The early development of the cat 4
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Hill JP. and Tribe M. The early development of the cat (Felis domestica). (1924) Quart. J. Microsc. Sci., 68: 513-602.
- 1924 Cat Development: ￼1. Ovum of the Cat | ￼2. Process of Cleavage | ￼3. Formation of the Blastocyst | ￼4. Discussion | ￼Plates | cat
Chapter IV. - Discussion
1. Mode of Formation of the Blastocyst
The blastocyst of the Cat, like that of other Monodelphia, is derived from the completed morula as the result of the appearance at one of its poles of a fluid-filled cavity situated between the central cells destined to form the embryonal knot or inner cell-mass and the peripheral layer (trophoectoderm, trophoblast). The precise mode of origin of this cavity is a matter of some little interest, though but few observers have discussed it in any detail.
It is worthy of note (1) that the zona attains its maximum thickness (0012 mm.) in the late morulae and early blastocysts described in the preceding pages, and (2) that the morula shows no appreciable increase in size during the period the blastocyst-cavity is in process of appearing.
The progressive increase in thickness of the zona is no doubt simply due to the fact that up till now the egg has undergone no marked increase in diameter, but whether the presence of a very thick zona has any significance in relation to blastocyst formation is a question not easy to answer, though it is conceivable that it tends to inhibit the too rapid diffusion of fluid into the egg when the blastocyst-cavity is in process of formation and, once that cavity has appeared, the too rapid expansion of the blastocyst.
The facts that the morula shows no appreciable increase in size during the formation of the blastocyst-cavity, and that the cells of the embryonal knot are no more compactly arranged after than before the appearance of that cavity, render it clear that no mere flowing together of inter- or intra-cellular spaces or vacuoles is a sufficient explanation of its origin in Pelis. The only other alternative mode of formation is by the cytolysis of certain of the central cells, and of that there is evidence in our eggs 29, 30, 31, 32, and 33.
The evidence derivable from study of these eggs leads us to conclude that the blastocyst-cavity in Pelis arises partly by the degeneration of certain of the central cells, partly by the running together of fluid-filled intercellular spaces. Once the cavity has appeared its subsequent enlargement is brought about by the active expansion of the enclosing layer of trophoblast, with accompanying absorption of fluid from the uterine lumen. Growth is at first most marked over the lower hemisphere, since the embryonal knot, closely applied to the thin and inactive covering trophoblast at the upper pole, acts as a hindrance to expansion in this region. This is shown by the fact that in our early enlarging blastocysts, the zona, though very much thinner than in the late morulae, is thickest over the upper hemisphere, and also by the fact that the trophoblast is thicker immediately around the embryonal knot than elsewhere.
Kohlbrugge (33), in describing the formation of the blastocyst in the Bat, Xantharpya amplexicaudata, clearly recognized that the first appearance of the blastocyst-cavity in the form of a series of small isolated cavities which subsequently run together is the result of the breaking down of certain of the central cells. He says, ' Es kann dies nur durch Zellenschwund geschehen, da das Ei ja immer noch von der festen Zona umgeben ist, die dabei prall gefiillt ist' (p. 14). His figures 9—12 illustrate the process and show that during the period when the blastocyst-cavity is forming the egg does not increase in size.
In the Mouse, Sobotta (47) describes the cavity of the blastocyst as arising by the confluence of a number of irregular spaces which appear between the cleavage-cells, whilst Melissinos (38), also in the Mouse, Huber (26) in the Eat, and Hubrecht (29) in Tarsius, state that it arises as a single intercellular space. In the Eabbit, Assheton (3) figures the first appearance of the blastocyst-cavity in a morula of seventy- seven hours (fig. 21, PI. 15) as a curved intercellular cleft situated between the trophoblast of the lower polar region and the cells of the inner cell-mass. He admits that the question of how the cavity is actually produced is one of very great difficulty, but thinks that ' the first cause which produces the cleft that subsequently enlarges into the cavity of the blastodermic vesicle may be a more active growth of the outer layer of cells '. He adds ' undoubtedly there is after this time a more active growth of the outer layer of cells '. No mention is made of intracellular vacuoles or of cell-degeneration, but in the Pig (4) he is inclined to think that the cavity owes its origin to the running together of such intracellular vacuoles, so also in the Ferret, and ' less clearly so in the Sheep ' (6).
