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Hamilton WJ. Boyd JD. and Mossman HW. Human Embryology. (1945) Cambridge: Heffers.

   Human Embryology (1945): 1 Introductory Concepts | 2 Formation Maturation and Structure of Germ Cells | 3 Cyclic Changes in Female Genital Tract | 4 Fertilization Cleavage and Formation of Germ Layers | 5 Implantation of Blastocyst and Development of Foetal Membranes Placenta and Decidua | 6 Fate of Germ Lavers and Formation of Essential (Primary) Tissues including Blood | 7 Growth of Embryo Development of External Form Estimation of Embryonic and Foetal Age | 8 Determination Differentiation Organizer Mechanism Abnormal Development and Twinning | 9 Cardio Vascular System | 10 Alimentary and Respiratorv Systems Pleural and Peritoneal Cavities | 11 Urogenital System | 12 Nervous System | 13 Skeletal System | 14 Muscle and Fascia | 15 Integumentary System | 16 Comparative Vertebrate Development | Figures
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Chapter Xvi Comparative Vertebrate Development

Considered objectively and samt^au the embryology of man has no more interest than that of any other mammal or lerttbrale and from this standpoint special endeavours to noth out human embryology by itself may to be misplaced — Keibel {iQio )


The study of human dcNcIopment has been greatly influenced by the knosvlcdt^e obtained as the result of imestigations on other vertebrate types This has been in part due to the greater ease with which closely sta ed embryos of kno^n age can be obtained m animals and to tlic absence of limitation of expenmcnl Further, in order to explain certain peculiar structural and functional phenomena occurring tn human development a knowledge of comparauve embryology is imperative Thus the presence of the notochord, the visceral arches, the sequence of kidnevs, the functional differentiation of the nervous system and the foetal metabolism can best be understood on the assumption that they arc at least in part features inherited from ancestral stages in the development of the human race Since many ancestral organs seem to have disappeared entirely, it may be assumed that during the course of evolution features have persisted when they are functionally necessary during development as for example the mammalian mesonephiw or when they provide a scaffolding for some essential structure of the later embrvo or adult, as for example, Meckel s cartilage

Fifty years ago most competent zoologists vvere satisfied to explain embryonic development mainly in the terms of the so called Law of Reeapitulalton or Law of Biogenesu This law stated that embryonic development repeats m order the adult stages through which the race has passed during its evolution This is often expressed by the statement Ontogeny repeats phylogenv While there is nothing in the known facts of embryology evolution or genetics to show that ancestral adult features arc handed down by heredity to the embryos of more advanced forms yet there arc a multitude of characters appearing temporarily during the development of an individual that arc known to be primitive and can be explained only in the light of the evolutionaiy past of the speaes Most modem embryologists therefore, would restate the Law of Recapitulation in the highly modified form that Ontogeny repeats funda mental steps in the ontogenies of ancestral forms especially when these steps are of structural or functional importance to the indindual (de Beer 1940)

Although the original law especially as expressed by Haeckel (1874), has been replaced by a more tenable modem version the general idea of recapitulation has been of the utmost importance m the stimulation and imerpretation of investigations in the field of comparative embryology For one fact which does not seem tofit in with the modern thcorvof recapitulation a thousand can be cited which arc meaningless without it No matter how inadequate the modern theory may be regarded as an explanation of the reason for the developmental course taken by a species the general pnncjple wiH always be found of value in embryological study With few exceptions, the younger the stage of development of an embryo of a particular species the lower is the animal group which it resembles both morphologically and physiologically The value of this pnnaple for (he correlauon of facts is far greater for the student than the question of its worth as a philosophical explanation of ontogenies

It must be staled that the authors are under no illusion that the subject of comparauve vertebrate development can be adequately presented in a book of this character However some of the more fundamental facts especially those relating to early stages of development will be given. It is hoped that the brief presentation of these facts will help to make more clear and meaningful many otherwise uncorrelated phenomena of human development, and that they will at the same time stimulate interest in the general field of embryology,

The Germ Cells

There are significant differences in the morphology and physiology of the germ cells of various vertebrate species just as there are differences between adults of the species. But as the germ cells are relatively simple structural and functional units compared with adults, the apparent differences are neither as numerous nor as extensive. Both male and female germ cells are nevertheless highly specialized and their structure is adapted to, or determined by, the functions they perform The sperm cells are more likely to possess visible distinctive characters than are the ova , but most of these sperm peculiarities are of no known significance It IS generally believed that their morphological traits are chiefly adaptations to the particular problems which they must solve in reaching and penetrating the ova. In order to accomplish this function the amount of cytoplasm in a sperm is reduced to a minimum, a flagellum is oes^loped tvhich renders it highly motile and the sperm head frequently possesses a special mechanism for the perforation of the ovum and its membranes. After fertilization, sperm morphology does not appear to be concerned with the further development of the embryo, although the genetic structure of the male gametes is of fundamental importance.

Ova, on the other hand, are always distinctly larger cells than the normal somatic cells of the organism from which they are derived. Further their increased cytoplasmic mass is frequently enormously enlarged by the accumulation of yolk oi deutoplasm (Fig. 410). They frequently possess protective envelopes, or egg membranes, and owing to the absence of motile organs they can only be moved passively. The size of ripe vertebrate ova, excluding their membranes, range from a diameter of about loop. in Amphtoxus and eutherian mammals (range 80-150/i) to about 85 mm. m the ostrich. The structure of an ovum, especially the degree to which nutrient material is included in its cytoplasm, has a marked effect on early development. Yolk-rich (megaleathal — mega = muc , lecithal = yolk) eggs support embryonic development of a vegetative sort to a relatively late stage; yolk-poor (mwlecithal ^m(e)io — less) eggs can do this only for a very short time, after which the embryo must acquire means 0 obtaining its nourishment from outside itself be that from sea water, soil, the tissue of a ost or the mammalian uterine mucous membrane.

The primitive Metazoan reproductive method appears to have been one in which a large number of miolecithal eggs ivere produced and widely dispersed. With little stored materia an early larval, or free-living embryonic stage, was necessary. In vertebrate evolution t tendency was to increase egg size and reduce the number of eggs laid. This tendency was associated ^v'lth the prolongation of the developmental period as in reptiles and birds w ere a larval stage is suppressed. In the mammalian class the evolution of specialized viviparo mechanisms has resulted in egg size being secondarily reduced, only slightly in Monotrem but markedly in Euthena. . r

Ov'a can be classified, therefore, on the basis of the relative amounts and distnbution 0 yolk and cytoplasm within them Table IV is designed to present this classification and correlate vertebrate ovum types with cleavage types Like all classifications this is for co • venience, and there are intermediate ova and cleavage types which do not quite con 0 to any compartment in the scheme. The most complete intergradation is miolecithal and medialecithal types. A fairly well marked gap exists between the medialcc and megalecithal eggs, but even here a few transitional types are kno^cn (eggs o P Lepidosteidae ) .

Fig. 410 — Schematic section of mature amphibian egg co\ii’\u\ii\r \iRrniRMi diviiopmivi

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As has been described on paijc fa deisn^c i* the process wJjerebt the protoplasmic rnass of the fertilized efc,t, is pirlitioncd (either completel) or mcomplctel> ) into cells of il)out the size normal for the particular species Ostini, to the hrge size it is Iikcl> tint the unfertilized egg IS in an ibnonmJ metabolic state As clctsage progresses tlic diminution m cell size ol the successisc generations ofbhstomcrcs establishes gncluallj normal metabolic conditions ^ncomitant with tlic diminution in cell size greater mobilit) is conferred on the mdisidual hlastomeres thus facihnting liter morphogenetic mosements (see gastnihtion page 383) and in those eggs with gross accumulation of deutoplasm this material is gradually extruded from the effective protoplasmic mass.

Cleavage may be classified either in relation to the fate of the resulting blastomeres in subsequent development or, descriptively, in accord with the actual pattern of the cellular divisions Utilizing the former method cleavage is either determinate or indeterminate. Ova ■with determinate cleavage are those (mosaic eggs) in which the organ-forming regions are already predelineated m the fertilized egg. Indeterminate ova, which are usual in vertebrates, are those in ^vhlch there is no obvious mosaic structure at the time of fertilization and it is only after a certain, and generally quite late, stage of cleavage that presumptive organ regions are established. Up to this stage the blastomeres are pluripotent and are not yet “determined” (see page 121) so that, unlike the blastomeres in determinate cleavage, their prospective potency IS not necessarily identical with their actual developmental fate This implies that such blastomeres possess certain powers of adaptation to changes in their cellular environment, and consequently, eggs showing this type of cleavage are often called regulative eggs.

purely descriptive classification of cleavage is 1 elated to ^ actual pattern of the cell divisions. This pattern is largely

Ll .5 y dependent on the amount and distribution of the stored

JrC deutoplasm and thus the type of cleavage is related to the initial

size of the egg and varies according to ^vhether the eggs are niiolecithal, medialecithal or megalecithal (Table IV).


