or duplicate twins, that is, those true twins always of the same sex and strikingly similar in form and feature, arise from two growing points on the embryonic cell mass, each of which develops as a separate embryo within the common chorion. The identical quadruplets of certain armadillos are known to result from the division of a single blastoderm into four parts. Separate development of the cleavage cells can also be produced experimentally in many of the lower animals.

Occasionally twins are conjoined. All degrees of union, from almost complete separation to fusion throughout the entire body-length, are known. If there is considerable disparity in size, the smaller is termed the parasite; in such cases the extent of attachment and dependency grades down to included twin (fetus in fetu) and tumor-like fetal inclusions. In some - monsters - the duplication is partial, as doubling of the head or legs. All of these terata, like identical twins, are the products of a single ovum, but variably fused in accordance with their original degree of separation on the blastodermic mass.

Stockard reduces the primary cause of all non-hereditary abnormal developments, including twins, to a single factor - developmental inhibition or arrest; the exact type of deformity that results depends solely on the precise moment when the interruption occurs. A slowing of the developmental rate at the critical moment (gastrulation) when one of several potential embryonic axes is about to assert its dominance, causes it to lose its original advantage and one or more neighboring points may then appear as additional axes. The direct cause of the arrest is referred to retarded oxidations.

Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)
Developmental Anatomy: Chapter I. - The Germ Cells and Fertilization | Chapter II. - Cleavage and the Origin of the Germ Layers | Chapter III. - Implantation and Fetal Membranes | Chapter IV. - Age, Body Form and Growth Changes | Chapter V. - The Digestive System | Chapter VI. - The Respiratory System | Chapter VII. - The Mesenteries and Coelom | Chapter VIII. - The Urogenital System | Chapter IX. - The Vascular System | Chapter X. - The Skeletal System | Chapter XI. - The Muscular System | Chapter XII. - The Integumentary System | Chapter XIII. - The Central Nervous System | Chapter XIV. - The Peripheral Nervous System | Chapter XV. - The Sense Organs | Chapter XVI. - The Study of Chick Embryos | Chapter XVII. - The Study of Pig Embryos | Figures


Arey LB. Developmental Anatomy. (1924) W.B. Saunders Company, Philadelphia.

Cite this page: Hill, M.A. (2019, January 19) Embryology Book - Developmental Anatomy 1924-2. Retrieved from

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