E. van Beneden (10) attached great theoretical significance to the precise mode of formation of the blastocyst-cavity, and in his preliminary paper of 1899 on the early development of Vespertilio murinus, he considers the process in some' detail. His conclusions as set forth in that paper may be summarized as follows :
(1) Intracellular vacuoles appear in those cells of the inner cell-mass, situated in one hemisphere of the morula, which in subsequent stages come to limit the blastocyst-cavity; (2) the protoplasmic walls separating these vacuoles are then gradually withdrawn into the cells on what will be the convex surface of the mass of embryonal ectoderm, and thus the vacuoles run together to form the single continuous blastocyst-cavity, the process first beginning on the side where the vacuoles adjoin the enveloping layer of trophoblast. The cells in which these vacuoles are formed, by ' un veritable acte de secretion ', give origin to the layer which is by most embryologists termed the entoderm or hypoblast, but which in van Beneden's view is not the true entoderm, and so he terms it the ' lecithophore ' and includes with it the fluid filling the blastocyst-cavity, since this fluid is a secretory product of the lecithophoral cells. The yolk-entoderm of other Vertebrates may for practical purposes be taken as the equivalent of the ' lecithophore '. In his posthumous paper of 1911 (11), edited by A. Brachet, emphasis is laid on the presence in the inner cell-mass as well as in the blastocyst-cavity of cells in process of degeneration,' de noyaux en chromatolyse dans un protoplasme en voie de degeneres- cence ' (p. 38 ; cf. figs. 89, 44, 45, 46), and it is stated, ' il semble done que la formation de la cavite blastodermique, bien que resultant essentiellement d'un processus d'elaboration et de secretion des cellules, ne s'acheve pas sans que certaines de celles-ci n'y trouvent la mort ' (p. 38).
To this mode of formation of the blastocyst-cavity by the flowing together of intracellular vacuoles, van Beneden, on theoretical grounds, attached great importance since he believed it demonstrated the correctness of his view of the homology of the blastocyst-cavity of the mammal with the sub-germinal cavity of the sauropsidan egg, extended by further accumulation of fluid so as to include the whole of the yolk. In the case of both cavities he believed that the fluid filling them resulted from a definite process of intracellular secretion.
In the present connexion the essential point in van Beneden's interpretation is that he regards the cells in which the vacuole3 appear as lecithophoral cells, i.e. as cells which in the broad sense are entodermal or, more strictly, yolk-entodermal. In any case the cells in question form the layer which clothes the under surface of the embryonal ectodermal mass in the early blastocyst, and is by the majority of writers termed the entoderm. Now van Beneden's interpretation presupposes a precocious segregation of these cells in one hemisphere of the morula, and of that no evidence is forthcoming from what we know of other mammals. Indeed, such evidence as we possess concerning the origin of the entoderm in the Mammalia is directly opposed to the occurrence of any such early segregation.
(1) The observations of one of us on the origin of the entoderm in the marsupial Dasyurus demonstrate that the unilaminar formative or embryonal region of the blastocyst- wall is composed of two varieties of cells, viz. a more numerous series of larger, lighter-staining cells, destined to form the embryonal ectoderm, and a less numerous series of smaller, more deeply staining cells which eventually migrate inwards to form the entodermal lining of the vesicle. (2) In Didelphys. Hartman (23) has obtained entirely comparable results. (3) The observations of Patterson (42) on the formation of the entoderm in Tatusia show that the inner cell-mass of the blastocyst likewise consists of two types of cell, viz. larger, lighter-staining cells destined to form the embryonal ectoderm and smaller more darkly staining cells, with sharply denned outline which at first are evenly distributed amongst the former and which later migrate down to the deep surface of the inner cell-mass and eventually separate off to form the entoderm. (4) The observations of 0. van der Stricht on the origin of the entoderm in the Dog show that the entodermal cells only make their appearance subsequently to the disappearance of Eauber's layer and the intercalation of the embryonal knot in the trophoblast, i.e. long after the formation of the blastocyst-cavity.
Whilst we are prepared to accept van Beneden's description of the formation of the blastocyst-cavity in Vespertilio by the confluence of intracellular vacuoles, accompanied by the actual breaking down of certain of the central cells, we do not think that his interpretation of the vacuolated cells as exclusively lecithophoral is fully established. At the same time we must confess that we attach little or no phylogenetic importance to the precise way in which the blastocyst-cavity arises in the mammals, since its mode of formation differs in the three subclasses and may very well vary in its details within the limits of the Monodelphia, even though it is an homologous cavity throughout.
2. History of Embryonal Knot and Covering Trophoblast
Our observations show that the embryonal knot furnishes, as in other Monodelphia, the embryonal ectoderm and the entoderm of the vesicle, segregation of the two commencing shortly after the appearance of the blastocyst-cavity and being completed relatively early. Our material is not sufficiently extensive to enable us to trace the origin of the entoderm in detail, but we have produced some evidence indicative of the presence in the embryonal knot of two varieties of cells which we interpret as the parent cells of the embryonal ectoderm and entoderm respectively, and which we regard as entirely comparable with the two types of cell observed by one of us (24) in the formative region of the blastocyst-wall in Dasyurus, by Hartman (23) in that of Didelphys, and by Patterson (42) in the embryonal knot of Tatusia. In these three mammals the entodermal mother-cells reach their final position on the under surface of the layer or mass formed by the segregation of the other variety (embryonal ectoderm) as the result of a process of active migration, and we see no reason to suppose that the same process does not occur in the Cat. Already in our blastocyst 36 (0-25 mm. in diameter) the entoderm appears as a more or less connected layer underlying the mass of embryonal ectoderm, and from there it gradually extends by its own growth to form a complete lining to the blastocyst-cavity.