^ ^ In these eggs the first cleavage spindle forms near the centre of the egg so that two equal-sized blastomeres are formed (complete (holoblastic) and equal cleavage). These blastomeres in turn divide equally and successive equivalent divisions of the daughter cells result in the formation of a morula made up many cells of nearly equal size and containing neaily equa ( ^ amounts of yolk and cytoplasm. In practically all these

Vsi ’■‘tl miolecithal eggs, however, there is a slight difference in blasto mere size and quality after the third cleavage. In Amphioxus after this third (equatorial) cleavage the four cells at the so-ca e

“animal” pole are slightly smaller than the four at the

n pole. Subsequent divisions emphasize this difference so t at t e „ , morula (Fig. 411) possesses an “animal” pole with smaller ce s

tion of mature'"^cgg **^0? ^ “vegetal pole” "wnth larger cells. Even P f

Amphtoxus B Early blastula mammals some difference m blastomere size is usually detecta

early in cleavage (Figs 28 and 412)

Cleavage In Medialecithal Eggs

In these eggs with a moderate amount of yolk the first two cleavages ordinarily ^ our equa astomeres, but the third cuts off animal pole cells which are much sma er ose e t at the vegetal pole (complete and unequal cleavage) Moreover, the sma con am itt e yolk, while the vegetal cells are loaded with it. This inert nutritive ma 'eeps ^ e metabolic rate of these vegetal pole cells relatively lower than that of the anima p’oup, e ^tter, therefore, divide much more rapidly and so assume the „igte

formation of the embryo The most familiar examples of medialecithal ova with complete u unequa c eavage are amphibian eggs, especially those of frogs and toads (Fig- 4 U

tb ^ megalecithal eggs of reptiles, birds and the egg-laying mammals {Monotremata) ^^P the greatest development of yolk storage. Sharks and Lyt {Euselaehn) have almost as mu

I'lG 411 — A Schematic section of mature egg of Amphtoxus B Early blastula of Amphtoxus

^olW, while the bon> fishes {T<Uostei) have notice ^

abh less but still enoutjh to limit cleavage to the | ,

mcomplece type In megalccithal eggs the active ( ^

egg cytoplasm with Us nucleus is a relatively ’

minute mass at the animal pole of the heavily ‘ F )\ 1

yolked egg Cleavage is at first equal but only f ^

involves the active cytoplasmic region The yolk j f \ '1

mass does not divide but is graduallv used as ^ I 1 I*

pabulum for the embryo and the extra embryonic ‘ ^ i ‘

membranes derived from the cells of the animal , j^r * jj ^

pole This incomplete partial or discotdal type of j

cleavage (meroblastic) results m a disc shaped \ ' j

morula and blastula instead of the essentialK v •* /

spherical structures seen in all the previously n.

mentioned types (cf Figs 415 417 and 419) ^ ^ TT % ^

In the phylum Chordata the miolecithal ^ ^ ^ ^

medialecithal and megalccithal types are all

found although the latter two are the more Fic 412 —A living morula of sheep killed five ° _ , , , , ^ ... days after mating x 380 (Reproduced

common The (^ephalochordata possess miolccitnal from Physiology of Reproduction by per

eggs with nearly equal complete cleavage In the mission of Messrs Longmans Green & Co

C}closlemala the pelr<}iin.,onU have medialecithal ova vvith unequal complete cleavage while the

mytinoids have megalecithal eggs wath incomplete cleavage Among the fishes the sharks and rays {Eusilachi) have megalecithal eggs unth incomplete cleavage The Poljplertdae the CkondrosUt the holostean Imia (i e , the group formerly called the ganoids) the Dipnoi (lung fishes) and the Holoeepkali have medialecithal eggs with unequal compleic cleavage The eggs of the holostean Lepidosteus (also a ganoid form) are transitional m type having so much yolk that cleavage is never complete yet m general pattern 1$ more like the unequal complete type than the discoid The true bony fishes (formerly grouped together as TtUostei) have relativclv small megalecithal eggs with defimtelv discoid cleavage Amphibia are characterized by

Frc 413— Section of an early blastocyst of the golden ham ster Cruttus au alus The outer cells are developing to form the trophoblast which is more darkly jtained than the cen trally placed cells x 640

(Reproduced from Physiology of Reproduction bv per

mission of NIessrs Longmans Green &, Co Ltd )

medialecithal eggs and complete but unequal cleavage Here the Apoda (Gjmnophionia) arc exceptions having so much yolk that their eggs should be classed as megalecithal with incom pletc cleavage AU reptiles and birds have large megalccithal eggs with incomplete cleavage All marsupials (Mctalhena) and placental mammals (Euthcria) have miolecithal eggs with complete and almost equal cleavage The reJalive ahscnce of yolk in both Metathena and Euthena is considered by some to represent a revcoal m evolution from the ^gs of ancestral oviparous reptile like mammals which undoubtedly possessed megalccithal ova The eggs of marsupials contain rather more yolk than do those of placental mammals, and yolk bearing fragments are commonly eliminated during cleavage {deutoplasmolysu) This phenomenon may represent a stage in adapution to viviparity The rare egg laying mammals (Monotremata or Protothena) have megalecithal ova with discoid cleavage (Caldwell, 1884 Flymn and Hill 1939 1947) There is now an extensive literature concerning the mechanism of cleavage the rates of cleavage in different animal groups and the effects of cbcimca! substances, especivlly mitotic poisons on cleavage This has been summarized by Boyd and Hamilton (19^2)

Fig 414 A Section of sheep blastocyst 10 days post insemination The endoderm can be seen lining the upper half of the blastocyst cavity X 230

B Section through inner cell mass region of another sheep blastocyst at the 10th day The inner cell mass is becoming intercalated into the trophoblast x 230.

C Section of embryonic disc of a sheep blastoc%st 12 days post insemination The embryonic formative ectoderm is now bulging above the lc\el of the adjacent trophoblast x 280

(Reproduced from “Physiology of Reproducnon,” by permission of Messrs Longmans Green & Co , Ltd )

In miolecithal eggs the blaslula is the hollow sphere of cells which results from the process of cleavage. The cavity of the blastula {blastocode) IS enclosed by cells which are slightly smaller m the animal than in the vegetal hemisphere (Fig. 41 7A), In medialecithal eggs the blastocoele is relatively small and, since the animal pole cells are definitely smaller than those in the vegetal portion of the sphere, the blastocoele cavity is much nearei the animal pole (Fig. 417®)* no longer speak of animal and vegetal hemispheres, but rather of an animal portion (usually about one-third) and a much larger vegetal portion. In megalecithal eggs the blastula is merely' a thin flattened disc of cells resting on the yolk mass, but separated from the yolk, except at its margin, by a shallmv cleft-like blastocoele (Fig. 419).

Although the mammalian egg is relatively yolk-poor and cleavage is at first complete and nearly equal, the late morula and blastula are distinctly different from those of lower vertebrates with miolecithal ova (e.g., Amphioxus). In the mammalian moiula an outei layer of small, slightly flattened cells can be distinguished from the larger polyhedral ce s of the inner cell mass This outer layer is t e trophoblast or trophoblastic ectoderm (

33i 34i 35i 56 and 4i3)- The blastula caw^^^ appears between the trophoblast and t cell mass and separates them side where they remain m contact. This yp of blastula, which is peculiar to the eutberia mammals, is probably not quite compara e the blastulae of lower forms, and part y or reason it has long been called a '^1^ *„ei The eggs of marsupials are slightly la g and more yolk-laden than those o p «  mammals and they diffeientiate more ra so that blastocyst formation is not qui same. Hill (1918), Hartman (1920), (1934) and McCrady 'SjS an ,,,

shown that in several of these ( Dasyurus, Macropus and Perameles) true morula, for, after the second blastomeres arrange themselves 1 layer around the inner surace „ ^12) pellucida, forming a hollow sphe ( g- j Lh eliminated yolk-fra^ents m the cc" cavity. This is a typical blastula and blaslocjst for ihrro ,s no inner cell mas Certain largercells at the animal |»le (formatne area) m,™ie innards to form the endodem. (n)-nn and Hill 19(0) In the insectirores HmictnleUs stmtspinosus (Goetz, 1938) and Btphanlulus Jamesonu (van der Horst 1942)

a smeic lavered blastula ( mammalian blastula ) is formed without an intervening morula stage and at first without an inner cell mass \toncpolc however, a thickening resembling an inner cell mass, soon appears This is perhaps caused b> dehmination of an

inner cell mass in the true sense It is conceivable therefore that the **

marsupials and certain inscciivorcs show some of the transitional steps leading up to the typical mammalian blastocyst / ra-V