The embryonal ectoderm in the just-mentioned blastocyst has the form of a lenticular mass of cells which is in the closest apposition with the already very attenuated covering trophoblast (Eauber's layer). It soon assumes a more rounded form and at the same time its cells undergo rearrangement and take on a columnar form. This results in the formation of a slight depression on its surface and the disappearance of the covering layer in the region of the depression, the trophoblast now becoming connected with the embryonal ectoderm round the margin of the same. In this way the embryonal ectoderm becomes intercalated in the trophoblast and so exposed at the surface. As the vesicle grows, so the embryonal ectoderm expands to form an approximately circular disc, the shield- ectoderm or ectoderm, of the embryonal area, composed of a layer of columnar cells and in continuity marginally with the trophoblast.
0. van der Stricht's observations (53, 54) show that in the Dog the sequence of events in the region of the embryonal knot is somewhat different from what we describe in this paper for the Cat. According to his account, in blastocysts 0-2 to 0-3 mm. in diameter, the embryonal knot is still undifferentiated, and appears as a convex mass attached to the inner surface of the trophoblast. As the result of the increasing pressure of the fluid filling the blastocyst-cavity, the knot gradually becomes flattened out, and in vesicles 0-3 to 0-4 mm. in diameter it 'compresses and gradually repels laterally, outside the embryonal pole, the overlying cells of Eauber's layer. Eventually the knot is intercalated within the unilaminar layer of the blastocyst which is now everywhere monodermic. This stage recalls that of Marsupials ' (J. P. Hill). In other words, in the Dog it is the embryonal knot itself, according to 0. van der Stricht, which expands and becomes intercalated in the trophoblast, whereas in the Cat the knot first undergoes differentiation into its two constituent parts and then the embryonal ectoderm, without preliminary expansion, becomes intercalated in the trophoblast, Rauber's layer at the same time disappearing. According to O. van der Stricht, it is not until the blastocyst has reached a diameter of 0-7 to 0-8 mm., the embryonal knot having meantime become more flattened and thinner, that' a few small cells seem to be forced or compressed towards its inner surface, next the blastocyst-cavity ; these give rise to the lecithophore or hypoblast which is now virtually laid down '. O. van der Stricht has made the very interesting observation that the entoderm cells which first appear are capable of passing back into the knot if the internal pressure be reduced by accidental puncturing of the wall of the living blastocyst, a valuable confirmation of the migratory powers of the entoderm to which attention was first called by one of us, in the case of the entoderm mother-cells in Dasyurus. In blastocysts 1 to 1-5 mm. in diameter, van der Stricht states that the entoderm forms a continuous layer below the embryonal ectoderm and has also extended out to line the trophoblast, the vesicle-wall eventually becoming didermic throughout. The relatively late appearance of the entoderm in the Dog is a noteworthy difference from the Cat.
Much more important, however, is the fundamental agreement in the development of these two Carnivores, which is to be found in the fact that the embryonal ectoderm becomes freely exposed at the surface and intercalated in the trophoblast as the result of the thinning out and eventual disappearance of Eauber's layer, no closed ecto-trophoblastic or (so-called) primitive amniotic cavity being formed.
From the descriptive part of this paper it seems clear that the thinning and eventual rupture of Rauber's layer is not directly due to the expansion of the embryonal ectoderm to form the shield-ectoderm, as is apparently the case, e.g., in the Rabbit, since this expansion only takes place after the disappearance of the covering layer. If we are justified in ascribing the attenuation of the covering layer to a mechanical cause, then we think an efficient cause is to be found in the close attachment (amounting almost to fusion) of the embryonal ectoderm to the covering layer, which no doubt prevents the growth of this area of the trophoblast during the expansion of the vesicle, whilst the embryonal mass probably also exerts a certain amount of pressure on the covering layer, as 0. van der Stricht suggests, such pressure resulting from the gradually increasing tension of the fluid in the blastocyst-cavity, consequent on the growth of the blastocyst-wall and the imbibition of fluid from the uterine lumen. But the actual rupture of the layer and the concomitant appearance of the slight depression on the surface of the embryonal ectoderm seen in blastocyst 38 (fig. 33 a) are, we think, related phenomena, the result of the commencing assumption by the ectodermal cells of a columnar arrangement. This surface depression, we would emphasize, is a mere transitory formation with, in our opinion, no significance other than that just indicated, and is in no sense to be regarded as a vestigial representative of the so-called primitive amniotic cavity seen in certain other mammals (Pteropus, Galeopithecus, Tatusia, Cheiroptera, higher Primates, &c).