There is considerable variation in the relation of the trophoblast "f> to the mner cell mass ( formative cells ) in the stages immcdiatclv following the formation of the blastocyst m the different cuthenan groups In some e g , pnmates (probably including man) bats and a .

most rodents the trophoblast at first complcieK covets the tnner cell <

mass (Figs 56 58 and 428) In others like the pn, and probablv most of the ruminants and carnivores, the trophoblastic cells (Raubtr s laitr) covering the inner cell mass soon disappear exposing on the surface the cmbrvonic ectodermal portion of the inner cell mass This remains exposed until the amniotic folds form at a later stage


The Metazoan embryo at the end of cleavage (1 c in the blasiula B stage) undergoes a rapid change m shape due to a complex rearrange ment of the constituent cells This arrangement results in the establishment of the germ layers and is essentially a process enabling presumptive organs to reach (iieir correct position (RabI 1915 \ ogt 1929 Lehmann 1945) It is called ^af/ri/fa/ion The nature extent ^ and chronology of the gasiruiation movements IS different m different J species but thev always precede by a little the appearance of the 5 us ii

primordial organs In the mammals the process is delayed and when It occurs IS restricted to the formative cells of the inner cell mass The simplest form of gastrula is an embryo with only tvvo germ layers ^ an outer xhe ectoderm and an inner the rniAx/rm (Pig 415) The term gastrulation is often defined as the process by which the single lavered ^

blastula IS converted into a two-layered gastrula Tins is an adequate ' TT S

definition for a stage m many invertebrate types eg the miolecithal eggs of CoelenUrata and Cchnodermata as it desenbes a liurlv definite r'

period m development for these eggs owing to their complete and ::

nearly equal cleavage produce blastulac which are hollow spheres ^

with the cells of the vegetal hemisphere only slightly larger and more yolk laden than those of the animal hemisphere Xmphioxus possesses a q "■Xr?— t_i-J^ similar blastula (Fig 415)

4'5 — Semi schemaiic drawings lo sho» gasiruiation and chorda mesoderm lormation in Imphtorus (Based partly on Conklin 1933 ) Ectoderm and neural tube in section in blue Endoderm in yellow Chorda mesoderm and oelinitvc chorda in reverse red sCipple Unsectioned mesodermal cells are shown with red stipple

' Late blastula stage (longitudinal seclionl B Earl) gastrula stage (longitudinal section)

^ Late gastrula stage (longitudinal s ction;

U Early mesodermal diverticula stage (transverse section)

h Definitive coclomic pouch stage (transverse section)

the arrow in A represents the future amcro posterior ams of the embrvo

In order to understand the morphogenetic movements occurring at gastrulation it is necessary to know the position of the presumptive organ-forming areas in the late blastula stage. Maps (Fig. 418) showing these areas have been provided for amphibian eggs by a number of investigators who have applied coloured marks to portions of such eggs and followed the fate of the stained regions in subsequent development (Vogt, 1925 and 1929)

Gastrulation in Miolecithal Eggs

The blastulae derived from miolecithal eggs gastrulate by invagination of the vegetal hemisphere into the animal hemisphere, thus obliterating the blastocoele and forming a new

Fig 416 — Schemes to shotv the relation of the amnion and chorion to the somatopleure

A — Cross section of a typical vertebrate embryo in the region of the fore or the (q

B — Cross section of a typical mediolecithal vertebrate embryo in the region of the yo m show the potential “yolk sac ” gj

C Cross section of a typical anamniote vertebrate embryo of the megalecithal group, of a teleost, to show the trilaminar yolk sac. tvpic^^

D, E and F — Cross sections of successive stages in the development of the nsing

ammote vertebrate such as a reptile In these three schemes the amniotic folds are s from the extra-embryonic somatopleure

ted cavity, the gastrocoele (also called the archenteron or primitive gut), lined by the ^ q’jje cells which constitute the primary endoderm. The outer layer of cells is now the ^ blastopof^ circular opening, where the latter is continuous with the mvaginated endoderm, is tn In the Coelenterata the gastrula develops into the adult without any fundament in its morphology Even in the Echinodermata and Amphioxus the embryo retains i gastrula form for an appreciable time, becoming motile and feeding during ^ .jefly at was formerly held that these simple gastrulae grow in length by cell multiplication the nm of the blastopore. This rim was regarded as an undifferentiated area, an cells believed to arise there were considered to become ectoderm if they happenea

cMcrmI to the nm or cnclodcrm if just intcmil to it More recent work howescr ind especiall> the results of mappint, has shown tint the cells of the bhstuh ln\e a prospectisc su’nific'ince licforc Ristnihtion I he chaOsCs it the hlxstoporic hp therefore in%ol\c extensive migratory movements nlhcr than simple proliferation Indeed in \wphtovus a.s subsequent development showa (Conklin 1932) the invat,inated inatcria! includes more than the primary endoderm (I ig 415) as it also gives to the third germ lajer (tlie mesoderm and notochord) In all vertebrates inv agination of the primary endoderm precedes bv onlv a bncf penod the invagination of mesoderm and notochord m fact the three processes occur more or less concurrently In verte brales then there is no clear distinction between the period or the process of formation of cnthxlcrm mesotlcrm and notochord there fore It IS liecoming common practice for vertebrate embryologists to include as gastrulation not onlv the process of endoderm formation but also that of the early formation of mesoderm and notochord for the sake of continuity the origin of the somites coelom and neural plate will lie discussed here although these processes arc not even in a general seme a part of gastrulalion

Careful study of the growing gastnila of Impktotus reveals that the invaginated vegetal hemisphere cells form onlv that endoderm which lines the floor and approximately the lower lsvo.tJurds of the lateral sides of the elongating gasirocoelc or primitive gut 1 his primarv endoderm is augmented by secondaty endoderm or thorda mtsodem consisting of small yolk free cells (Pig 4J5) which migrate in through and proliferate from the region of the blastopore ami form the roof and upper tliird of the sides of the primitive gut This chorda mesoderm is not considered to contribute much to the definitive gut It is really a stage m tlic denvalion of the mesoderm and notochord from the cctodenn In this process the chorda rneso* derm along the midline of the roof of the gastrocoeic cvaginalcs dorsal ward forming a ridge wliicli soon separates from the gut l>eginning at the cephalic end and forms a solid rod of tissue the notoihord At the same time lateral diverticula (the mesodemie or totlomic pouches) ansc in consecutive pairs from the lateral part of the chorda mesoderm on either side of the notochord cv agination The first pair

appear at the anterior (head) end and the succeeding ones, m sequence back towards the blastopore I he pouches enlarge, separating the ectoderm from tlic primitive gut and finally sever their own connection with the gut cavity and endoderm Thus a senes of isolated paired mesodermal sacs enclosing paired cocinmic cavities arc formed throughout the length of the embryo (Pig 4i5r) Phev expand ventrally and dorsally separating the cndodcrmal gut completely from the ectoderm Along the mid sagittal plane where the adjacent portions of right and left mesodermal pouches come into contact

ventral and dorsal to the gut they form the temporary ventral and permanent dorsal mesentery Tig 416) The lateral portion of the

Fio 417 — Semi schemaiic drawings to show Kastnilation and chorda mesoderm formation in Amphibia The same conventions are adopted as m I ig 415 \ Cleavage stage B Section of cleavage stage C Tarly gastrula stage (longitudinal section)

D Intermediate gastrula stage (longiludinal section)

E Late gastrula stage (longitudinal section)



mesoderm of each pouch comes into contact with the ectoderm and becomes mainly translormed into a segment of the body musculature, the medial portion, m contact with the endoderm, forms the smooth muscle and connective tissue of the alimentary tract and mesenteries Probably relatively little of the chorda-mesoderm remains after formation of the notochord and mesoderm.

any which persists is found as a median strip m the roof of the definitive gut cavity. The processes just described constitute the fundamental steps in the segregation and differentiation of ectoderm, endoderm, mesoderm and notochord.


Gastrulation in the medialecithal ova of the lampreys {Petromyzontidae), certain of the “ganoid” fishes (Polyptendae, Chondrosiei, Atniidae) and the Amphibia is typified by that of the frog although, of course, there are variations in detail. In the frog


Fig 418 — Scmi-schematic drawing to show primiU\c streak stages

.\ Late gastrula

stage through pnmiUve

streak (trans\ ersc sec tion)

B Farlj ncurula

(trans\ersc section)

C Formation of neural folds (surface vnew) D. Prcsumptite regions on the surface of the hlastula

(Fig. 417) the relatively great size and slow cleavage rate of the yolkladen blastomeres in the vegetal two-thirds of the blastula is the chief cause of differences in its gastrulation from that of such forms as Amphioxus. As the large cells form too bulky a mass to be mvagmated within the fewer and smaller cells of the animal pole, gastrulation is effected by the proliferation and spreading of the smaller animal pole cells downwards and over those of the vegetal pole while, at the same time, the animal pole cells of the advancing margin are progressively mvagmated so that a new cavity (the gastrocoele) which communicates with the exterior is formed, and the original segmentation cavity is obhteiated The gastrocoele is partially lined by animal pole cells (chorda-mesoderm or secondary endoderm) in addition to the heavily yolked cells of the original vegetal pole (primary endoderm) The former will give origin to the mesoderm and notochord. Those animal pole cells which are never mvagmated (1 e , those furthest from the area of invagination) will in later stages form the definitive ectoderm and neural plate The process of spreading, or overgrowth, by the smaller animal pole cells, is called epiboly It commences at the margin of the animal hemisphere and from the first shows a bilateral symmetry, the- overgrowth is more rapid at the future cephalic margin [dorsal lip) of the blastopore and slower at the future caudal margin [ventral lip) , the marginal regions joining the dorsal and ventral lips are the lateral lips and they show a dorso-ventral gradient in the degree of overgrowth. The entire margin of overgrowth is the blastopore As epiboly nears completion the blastopore becomes a small circular opening plugged with buried endoderm cells. This is known as the yolk plug and is of little significance except as a characteristic condition at one period in the gastrulation of most medialecithal eggs of vertebrates The original yolk-laden cells of the vegetal two-thirds of the blastula now form a mass within the ectodermal shell and beneath the sht-hke gastrocoele which lies between the mvagmated chorda-mesoderm and the primary endoderm The chorda-mesoderm is continuous with this primary endoderm cranially, and temporarily forms the roof and upper lateral portions of the gastrocoele or primitive gut cavity With continued development the periphery of the mvagmated chorda-mesoderm extends ventrally on the lateral side of the primary endoderm At the same time the upper edges of t e latter extend medially and eventually fuse in the mid-hne an



undemcith the axial portion of the chorda mesoderm This axial portion is the notochordal plate and as it is separated from the roof of the I'astrocoelc it becomes the notochord The fused edges of the primary endoderm underlnni, the notochord form the permanent roof of the enteron or gut Lnlike Im/Aiono mesodermal pouches are not formed b> csagination from the chorda mesoderm The mesodermal sheet mcrcl> extends \entrall} between the endoderm and the o\crl\ing ectoderm Mesoderm formation begins in the late >olk plug stage as the blastopore is constricting to form a \erucal dumb bell shaped slit The lower end of this slit remains open as the definitive anus the upper end persists tcmporanl) as a duct xhc neurenltrie eanat leading from the caudal end of the ectodermal neural groove into the gut just caudal to the point where the secondarv endoderm and notocliordal plate are still con iinuous Between these two openings tlic lateral lips of the blastopore fuse and from this fusion line or e streak the mesodermal sliect

continues to be proliferated from the ectoderm and extends laterally and anteriorly on each side of the notochord As each sheet grows laterally it separates the ectoderm from the cndoticrm until finally as in Imp/uoxus the sheets meet ventral to the gut (Fig ji8\andB)

The further differentiation of the mesodermal somites lateral plate mesoderm and coelom is typical of that of most vertebrates

GASTRULATION IN MEGALECtTIlAL EGGS Fishes The process of gasinilation in vertebrate mcgalecithal eggs vanes with the amount of yolk relative to the cytoplasm In the Teleostet (bony fishes) the cytoplasmic area is relatively large compared w ilh that of sauropstdan (reptiles and birds) eggs After early cleav age in the telcosts the blastoderm usually covers about one fifth of the surface of the egg \t the margins of the blastodtse the deeper cells separate (by delamination) from the outer thus forming a circular zone of primary or yolk endoderm \t about the same lime liouever a definite inturning (invagination) of the surface cells begins at the caudal margin of the disc to form a layer of secondary endoderm (chorda mesoderm) corresponding to that of Amphtoxur and the \mphibia This spreads rapidlv over the upper surface of the yolk separating it from the overly ing ectoderm and fusing on all sides with the marginal yolk endoderm As this overgrowth continues its rim passes the equator of the egg and constricts on the caudal side of the vegetal pole to form a somewhat circular opening which is readily recognized as the blastopore \Nhen this process is ncarlv complclcd the two layered blastoderm grows downwards and envelops the yolk mass to form the bilaminar yolk sac which is part of the primitive gut and characteristic of all mcgalecithal vcrlcbrales Tlie invagination

Flo 419 — Srmi schematic dras mgs in shos gasinilation and chorda mesoderm formation in the asian egg

\ Germinal d sc \ ith w o polar bodies B Lateral surface lies of early biaslixlisc C Longitudinal section through early I lastodisc

D Longitu I nal section through later blastodi c (The arrows in the inset show the direction of migration of the mesoderm )

E Farlv gastrula stage {longitudinal section^

F I resumptiie regions in the surface of Ihe blastoderm (superior view)

G Presumptiie regions in the surface of the blasiodeim (lateral vies )

H Transverse section through late gastrula stage in region of notochordal plate

I Transverse section at level of primitive streak



at the blastopore is much more marked, and the primitive streak persists for a longer time than in the frog. The process of primitive streak formation is still active and the blastopore is still open even after the formation of the head fold and many somites. The notochord and mesodeim arise much as in the frog, the former by invagination of the chorda-mesoderm through the doisal hp of the blastopore (primitive node) and the latter by invagination of surface cells thiough the primitive streak (fused lateral lips of the blastopore).

Reptilia. Owing to the still greater proportion of yolk m the reptilian egg, gastrulation IS even less like that of the frog than is that of the Teleostei The blastodisc is a relatively small aiea on the huge yolk mass, and the segmentation cavity is insignificant. Under the entire blastoderm yolk endoderm cells separate from the surface cells (ectoderm) and orgamze to form a complete sheet of primary endoderm. The two-layered disc now begins to overgrow the yolk, as in the fishes, and at the same time a small depression forms on its surface near the ( audal margin. This is an area of invagination, the dorsal hp of the blastopore. There is a convergence of surface cells towards this area and a short primitive streak or “plate” is formed, ■d though apparently no such movement of the actual edge of the bilaminar disc occurs, as ,n the fishes From this the notochord and mesoderm arise as in the Fishes and Amphibia.

Peter (1935), however, considers that in the chameleon and lizard most of the notochord and gut endoderm is formed from the delaminated yolk endoderm, only the caudal portions of each arising from the invaginated chorda-mesoderm (see also Pasteels, 1937 and 1940).

Aves. Cleavage and blastoderm formation in birds are almost identical with these processes in reptiles. There is a blastula stage in which the cleavage cells form a blastoderm three or four cells thick, separated by a shallow “segmentation” or “subgerminal” cavity from the centrally placed yolk and continuous with it at the periphery. The central, unattached region is the area pellucida, the attached margin, the area opaca. Around the margin, yolk endoderm delaminates from the overlying ectoderm as m reptiles. According to the usual description, based largely on Patterson’s (1909) investigation of the pigeon, the caudal margin of the blastoderm invaginates to form secondary endoderm much as in the bony fishes. Convergence of the blastoporic lips gives rise to a distinct primitive streak, and it is during the initiation of this process that the blastopore is closed (Fig 419). Jacobson (1938) believes that much of the foregoing description of gastrulation m birds requires modification He states that there is practically no segmentation cavity and that there is a very brief period when the area pellucida of the blastula is made up of a single cell layer He considers that there is no invagination of the caudal edge of the blastoderm to form a temporary blastopore Instead, there IS an o\'al area of the caudal region of the area pellucida, not involving the margin of the disc, from which individual cells migrate beneath the blastoderm, proliferate, and organize to form a sheet of secondary endoderm which soon spreads out like that of the reptiles and bony fishes to fuse with the marginal yolk endoderm This area is the primitive blastoporal plate and coriesponds to the dorsal lip of the blastopore, although there is no invagination. There follows a movement of surface cells toivards the plate, and the area caudal to it, which is comparable to convergence in the t^qies previously described. These cells form a definite primitive streak from the lower surface of which, for a short time, endoderm continues to be budded Soon, however, all the cells proliferated laterally from the streak he between the ectoderm and endoderm and are, therefore, mesoderm (Fig. 420). From the cephalic end of the streak the notochord arises m the usual manner, being first included, as a notochordal plate, in the roof of the primitive gut, and later separating from it to assume its typical position between the gut and the central

Fro 420 — Schematic representation of the surface view of the developing blastoderm in the chick embrj’o The area vasculosa IS represented in red dots.



nen'ous system (Fig 42 1) More recently Pasleels (1945) Has rein\ estigated the origin of the avaan endoderm In the duck he found the primary cndoderm to arise as the result of the progressive delamination of the dealing blastodisc into a superficial and a deep layer between which a cleft appears He homologizes this cleft with the blastococle and considers that the sub germinal cavity IS not a blastococle being infact only theresuk of theprogressiveliquefaction of the yolk acted upon by enzymes produced by the yolk syncytium and perhaps the blastoderm itself