If now we turn for a moment to the consideration of the developmental history of the embryonal knot and its covering layer in the Monodelphia generally, we find that the knot, whilst in all cases giving origin to the embryonal ectoderm (including probably also the amniotic ectoderm) and the entire entoderm of the vesicle, varies considerably in the details of its differentiation, and that the fate of its covering layer is also very variable. During the assumption by the embryonal ectodermal mass of its definitive epithelial form, the covering layer may, as in the Cat, disappear, with the result that the shield- ectoderm becomes intercalated in the trophoblast and exposed at the surface or it may persist either temporarily or permanently, in which case a cavity arises either between it and the shield-ectoderm or actually in the embryonal ectoderm itself. The cavity so arising may have merely a temporary existence or, on the other hand, it may persist to form the definitive amniotic cavity.
The variations just indicated may be grouped as follows :
G r o u p I.—The shield-ectoderm becomes intercalated in the trophoblast and exposed at the surface as the result of the thinning out and disappearance of the covering trophoblast. No closed cavity is formed during the differentiation of the shield-ectoderm. The arnnion arises by fold-formation. Lepus, Felis, Cam's, Ovis, Sorex.
G r o u p II.—During the differentiation of the shield- ectoderm a transitory (ecto-trophoblastic) cavity appears between the latter and the covering trophoblast, the shield- ectoderm forming a more or less curved or even Y-shaped plate. When the shield-ectoderm flattens out, the covering trophoblast is ruptured, and the ectoderm at the same time becomes exposed and intercalated in the trophoblast as in Group I. The amnion develops by fold-formation.
Tupaia, Talpa, Tarsius, Sus. In Cervus (Keibel, 32) a temporary cavity generally appears in the embryonal ectodermal mass itself, though sometimes the covering layer ruptures before the appearance of such a cavity as in Group I.
Group III.—An ecto-trophoblastic cavity arises as in Group II (Vespertilio) or the cavity appears in the embryonal ectodermal mass, its roof soon opening out (Erinaceus) or disappearing (Miniopterus). The shield-ectoderm never becomes exposed and the amnion is formed by fold-formation below the persisting covering layer, the ecto-trophoblastic cavity becoming secondarily enclosed to form the amniotic cavity. Arvicola and Mus spp. may also be included here : a primitive amniotic cavity arises as in Group IV, but it later opens into an ectoplacental cavity situated in the ectoplacental trophoblast and the amnion is formed by secondary closure.
Group IV .—The covering trophoblast persists and the shield-ectoderm never becomes exposed. A cavity (the primitive amniotic cavity, sensu stricto) arises in the embryonal ectodermal mass, which persists to form the definitive amniotic cavity, its floor being constituted by embryonal ectoderm and its roof by amniotic ectoderm. Mesoderm and coelom penetrate later between the latter and the trophoblast, thus producing amnion on the inside and chorion on the outside. Pteropus, Cavia, Tatusia, Xantharpya, Galeopithecus, higher Primates.
The question of amnion-formation in the mammals generally is outside the scope of this paper, but it is so intimately bound up with the history of the embryonal knot and its covering layer that some brief reference to current views is here necessary. For a detailed exposition the reader is referred to the papers of Hubrecht (28, 30, 31), van Beneden (10), Assheton (6), and Da Costa (17, 18). Hubrecht, in his dissertation on the phylogeny of the amnion and the significance of the trophoblast published in 1895, was, we think, the first to draw attention to the occurrence of two types of amnion-formation in the Monodelphia, viz. (a) by the closure of amniotic folds and (b) by the persistence of a, cavity which appears already completely closed in the blastocyst, to form the definitive amniotic cavity. He formulated the view that the latter type of ' closed amnion-formation ' is the primitive one for the Amniota as a whole, and that the more familiar mode of amnion-formation by the closure of amniotic folds has been secondarily derived from the ' closed ' type as the result of coenogenetic modification (' als einen bedeutend cenogenetisch modificierten Entwickelungsprozess ') (28, p. 24). Hubrecht's views on this question are based on his conception of the trophoblast as of the nature of a larval envelope, the homologue of the ' Deckschicht' of the amphibian embryo, a conception which has met with much adverse criticism from various writers (cf. Hill, 24) and which we do not propose to consider further here, though we acknowledge the value and stimulating character of Hubrecht's contributions to our knowledge of amnion-formation.
In 1899 E. van Beneden (10), in his classical paper on the early development of Vespertilio, also supported the view that the ' closed ' method of amnion-formation is more primitive than that by fold-formation, not for the Amniota as a whole, however, but only within the limits of the Monodelphia. This conclusion he reached on quite other grounds than those advanced by Hubrecht, to whose .theoretical views he was, as is well known, strongly opposed.