Up to the present it has not been possible to make an adequate experimental analysis of the process of gastrulation m the mammals The precocious segregation of tissue regarded as ectodermal to form the trophoblast limits the formation of the endoderm and the intra embryome mesoderm to a restncied group of cells in the typical euthenan blastocyst Earlier investigators (e g Keihel 1889 and Hubrecht, 1890) thought that mammalian gastrulation occurred m two stages The first of these is the formation of primary endoderm by delamma lion of cells from the inner cell mass or ils equivalent and the second the imagination of embry oruc disc cells to form secondary endoderm mesoderm and notochord Most modern investigators necessarily basing tbeir conclusions on morphological findings regard both the processes as essentially part of gastrulation though invagination is much modified and reduced Endoderm formation in all mammals IS basically similar to that m the avian egg in that cells migrate or are delaminated from the deep surface of the inner cell mass (Fig 414) These endodermal cells may in part become intimately related to the trophoblast in the formation of the yolk sac but there is no reason to doubt that their initial formation is an integral part of gastrulation In the second stage of gastrulation there is a migration of surface ectodermal disc cells to a limited axial region of the posterior portion of the embryonic disc to form the primitive streak From tins streak cells come to he between the embryonic disc ectoderm and the endoderm to form the intra embryonic mesoderm (and in many species by later extension the extra embryonic) The anterior extrcmitv of the pnmuive streak is specialized to form the primitive or Hensen s node Some of the cells of this node form an invagination which gives origin to the notochordal or head process as described in human development (page 49I This notochordal process becomes temporarily intercalated in the axial region of the endoderm hut later separates from it to form the notochord In addition to the formation of mesoderm from the primitive streak as an integral part of gastrulation mesoderm can also arise from the trophoblast (extra embryonic mesoderm) from the prochordal plate (cephalic mesoderm) and from the neural crest (page 270) The theoretical consequences of these additional methods of mesoderm formation on our conception of gastrulation are not vet clearly understood For details of gastrulation in marsupials the reader is referred to I Ivnn and Hill (1942) and McCrady (1938 and 1944)


As has been stated earlier (page 69) a structure or tissue developed from the fertilized egg that does not enter into the formation of the embryonic body is called an (extra )embryonic or foetal membrane These membranes are of functional importance during embryonic hfe being concerned with the supply or storage of nutriment respiratory txchange and protection oftheembryo They arelargely shed or absorbed at hatching or birth The foetal membranes include the_job sac the chorion (or serosa) the amnion, the allantois the trophohlasl (m mammals) the piacinia and the orn6jfif<3l cord Certain of them are not necessarily membranous m character

Flo 431 — Section of somite stage of (he de veloping chick embryo to show formation of amniotic caviw and formation of >oIk sac and extra embryonic coelom



(e.g. many placentae and the umbilical cord). In many mammals (deciduate types) the uterine tissues come to be intimately connected with the outermost embryonic membranes (page 67).


The cyclostomes, fishes and amphibia do not possess an amnion and are consequently known as the Anamniota, In the embryos of these vertebrates the only embryonic membrane developed is the yolk sac This sac, whether in the form of a definitive yolk sac (e g., m the megalecithal eggs of the hag-fish, the sharks and the bony fishes, Fig 41 6G) or of a mass of heavily yolked cells (e.g , in frog, Fig 416B), is enclosed within the ventral wall of the body In theforms with a definitive yolk sac during orsoon after gastrulation the ectoderm, mesoderm and endoderm of the embryonic disc grow down over the yolk mass, thus enclosing it within the primitive gut and body wall. This three-layered (trilaminar) yolk sac wall has exactly the same fundamental structure as the gut and abdominal wmll of the frog embryo at about the time of closure of the neural groove The only difference is that in the frog the yolk material is intracellular, within the endoderm cells of the gut (Fig. 416B), whereas in the megalecithal species it is in the form of a relatively large non-cellular mass lying within the gut cavity and distending the whole “abdomen” far beyond the normal body contours (Fig. 41 6C) In these trilaminar yolk sacs the mesoderm becomes very vascular and gradually transports the nutritive material, absorbed from the yolk by the endoderm, to the growing tissues of the embryo proper. Thus the yolk sac shrinks as the body grows, and finally becomes incorporated into the ventral abdominal w^all and gut Its tissues are not only homologous with those of the gut wall and body ^vall, but they actually become part of these structures.

Some Euselachii are viviparous, and in these the yolk sac wall functions both to absorb the yolk through the endoderm and to absorb oxygen and nutriment through its ectoderm from the uterine wall of the mother This is a type of yolk sac placentation, and in some species It consists of a fairly close apposition of the yolk sac wall to the uterine lining (Gate-Hoedemaker, ’^933)* III the relatively rare viviparous bony fishes the yolk sac is usually very small as the eggs themselves approach the medialecithal type In these, therefore, no yolk sac placenta is formed, but absorption from the maternal tissues is carried on by vessels of an excessively enlarged pericardium or by special modifications of gill or anal filaments (Turner, 1940)


Most of the anamniota discussed above deposit their eggs in water, but there are other groups of megalecithal vertebrates {Reptiha, Aves and Monotrematd) which lay their eggs on land These are all characterized by the presence of an amnion, a modification of the extraembryonic body wall (somatopleure) to form a liquid-filled cavity, surrounding the embryo (Figs 416E and F and 422). The most obvious purpose of the amniotic cavity is to provide a local aquatic habitat for the embryo in eggs laid in non-aquatic surroundings The amnion develops before the embryonic body is definitely formed and persists, in these types, until hatching. The ev'olution of the amnion is uncertain, but its probable primitive manner of formation is showm in Fig. 41 6E and F. The chorion, or serosa, is formed during the closure of the amniotic folds from that part of the extra-embryonic body wall which does not contribute to the amnion (Fig. 423) • The development of the extra-embryonic coelom completely or incompletely separates the non-amniotic somatopleure, consisting of extra-embryomc ectoderm and its lining of (somatoplcuric) mesoderm from the splanchnopleure formed by the extra-embryonic endoderm and its covering of (splanchnopleuric) mesoderm This portion of the extra-embryonic somatopleure is the chorion The extra-embryonic endoderm and its covering splanchnopleuric mesoderm form the bilaminar splanchnopleuric yolk sac The chorion and the splanchnopleuric yolk sac are structures not found as such in the aquatic egg types, but nevertheless they are represente in the latter by the somatopleuric and splanchnopleuric layers of the anammote yolk sac (Fig. 41 6C).




This structure is a special precocious!} dcselopcd embr\omc membnne found m the desclopmenl of Metathcna (marsupials) and Emhcna The primara object of this membrane








IS the formation of a vesicle capable of absorbing nutritive material and, by its rapid growth, the provision of a space m which the embryo can grow and differentiate


In viviparous mammals an amnion is always developed and in its definitive stage of development is essentially similar in all metathenan and eutherian groups although it originates

m different ways. The most primitive method of amniogenesis would seem to be by folding of the extra-embryonic somatopleure, as has been described above for the megalecithal amniotes. There are all gradations from this method of amniogenesis to that of such species as the monkey or man, m which the amniotic cavity arises by a cavitation of the inner cell mass as a result of the confluence of intercellular spaces in that part of it related to the covering trophoblast. In some mammals, e.g., carnivores and ungulates (Fig 422), showing amnion formation by folding, the trophoblast over the embryonic disc becomes a thin membrane (known as Rauber’s layer) and disappears, leaving the embryonic disc secondarily intercalated in the wall of the blastocyst and thus exposed until the amnion is formed In many bats (Fig. 422) an ectotrophoblastic cavity appears between the trophoblast and the embryonic disc ectoderm, the definitive amnion IS formed later by folding within this space. In many rodents (Fig. 422) the trophoblast covering the inner cell mass proliferates an , at the same time, the inner cell mass is invaginated into the yolk sac This condition, especially when it occurs at the embryonic isc stage, IS known as “inversion” or entypy 0 the germ layers. The proliferating column o trophoblast is called the “carrier, or rager. The space enclosed by the embryonic disc and the cells of the Trager is the pro-ammotic space. This space is divided by the development o amniotic folds, into a lower amniotic ^ and an upper epamniotic (ectoplacental) cavi y.

In rodents with superficial implantation only partially interstitial implantation

formation IS by simple folding. Thus m with partially interstitial (intramural) imp a tion of a large blastocyst where the uteri epithelium does not grow over disc at the site of penetration, the a develops by folding (Figs 428 an 433 h

The later htstory of the amn,on ar « 





Fig. 423 embryonic

/ -- |Vlossman

■Three stages in the development of the considerably as ^as een ® ^ independent

ic membranes of the chick. (l937)' remain. G/



non \ascubr membrane until fuW term as tn roost mammals twth a small or no allantois (a) it mat expand to obliterate almost coTnpleta> the extra emhT>oroc coeloro the mesodetin coveting the ammon fusme nith that of the chorion, (3) »t ma\ become surrounded b% the allantois thus becoming x asculanzed as in Artiodactyh Pmssodactyla ind Cami^^ra These dificrcnt conditions of the amnion are more hheU dependent upon the degree of development of the allantois than on mtnnsjc functional difTcrcnces in the ammon itself

There ma> be some correlation between the t>pe of ammon formation m mammals and the time and the method of implantation of the blastocvst Early implantation seems to favour ammon formation by cavitation, late implantation is associated with ammon formation by folding


In the development of reptiles, birds and monotremes all of which have mcgalcciihal eggs the first foetal membrane to appear is |he yolk sac It vs formt d vmtiaUy by the extension of blastodermic endoderro round the >olk mass Later the roesodetm becomes interposed between this endodetm and the overlying ectoderm \Nhcn the extra embryonvc coelom appears U splits the mesoderm into an outer somatopleunc layer and an inner splanchno pleunc layer ^Flg 423) The former tot ether with the ectoderm constitutes the Jema or ehrn It while the inner splanchnopkuric layer and the endoderm form the definitive yolk


Metatheria (Marsuptalta) Jnspite of the iact that these mammals have miolecithal eggs they develop a yolk sac soon aficr the falastula stae-e In us fundamental structure this sac resembles very closely that found m the reptiles birds and monotremes After the formation of the endoderm (page 389) this embryonic layer by its own growth extends gradually round the inner surface of the ucutammac ectoderm Eventually the endoderm iQtms a complete lining for the blastocyst wall vvhich thus becomes bilanumr Hill (rgio) from hw study of the development of £)as>unu concluded that the marsupial bilammar blaslo cyst consists of embryonal and extra cmbrvonal

Ftc 424 — Otagrami comparing th^ stager ik early development of a primiUve rod nt of the sijuirrel family [CilrUuj /rtdnmhnealtis) with riniiUr stages in a specialized rodent (laboratory mouse) A B and C — C trtdtCimlintatus (after

Mossman and Weiifeldi 1939) D E and F

Ifw rear a?tir (from Snell 1941)

leyona The fermer is constituted b\ an outer lajer of embf>onic ectoderm tvith an underlying poitionotendodenn (seiiig 40^) these tno lajm ntll form the future embryo The ectra ewhrytinal region separated from the other area by a junctional line is formed bs the Kophohlastic ectodenn (Iroph ectodenn) together nilh the underlying portion of endoderm The tuo layers ectodermal and endodermal of the cetra embryonal region constitute a buatnmar omphalopleurc (or yolh sac) Later In eleielopmetit e-ctension of mesoderm beyond the margin of the embryonal area forms a tnhinunar omphalopicure Since tins mesodermal extension does not usually reach more than a third of the distance to the abembryonic pole of the b asiocyst the b.lammar omphalopleurc preatsts in the abembryomc hemisphere thromhout gestatton and the endoderm of the yolk sac in marsuptals remains ,n permanent contact yyoth the outer nail of the chonomc sac oter a considerable part of m extent (see II, nn 1923 and

^^ove, th,

tije v^T ^ Pericarw ^ ^espiraf dev^, ’ -fJence an ^ f exch^n ^

£S~ ~S- '$?&rs*sz*«Ss^

5f^;S?‘33s '5:5.-S£= t aZ »?5H

an ^'"^mense^ f'^ncZ^- '^^us ,n /r envl^^'T'"^

a storage

a^iantojs varilc “^^ae dur,n 1”^^ indeed, in

appearance and


m the s.ze of endodcrmal component It is iE%a'5 a highW vascular structure -md from us mesoderm is derived the foetal blood svstem to the mam placenta (Figs and 43BI The fused aJhncoic mesoderm (with us vessels) and the chonon Vvsilh us trophoblast) « the foetal portion of all definitive (or chom aUanlou) placentae in mammals The cmlodcrmal portion of the allantois is nell developed in primitive tvpcs (Fig 42B) while in the more specialized species U ma> be either excccdingl) large (Figs 427 and 428) or more often \cr> much reduced (mart) or absent as in some rodents (Ca la)


\s has been stated earlier certam viviparous fishes have developed a t>pe of >olk sac placenta In the amniotes placental mechanisms are found in a slight!) developed condition in certain reptiles and marsupials In the emhcnari mammals placentae are univ ersall) present though as Will be indicated later there is a veo consider able range of variation shown in their nngin histological structure and superficial appearance

Reptilia A few reptiles eg, ccriam snaves, and lizards imfaia and I i/>efO fceno)

arc ovoviviparous that is to sa) the eggs although esscntiall) like those of oviparous forms are heW in the female leproduetive tract until the) hatch The foetal membranes of these species ate not din’erent from those species who c eggs develop outside the bod) Ihere are however a still smaller number of U/ards which are truls vivt parous that is their eg^s have poorl) developed shell and albumen W)ers and their membranes form a rather close union for respirator) and nutritive purposes with the uterine lining of the mother Usuall) it is the )Cilk sic and thr inUf venmg chonon vshich form this placental contact with the maierna.1 tissue but vn one or tv\o species the allantois and the intervening chonon acmallv fuse with tlie uterine lining to form a fairly complex chorjo allantoic placenta (Wcekes 1930 and >935)

Placentatson in Marsupials Like the viviparous lizards the membranes of these lower mammals vary m the degree lo which the )oIk sac and allantois are developed as nutritive, respiratory and excrctor) organs Those with shorter gestation periods like the opossum {Didelphys) and kangaroo {\factopus) seem to depend chiefly upon the )olk sac for nutnijonal relations with the uterus although m all types which have been studied the allantois 1 at least of respiratory significance As has been explained earlier (page 393} the wall of the embryonic vesicle m the opossum eventually shows three different regent '/) an abcmbryonic non vascular portion (hilaminar yolk sac or omphalopleure) (2} a broad vascular zone formed where the mesoderm of the yolk sac remains in contact with the somatopleurc (trilaminar omphalopleure) and (3) the non vascular serosa or chorion Of these three regions though some fluids and substances from the uterine cavity may pass through the first and the third it is the tnfaminar omphalopleure which constitutes the important orpan of nutrition and respiration It can be regarded as constituting a chorjo Mtellme placenta Those marsupials with longer gestaUon periods like Perameles (the bandicoot)

fv - ^ vh- '/%. /5

Fio 425 — Trans\erse sreuon of the aniiin«c>meirial porlion of the uterine cavity m the goJden hamster C 1 e ut aurafus vo jhjw earb atlachment of the blastocMC <30 LRe potlufdfrom Phyiiology ofReprcxluction hy perinisiitn of Messrs Longmans Green 6 . Co Ltd '


have a chorio-allantoic placenta of about the same complexity as the most highly specialized placenta of lizards. (For details of marsupial placentation see Hill and Fraser, 1925, Flynn, 1923 and 1930, Pearson, 1949.)

Implantation in Eutherian Mammals. Before placentation in this sub-order can be described, it is necessary briefly to refer to implantation. In some eutherian mammals S ) P^S) sheep, cow, horse, dog, cat) the chorionic sac remains in the uterine lumen where it expands to fill the greater part of the cavity (Fig 427). This is called central, or circumferential and superficial, implantation. In other eutherian mammals (e.g , mouse, rat, hamster) the blastocyst comes to he in a recess of the uterine cavity which becomes closed off from the remainder of the cavity and in which the blastocyst becomes implanted (Figs. 425 and 426) This is eccentric implantation which later becomes partly interstitial. In still other euthenan mammals (e g , man,

chimpanzee, certain bats) the blastocyst comes to • he in a sub-epithelial position within the decidua

427)* This IS complete interstitial implantation usually occurs at a much earlier stage in development of the embryo than either eccentric or superficial The site of implantation of a blastouterus shows species differences. In many animals (e.g., most rodents and msectivora) on the antimesometrial side of the uterus, in ^ bat, and in Tarsius) li IS on the mesometrial side. In a few species the f implantation is orthomesometrial or lateral, that is,

approximately half-way betw'een the mesometrial antimesometrial positions. This occurs m the

> tenrecs [Centetes and Hemicentetes) where the sites ol implantation of a litter tend to alternate, every other embryo implanting on the same side (Goetz, igs?)*