He points out that between the types of development represented by the Primates and the Rodents with inversion on the one hand, and by the Rabbit and Shrew on the other, all transitional stages exist, and he proceeds to inquire which of these modes of development is to be regarded as the more primitive for the Monodelphia. ' II y a de serieuses raisons de penser ', he writes (p. 331), ' que le developpement du Lapin, considere pendant longtemps comme typique pour les Mammiferes placentaires, est au contraire le terme extreme d'une serie cenogenetique ; que le mode ancestral de developpement des Mammiferes placentaires se rapprochait beaucoup de ce que nous observons chez les Rongeurs a feuillets renverses et que c'est, par alteration progressive de ce processus primitif, que revolution en est arrivee a s'accomplir cornrne chez le Lapin et les Musaraignes". Van Beneden termed the cavity formed either between the embryonal ectoderm and the trophoblast or actually in the mass of embryonal ectoderm itself the primitive amniotic cavity irrespective of whether it persisted to form the definitive cavity or not, and on the view that the occurrence of such a cavity is the ancestral condition for the Monodelphia he regarded the temporary cavity as the vestigial representative of the persisting one.
Assheton (5, 6) also accepted the view that the closed type of amnion-formation was the more primitive. He writes (6, p. 267), ' this means that the rabbit, sheep or dog type of amnion formation has been derived from a type like that seen in Cavia, whose ancestors had the sauropsidan mode of amnion formation'.
More recently Da Costa (17), in giving an account of the development of the amnion in the Bat, Miniopterus, has reviewed the whole question, and without hesitation declares himself in favour of the views of Hubrecht and van Beneden, but without adding any arguments of weight in its favour. He says (18, p. 327), ' je considere comme primitive l'amniogenese par creusement du bouton embryonnaire et la formation de plis comme seeondaire. Cette opinion, qui a ete celle de Hubrecht et de van Beneden, me semble inattaquable, du moins au point de vue ontogenetique.' He distinguishes the former type as a ' Schizamnios', the latter as a 'Plectamnios'.
Van Beneden bases his view on the following considerations (10, p. 331) : (1) the formation of a cavity in the mass of embryonal ectoderm has been observed in all the orders of Monodelphia, from the Ungulates to the Primates ; (2) the occurrence even in the Babbit of an embryonal knot; (3) Rauber's layer is obviously in the Babbit a vestigial structure, homologous to a part of the ectoplacenta of other mammals, and in the Babbit and the Shrew plays neither a functional nor a phylogenetic role.
We must confess we are not impressed by any one of these considerations. As concerns (1) our own observations and those of 0. van der Stricht show that in two representatives of the order Carnivora, Felis and Canis, no closed cavity appears during the differentiation of the embryonal ectoderm, and in any case we are of opinion that the formation of a closed cavity at this period in the development of the blastocyst is of no phylogenetic significance whatever and is simply a by-product, so to say, of that peculiar adaptive condition, viz. the complete enclosure of the formative cells by the trophoblast which is characteristic of all the Monodelphia.
Its presence or absence and its permanent or transitory character are evidently conditioned by a variety of circumstances, e.g. the relation of the blastocyst to the uterus, the character of the covering layer and the mode and rate of expansion of the embryonal ectoderm, and we are inclined to think that its appearance can be shown to be related to the assumption by the constituent cells of the embryonal ectodermal mass of their definitive epithelial form, a rearrangement which in a number of cases (e. g. Talpa, Vespertilio) is apparently accompanied by the degeneration of some of the ectodermal cells. The case of Vesperugo noctula described by 0. van der Stricht (48, 51) appears to form an exception, since here the ecto-trophoblastic cavity only appears after the embryonal ectoderm has spread out below the covering trophoblast in the form of an epithelial layer, but in an earlier stage, when the embryonal ectoderm is in process of differentiation, van der Stricht states that there are present, between the latter and the already attached placental trophoblast, ' souvent des fentes, des espaces irreguliers, en quelque sorte virtuels, autour desquels sont seriees les cellules epitheliales de l'epiblaste embryonnaire' (51, p. 7). These spaces disappear as the embryonal ectoderm spreads out in close contact with the placental trophoblast, but there can be little doubt they represent the ecto-trophoblastic cavity which here becomes temporarily obliterated owing to some exceptional condition of pressure inside the blastocyst of this particular species.
Consideration (2) is discussed by van Beneden at some length, and the view is expressed that ' l'amas interne, massif, des Mammiferes actuels doit son origine a la substitution d'un processus cenogenetique a une invagination primitive de la tache embryonnaire ' (p. 332). Although it is nowhere expressly so stated, van Beneden would appear to have regarded the so-called primitive amniotic cavity as in some sense a reappearance of the hypothetical invagination cavity, and consequently those mammals in which such a cavity arises and persists to form the definitive amniotic cavity are more primitive than those in which the embryonal ectoderm becomes directly exposed and intercalated in the trophoblast as in the Babbit and Cat.