Placentation in Bnthetian Man.mals. Part of the explanation of the differences the eutherian placenta lies in the extreme variability of the foetal membranes themse ves, and in the manner and extent of their ^eve op ment. In general, the more primitive groups a membranef more nearly like those of the reptiles. Fig 426 — Transverse section through complete while the higher forms have much more specia ize

uterine cavity of the golden hamster, Cncetus membranes This is true for the developmeniai

r history of the membranes as f ^on

of Reproduction,” by permission of Messrs mature condition Since membrane Longmans Green & Co , Ltd ) have evolved independently in each group

after it began to diverge from the

mammalian stock, orders such as the Insectivora and Rodentia show a wide range m mem morpholog)' entirely within the group Because of this the resemblance between the mem of the primitive members of two orders is greater than that between the more specialize is clear, how ever, that there has been much less variation in the structure of the foetal ^

than in the adult morphology of the various groups For example, it would be \ ’-^ee

for an expert on placental morphology, to distinguish between the membranes of a c *'^P gorilla and man, or betw^een those of a sheep and a goat. In fact, even those o a sea-lion (both Carnivora, but of very different body structure) are very similar. .jy

such as these it can be argued that the characters of foetal membranes have changed m evolution than have the adult body chaiacters and that, there.ore, in general, they are

39 ?


criteria for determining phNlogenetic rdationsbips joammals— particularly affinities between the larger groups such as orders and families , , , v

It w not practicable here to give a detailed account of the great v arietv of methods whereby the foetal membranes of evttheriarv mammals dctclop or even to describe their mature structure Reference to Figs 427 and 428 tvhich illusiratt ihc development of the membranes in the pig dog Tarsius rhesus monkey ground squirrel hedgehog and man eives a general idea of repre senutive types of membranes and placentae These figures should be compared with Figs f2q and 430, and Table ^ to correlate the finer structure of the placentae

The chorion is relatively larpc m relation to the embryo m early stages of development but at term m all < utherian mammals the chononic cavity is practically filled by the amnion which in turn has its cavity ocrupted nevrly completely by the foetus In general the earlv chorion is relatively extensiv e m those forms (pig sheep) which develop thm or scattered areas of placentation at a rather late stage whereas in those which rapidly develop a thick and concentrated placental area (man r^ents) it is relatively small from the beginning A large allantoic vesicle is always a concomitant of a large chorion and of a thin or scattered placental «r“a like that of the pig and sheep


The \a cnUrization of the interposed mesodenw vn the trilaminar omphalopleure of many carnivores rodents and msectivores may give rise to a temporary rhono vitelline placentation (Figs 427 and 428) similar to that found mr’awupiah This serves the important function of ciQurtvIuni the embryo until the somewhat tardilv developing allantois has time to reach and v'vseulariitt the chonon

An entirely dilTerent type of volk sac placentation both structurally and physjologicallv develops m the mammals which show some /brm and degree of so called inversion of germ layer or entypy This is called inverted yolk sac placentation and occurs m Rodentva Lagomorpha (rabbits) many Nlicrochitoptcra (bats) andlnvectivora.andmthe Dasypodidae (armadillos) As de enbed on page 394 and illustrated in Figs fj?? and 498 no mesoderm develops m the abembryonic hemisphere of the blasiocvst or bdammar omphalopleure which therefore remains a very thin, membrane m contact with the uterine w all may disappear com pletcly ormavevennever develop asm the guinea pig In any case the embryonic hemisphere of the volk sac is very vascular and inverts into the abembrvonJc area thus bringing us lining rndodeiTn mio very dose relation to the utenne mucosa over a mde area The relative extent nf this inverted volk sac increases as gestation progresses, and m RodenUa and LagomorpfiQ at term it iv attached almost directly on all sides to (he placenta often in a ring very close to the attachment of the umbilical cord In most sprcics part or aF of (he outer or endodermal surface of the inverted volk sac is covered with well formed and often elaborately branched vascular vilU which are in intimate contact with the utenne mucosa These vilh arc usually longest near the chono allantoic placenta and in roam species they fit into crypts m the foetal surface of the placenta In some rodents (eg, Jamtus) endodermal vilh of the inverted yolk sac become so intermingled wuh the true (chono allantoic) placenta thit they form an integral part of it Its elaborate specialuation and the fact that it persists in a functional condition till term indicate that the inverted volk sac placcma « undoubtedly of great physiological significance and a major factor to be corjvjdered m laboratorv experiments concerning placental function m the*e animals

CHORIO ALLANTOIC PLACENTATION IN EUTHERIAN MAMMALS ^^am^lahan placentation may be defined as an apposition or fusion of the foetal membranes ^ the uterine mucosa (o permit of phvstolo^cal exchange between the foetus and the mother I he most tspical of the structures ind the defimtivc one m all Fmhcna is the chono allantoic

placenta However other placental mechanisms exist dunng the development of each euihenan

mammal Of these the chono vilelline and inverted yolk sac placentae of .ome tvpes have





been described above. Other accessor)'^ placental adaptations are illustrated and explained in Figs. 427 and 428. Further discussion of eutherian placentation here is confined to the chorioallantoic type The variety of gross forms of chorio-allantoic placentae has excited interest out of all proportion to its significance. Fig. 430 give some idea of the appearance of the better known varieties

A summary of the finer structure of the main types of chorio-allantoic placentae is given m Table V This is based on Grosser’s (iQsy) classification of them according to the intimacy of the union between the foetal and maternal tissues, or in other words, according to the structure of the membranes separating the maternal and foetal blood in the functional parts of the placenta Grosser rightly maintained that this “placental membrane” is the structure of greatest physiological significance in any form of placentation. The terms which he applied appear S'jrnewhat complicated at first sight, but will be seen to be appropriate, being lormed



Type oj ‘ c 1

1 Epitkeliochonal




Maternal ti,su

Endotlie >


Epithelii 'j

Foetal tissue

+ :


'h 1


Endothei' ,

+ 1



Familiar exari- \

Horse, pig, cattle

Cat, dog

Man, monkey.

Rabbit, guinea pig, rat

Main zoological t'l '1




\niodactyla, Penssodactyla, Cetacea, f Manidae,

1 Leniuroidea, American mole.




European mole





Most Microchiroptera, Hyracoidea, Myrmecophagidae, Dasypodidae,

Most Insectivora, Lower Rodentia (Sciundae, Myomorpha)

Higher Rodentia (Leporidae, Geomoidea, Hystricomorpha)

by a combination of the names of the maternal and foetal tissues which are in contact (Fig 4 ^ 9 ) For instance, if, as m the pig, the epithelium of the utei us persists and the trophoblast 0 t chorion meiely lies m contact with it, the placenta is spoken of as “epithelio-chortal ^

uterine epithelium disappears and the chorion comes into contact with the endothe mm the maternal vessels, as in the dog and other Carmvora, it is an “endothelto-chorial type considered that in many Ungulata the epithelium disappears leaving the chorion m mi with the connective tissue of the uterus. To this ty^ie he gave the name “syndesmo-chort^^^^ Since this condition occurs only in a very limited area of the bovine placenta, an is probably atrophic and non-functional, this type of placentation has been omitte ro table. There are accessory placental areas in other species which structurally syndesmo-chorial conditions, but there are no known cases where the main chorio p placentation is of this t^e. In many mammals (e g., Rodentia, most Insectivora, -yora,

and Cheiroptera) the invasive activity of the placental trophoblast is greater than in so that eventually even the endothelium of the maternal blood vessels is destroyed endothelio-chonal placenta becomes “ haemochorial” While Grosser’s classification ^00

considerable value in the study of different types of placentation, it cannot e app rigidly. Detailed study of the placentae of a number of species has shown


rc^ ate nceexari m an anrmpi in place a Riarn platrma m one nr rllicr nfCttmtei i calcROtaea In manv Lnculaica ftt raample it ba. I>«n .bnnn ibal cap.Uanra ate fnumi in the iropliolilasl ... i

In connwtion >mUj pliccnial iinicturr it mmt Mi • !*■ rrTnpml>rroi ifnt inan\ cliorioMhntoic placcntir Ini e a th.cVrr pberntM infmbrmt m Minr f -iThrr jnqri than \i\cT Hmi m thp rahhit iihrn tlir athntmc circubiinn i» fint rital.hihn! tlirrc arc arraiishcrr llic trophni>bix of thf ciiorion » ju't vntU the ulcnnc cptllicimm an cpithrlirv-clinnal rondition

baler in tlm animal a Incmnchonal cnmliu.m it trachctl tthcrc the maternal hWl it m direct contact ttilh thr irnphrhhti Slill liter the tn>phn»>bit itvlf »rrmt to dioppear from much

Hsrrnwfei 9I Ubff

int«cti<eri (CKCpt H«1eil Ch fOpt«ri HjrriM tfei T»f to tfea and lower S <id«tt Rodentii

Dupl c dent «nd H (her S m pi cident Podtmla

Oeifpodo iei Ctftop e^e<o 4*t and Hoffiineidci are « Hoot Cefeo del New World Am eaten and Oertvioptera an (rabeeular