One of us (24) has already discussed the significance of the enclosure of the embryonal knot by the trophoblast in the Monodelphia, and we need only say here that whilst we are at one with van Beneden in regarding the internal position of the embryonal cells in the Monodelphia as a purely adaptive phenomenon, we are unable to picture to ourselves an ancestral developmental stage involving an actual invagination of the embryonal area within an enveloping layer. There is no evidence of such a stage in ontogeny, and we think that the Monodelphian condition was attained quite suddenly as a direct advance on such an antecedent condition as is seen in the blastocyst of existing marsupials.
As concerns consideration (3) we think the statement that the covering layer plays no functional role either in the Rabbit or Shrew goes too far, and we venture to suggest that it has a functional value in completing the wall of the expanding blastocyst and in providing a place of attachment for the inner cell-mass, but we agree it has no phylogenetic value since it is essentially a structural adaptation evolved within the limits of the Monodelphian mammals.
Whilst we are quite prepared to accept the view that the early history of the embryonal knot in the Eabbit is atypical for the Monodelphia so far as concerns its unique mode of expansion, we cannot agree that in respect of the disappearance of the covering layer and the absence of a primitive amniotic cavity the Rabbit and Shrew are less primitive than Mus and Cavia. Indeed, we would maintain that the type of development seen in these Eodents with inversion and that exhibited by the higher Primates, Pteropus, &c, far from being primitive, represent the culmination of • specialization along separate and independent lines of developmental adaptation. Just as the palaeontological evidence demonstrates parallelism in the evolution of skeletal characters in the most diverse orders of the Mammalia, so we hold the embryological evidence testifies to the existence of parallel and ipso facto independent lines of ontogenetic development.
In spite of the weight of authority in favour of the opposing view, we hold fast to the conclusion, which is of course not new, indeed may be regarded as old-fashioned, that the type of development seen in our Group I is to be regarded as the most primitive for the Monodelphia. That view appears to us to be supported by the following considerations : (1) it is the type of development which most closely approximates to the conditions obtaining amongst the lower Mammalia, Canis, as 0. van der Stricht has shown, actually realizing, after the disappearance of Eauber's layer, the marsupial condition where the formative (embryonal) cells are from the first spread out at the surface to form the upper hemisphere of the blastocyst. (2) It is the simplest and most direct type of development, the embryonal ectoderm in attaining its definitive form and its ancestral surface-position simply bringing about the degeneration, with resulting complete disappearance of Eauber's layer. (3) The development of the amnion by fold formation is clearly the ancestral method for the Monodelphia, seeing it is the sole method met with in the Sauropsida, the Monotremes, and the Marsupials. The 'closed' method of amnion-formation as in our Group IV, as well as that by fold- formation below the persisting Eauber's layer as in Group III are, in our opinion, secondary specializations which have been acquired by various Monodelphia in adaptation to the conditions of intra-uterine development, and we would lay particular emphasis on the fact that in all such cases the blastocyst either becomes directly attached to the uterine lining as the result of the proliferative activity of the trophoblast over at least the embryonal pole (i. e. over an area including the covering trophoblast), or is actually imbedded or in process of becoming imbedded in that lining. AVe know of no recorded instance of closed amnion-formation in a blastocyst which reaches the embryonal shield stage whilst still free in the uterine lumen. Supporters of the primitiveness of the ' closed ' amnion would read the series from Group IV to I. We prefer to start with Group I and to regard the others as independent lines of specialization.
3. Prochordal Plate
It is outside the scope of this paper to deal at any length with the prochordal plate and in particular to consider in detail its later history, but in view of the fact that its presence has now been demonstrated in embryos of all classes of Vertebrates and of its great intrinsic interest, some brief discussion of its significance may not be out of place.
As already indicated, Hubrecht in 1890 was the first to direct special attention to the thickened patch of entoderm which in the blastocyst of the mammal underlies the anterior region of the shield-ectoderm, and with which the anterior extremity of the head-process later on makes connexion, and to apply to it the name of protochordal plate. In his paper on the development of the germinal layers of Sorex, Hubrecht (27) states that in blastocysts 0-8 to 1 mm. in diameter, in which the shield-ectoderm is differentiated and the hypoblast completely lines the blastocyst-cavity, he invariably finds that the hypoblast is thickened just below the anterior margin of the embryonic shield over an area comprising some five or six dozen cells. The cells over this area are thicker and more massive and the nuclei are much more closely packed (fig. 30, PI. xxxvii) than over the remainder of the hypoblast. He states further (p. 508), ' this patch of modified hypoblast-cells has at the beginning an oval shape, with the long axis perpendicular to that of the embryonic shield. Part of this patch will develop into the anterior portion of the notochord ; for this reason I will call it the protochordal plate.' Hubrecht reserved for a future publication fuller consideration of the history of this plate including its participation in the formation of the wall of the fore-gut and pharyngeal membrane as well as in that of the heart, and though, unfortunately, he never carried that intention into full effect, he deals in some detail with the protochordal plate in his papers on Tarsius (29) and on the early ontogenetic phenomena in mammals (30). It is worthy of note, however, that in none of his papers did he ever produce any definite evidence for his statement that it gives origin to the anterior extremity of the chorda. He was apparently still of that opinion when he wrote his Tarsius paper (v. p. 79),
though it is clear, as Assheton (6) and Brachet (15, p. 518) have pointed out, that it is incompatible with the theoretical views he expounds in the same paper, according to which the chorda is restricted to the notogenetic region of the body of the embryo (chordal region of head and the trunk), whilst the cephalogenetic region comprising the most anterior part of the head is prechordal. It is to this prechordal region that the protochordal plate belongs, and accordingly it should not, a p r i o r i , produce chorda. Hubrecht's views on the significance of the plate are referred to later.