[ Cp iref o><^eool(An oduifla (S odea Cawitlodra Traxviodei) PeruodaetpU Cctacta Lemgrt New World Holet and 0*d World Am-etten)

tnd t*^l (Carnirorti SloiKt Old World Holei and S ten a)

e £p iNrl oKhonol (hjrpoihetlcal)

MORPHOLOGICAL TYPES OF CHORIO ALLANTOIC PLACENTATtON Atfinjed at 1 tree with ibe mott pilmrtWe tjrpe Lrtow T»ie ijnatl V»p ffurra ibow In 1 mpt fed form (he iiructurc «( (he placental membrane aeparat nj the maternal and foeui blood « A ' t 4^ m T pK«»l < «BW U .« f P •> I w 9 Iwl IV ■ Ql M I Vhi>I >a flooe

Iin Itkwe m* IM mS •« 4t>rc.e

1 10 ^29 — I)i3((raini illuit rating it e riain morpl t4oC‘c»l t>1‘n of cliorio-aUantoic placrnta

of the placenta so that onl) foetal endnihrliiiin separatee tJic luf> 1 ;Io<k 1 streams a hafmo tndotktUal condiuon (Motsman 1936 ) The frrvdom uith tthich sidattances pats from one blood stream 10 the other is correlated to some drv^rec \Mth the thieVness ami slruclure of the placental membrane Thick membranes are pmbab]> lot [lermeablc than thm ^tso the earlier thicker placental membranes of a Riven ipecics arc stated to l>e less permeable than m the later tlnnnrr stiRcs (I lexner tnd Gcihorn tgp see alto pai,c BO It should be stated houcser that estimations of placental permeabiht) on the apparent structure of the placental metnliranc ate still leniativc

A placenta n said to be non deciduous if there « no actual fusion of foetal cliorion to the uterine tissues thus at hirth these pheenne separate without teanne; maternal tissues and therefore without Joss of blood by the mother All epithclio-chnnal tlilTute and rotjlcdonart



placentae are of Jis variety In all other types fusion takes place and more or less maternal Hssue IS shed and maternal blood lost, at b.rth; hence these are deciduous. SpecSclcX cells, as found m human and many other uten, are often absent from decdLs pWentaf

eg., tn the dog placenta, which is considered deciduous only because the maternal da„£ tissues and blood vessels are torn at birth Sianauiar

an ” cp«heho-choriaI placentae are vdlous (Figs. 427, 428 and 420)

All endotheho-chonal, haemo-endothehal and most haemochorial types f re UnLue (Figs 42 ' 428, 429 and 43. A) Some haemochorial types, especially among the primates, exhibit Lin intcr-gradations between a labyrinthine and a villous structure (Fig 43.) Applrentlymanand

ZoRiLLA Brown Bear

of the placema^.^ie^i!^ chorionic sacs of a number of mammals to show the gross forms

zonarj’ or annular rar deer and cow, cotyledonary; monkey, btdiscoidal, dog, etc,

derivations of thr zonary, otter, polecat, ZoriUa and brown bear show special

carnivore zonary placenta

Fiff. 68 illu^rateiffb^ ^^present the maximum expression of the haemochorial villous condition, labyrinthine placenm”^^^if*^ of development of one of the more primitive types of haemochorial Ume seems to be b ' J j change over from the labyrinthine to the haemochorial villous rcsultins- first in a t coalescence of the trophoblastic tubules carrying maternal blood,

that in most labvrmfb'^^^ ^ definite villous condition. As a general rule it seems

directions in areas d I^acentae the maternal and the foetal blood streams flow in opposite UqsSl has desrribpVfi^^ ^ j enough to have functional interchange. Mossman

and there is a nnss.ivi ^ P|^y®*o^ogical advantage of this arrangement in the rabbit placenta placenta (Chapter V Ind a somewhat similar functional provision exists m the human



One of the most puzzling problems of comparatisc morphogenesis of the foetal membranes has been raised h) the demonstration of the peculiar mesench>-niatous ewa embr)onic tissue in the earl> embryos of the primates generally (Hill 1932) of the lemurs (Gerard, i93'>) of man (Streeter 1926 and Hertig and Rock, 1941) and of the monke> (Heuscr and Streeter, 1941) and Its relation to the exocoelom and 4 oik sac From a stud> of comparative embryologv it would be expected that this mesoderm would be formed bj proliferation from the posterior (later pnmitne streak) region of the embrjo whence its cells would spread into the extra embryonic regions However, in both monkev and man the primary extra embryonic mesoderm develops before the appearance of the primitive streak (Figs 59 60 and 432) Hill (1932) and Florian (1933) are of the opinion that this mesoderm arises from the immotic ectoderm postenor to the site of the future tloacal membrane, Gerard (1932) believes that it arises from the endoderm of the volicsac Hertig (1935) Wislocki and Strcctei (1938) and Heuscr and Streeter (1941) have investigated the origin of this mesoderm in well fixed material from the monke> and are com meed that this pnmarv mesoderm IS derived at least in part, directl) from the tropho blavt Hertig and Rock (1941) found evidence of the same condition in their 8th-i2th da> human cmbr>os

— A sect on of a 12 day macac^u? blastocyst i^e yolk sac has now made us appearance between ihe mesoderm and the embryonic ectoderm I Vter Heuser and Stteettr 1941 ) x c 310 'Reproduced by the courtesy of the Carnegie Institution of Washinftol )

Fic 431 — Sections through the placenta of the New World monkey C/irysathn* m Kiialut \ labvnnihine portion E villous portion (After Hill 1932 }

Streeter and Hertig and Rock den> homolo gjcs between the earlv tissues and structure of the primates and those of other mammals and regard the precociousl> developed mesoderm and the cavnties in relation to it as special adaptations found only in higher primates If, however one recogmzes the value of comparative studies, as Heuser working upon the same matenal has done then an early primitive bilammar yolk sac can be recog mzed in the human and monkey with many resemblances to that of other mammals The recent work on the macaque has shown that the primary yolk sac which is essentially like that of all other mammals does not give nse directly to the secondary yolk sac The latter seems to arise by a rearrangement of

human embryology


the originally flat plate of disc endoderm to produce, adjacent to the embryo proper, a separate small cavity which qvnehly becomes surrounded by haematopoietic mesoderm The cavity of this secondary yolk sac seems to have no continuity with that of the pnmary sac (Fig 432) and as it enlarges the cavity of the latter recedes towards the vegetal or abembryomc hemisphere In man as has b«n described in Chapter V, the abcmbry'onic part of the pnmary yolk sac becomes separated completely from the remainder A surpns ingly comparable process is exhibited by the sloth Bradypus grisfus (Heuser and islocki, 1935), ^^here the exococlom extends around all except the abembryomc end of the primary yolk sac where the latter s original connexion with the trophoblasl is maintained A constriction develops between the abembryomc and embryonic portions of the sac which results in complete separation of the two portions There is then a small proximal haematopoietic, splanchno pleunc yolk sac homologous with the definitive yolk sac of man and the macaque, and a distal or abembryomc degenerating portion of the primary sac comparable with that part of the pnmary yolk sac of the monkey which is relegated to the abembryomc hemisphere of the chorionic vesicle It seems reasonable to assume therefore that the relatively direct and early method of separation of the two parts of the yolk sac m the macaque is merely an abbreviated and specialized method of pinching off of the distal portion seen m its more pnmitivc form in the sloth and possibly in man where the primitive abembryomc portion of the yolk sac is indicated in some embryos (Chapter V and Figs 75 and 76)


de Beer G R (i94o) Embryos and Ancestors Oxford Unn Press London

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Flynn T T (1023) The yolk sac and allantoic placenta in Prr<i«r/« Quart J Micro Set 67 123-163 — (1930) The uterine cycle of pregnancy and pseudopregnancy as 11 is in the Diprotodont Marsupial Bdieneia runirufus Proe Unn Set Setv Sauth ttabs 50*^531

and Hill J P (1939) The development of the Monotremaia IV Growth of the ovarian ovum maiura

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   Human Embryology (1945): 1 Introductory Concepts | 2 Formation Maturation and Structure of Germ Cells | 3 Cyclic Changes in Female Genital Tract | 4 Fertilization Cleavage and Formation of Germ Layers | 5 Implantation of Blastocyst and Development of Foetal Membranes Placenta and Decidua | 6 Fate of Germ Lavers and Formation of Essential (Primary) Tissues including Blood | 7 Growth of Embryo Development of External Form Estimation of Embryonic and Foetal Age | 8 Determination Differentiation Organizer Mechanism Abnormal Development and Twinning | 9 Cardio Vascular System | 10 Alimentary and Respiratorv Systems Pleural and Peritoneal Cavities | 11 Urogenital System | 12 Nervous System | 13 Skeletal System | 14 Muscle and Fascia | 15 Integumentary System | 16 Comparative Vertebrate Development | Figures
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