In 1901 Bonnet (14 a) gave a detailed account of the proto- chordal plate in the Dog, terming it, as already noted, the ' Erganzungsplatte des Urdarmstranges ' because he believed it produced the same derivatives as the ' Urdarm ', viz. mesoderm, chorda, and gut. Already in 1889 he had concluded from his observations on the Sheep that the anterior extremity of the chorda is derived from a ' Chorda-entoblast' area in the roof of the fore-gut and he re-affirms this conclusion for the Dog, but his evidence, we think, is insufficient to settle the question finally. He points out that in embryos with sixteen pairs of somites the anterior portion of the chorda reaches close up to the dorsal insertion of the primitive pharyngeal membrane (oral plate), and actually terminates in what he regards as the last remnant of the ' Erganzungsplatte ', viz. the ' Praoral- Entodermtasche' (Seessel's pocket). It thus extends over the area occupied in earlier stages by the ' Erganzungsplatte ', and he accordingly concludes that this anterior part of the chorda is formed from the latter plate pari passu with its reduction from behind forwards. It is, however, possible that the anterior portion in question is formed simply by the growth of the chorda itself, its original connexion with the plate or a derivative of the same being maintained during the process of elongation, and until that possibility is definitely excluded we must hold Bonnet's contention unproven. Apart from this question Bonnet's observations clearly demonstrate that the plate gives origin, by proliferation, to cephalic mesoderm, that it forms the upper part, at all events, of the entoderm of the oral plate, and that it furnishes the wall of the pre-oral gut- rudiment (Seessel's pocket) which in the Dog is small and inconstant.
Under the name ' Praoral-Entodermtasche ' Bonnet includes, besides Seessel's pocket, a median mass of cells (clearly shown in his fig. 67 representing a frontal section through the head of an embryo of sixteen somites) which he regards as forming part of the wall of the latter pocket. In this mass the chorda terminates, and from it grow out laterally two solid cellular buds which Bonnet identifies as the vestiges of the premandibular head-cavities of other Vertebrates. This mass is clearly the homologue of the median plate of cells which Oppel in 1890 described under the name of ' Praechordalplatte ' in Anguis and from which he showed well-developed premandibular cavities take their origin, and it is also identical in its relations with the irregular plate-like mass of cells described and figured by K. M. Parker (41, fig. 5) in an embryo of Perameles nasuta under the name of the prechordal plate. This mass is in continuity with the distal extremity of Seessel's pocket, whilst it is directly continuous behind with the chorda. Dr. Parker shows that the mass in question is the remnant of the more extensive prochordal plate of earlier stages, from which the primordia of the premandibular head-cavities take origin as solid lateral outgrowths (see especially her figs. 1 and 2), quite similar to the buds described and figured by Bonnet, though it is a significant fact that they appear in a relatively earlier developmental stage in Perameles than in the Dog.
The fact that the premandibular cavities are related to or take their origin from a median mass of cells (very variously designated by different observers) which forms part of, or is connected with, the anterodorsal wall of the fore-gut and with which the chorda is fused, has been recorded by a large number of observers, including van Wijhe 1882, Hoffmann 1886, Oppel 1890 (' Praechordalplatte'), Platt 1891, Rex 1897 (' inter- epitheliale Zellmasse'), Chiarugi 1898 (' massa cellulare mediana '), Corning 1899 (' terminate Zellmasse'), Dorello 1900 (' ammasso cellulare ' or ' endodermale '), Salvi 1903, 1905 (' massa entodermica preorale ' or ' massa cellulare '), Dohrn 1905 (' chorda-entoblast'), Filatoff 1907 (' Zwischenplatte der ersten Somiten '), K. M. Parker 1917, and Adelmann 1922 (prechordal plate). The relationship of the premandibular somites to such a median cell-mass has thus been widely recognized, but Bonnet has the merit of having been the first to show that this mass is a derivative of the protochordal plate. Dr. K. M. Parker (41), in the work on early marsupial embryos already referred to, reached the same conclusion, and has given excellent figures of the mass in embryos of Perameles and Dasyurus which, following Oppel, she terms the prechordal plate. Dr. Parker's results are in general agreement with those of Bonnet except that she obtained no evidence in support of the contention that the protochordal plate furnishes chorda. In particular she has been able to demonstrate that the pre- mandibular somites, which in a number of marsupials are quite well developed (E. A. Fraser, 21), ' arise (in Perameles) from a prechordal plate which represents a derivative of the anterodorsal wall of the fore-gut, which is formed from the protochordal plate '.
In Chrysemys, Brachet (15) recognizes the protochordal, ' ou plus exactement prechordale ', plate as the narrow band of yolk-entoderm (' endoblaste vitellin ') below the anterior margin of the shield-ectoderm. When the anterior extremity of the embryo becomes delimited, part of it, he states, becomes extra-embryonal, the remainder furnishes the end-wall of the fore-gut as well as part of its floor. It does not take part in the formation of the chorda : at the most it plays a role in the constitution of the premandibular mesoderm.
The most recent contribution to our knowledge of the pro- chordal plate is the interesting paper of Adelmann (1). He has failed, however, to realize that the diffuse cellular mass in which the chorda terminates anteriorly, and which he terms the prechordal plate, is not the protochordal plate of Hubrecht but only a secondary derivative of it. He also is convinced like Brachet that neither in Squalus nor in the chick does the prechordal plate contribute to the chorda, whilst with reference to Squalus he reaches the very interesting conclusion that the portion of the prechordal mesoderm immediately anterior to the chorda gives origin not only to the premandibular but also to the anterior head-cavities, whilst its lateral and posterior portions give rise to the anterior parts of the mandibular cavities. A firm believer in the so-called ' blastopore ' theory, he concludes (p. 88) that the prechordal plate represents pre-axial mesoderm ' which is formed at the primitive dorsal or cranial lip of the blastopore '. We think, however, that the author is on surer ground when he says (p. 68), ' accepting Hubrecht's definition [of gastrulation], it follows that the material for the prechordal plate is laid down early in development during the process of gastrulation '.
In his paper on the early developmental stages of Manis, van Oordt (39) discusses at some length the question whether or not the prochordal plate contributes to the formation of the anterior end of the chorda, and though he thinks that his own observations ' certainly are a support for the view of Bonnet', he considers ' it is not proved that the anterior part of the notochord arises from i t ' (the protochordal plate), and for that reason he employs the designation ' prochordal plate ' instead of protochordal plate to indicate the area of the entoderm in question.
We follow van Oordt in this usage, since the designation prochordal plate simply signifies a particular area of entoderm which is situated in front of the primordium of the chorda (the head-process), and which precedes it in time and does not imply, as does the term protochordal plate, that it has a necessary genetic relationship to the chorda.
Our present knowledge of the prochordal plate may be summarized as follows. The prochordal plate is a localized area of entoderm which early becomes recognizable in that part of the embryonal primordium which is destined to form the anterior region of the head of the vertebrate embryo, and with which the primordium of the chorda early becomes continuous. It gives origin to the following: (a) cephalic mesenchyme, (b) part at least of the lining of the fore-gut, in particular the whole or at least part of the entoderm of the oral plate (primitive pharyngeal membrane), (c) Seessel's pocket (preoral gut-rudiment), (d) a median mass or plate of mesoderm (the so-called prechordal plate of certain authors) with which the chorda remains for a time in continuity and from which the premandibular somites take their origin.
Whether or not the plate participates, either directly or by way of the prechordal mass of mesoderm, in the formation of the anterior extremity of the chorda is a question not yet conclusively settled, though the balance of opinion appears to be against any such participation, whilst the contention of Hubrecht that it furnishes the pericardial coelom and the heart- endothelium is not in accord with what we know of the origin of these structures in other mammals. Occurring as it does in the embryos of all Vertebrates, from the Pishes to the Mammals, it is clear this prochordal plate represents a very ancient heritage of the Vertebrates, though, ap Hubrecht complained years ago, students of vertebrate morphology have largely failed to take account of its existence.
If now, finally, we proceed to inquire what is the phylogenetic significance of this remarkable patch of entoderm, we think the most fertile suggestion is that put forward in certain papers of Hubrecht. Towards the end of his monograph on cleavage and germ-layer formation in Tarsius (29, p. 80), Hubrecht, in criticizing Bonnet's substitution of the designation ' Erganzungsplatte ' for his own term, protochordal plate, makes the following statement, without further explanation or comment: ' es sich hier gar nicht um eine " Erganzung " handelt desjenigen was mehr nach hinten in der Region der Notogenesis Vorgeht, sondern umgekehrt um das primordiale, das altere Entoderm, welches direct aus dem zweiblattrigen Gastrulastadium heriiber geliefert wurde ! ' (spaced type ours).
Six years later, in his paper on the early ontogenetic phenomena in mammals (30, p. 63), he returns to the same idea, and in reproducing a figure of Legros (PI. Y, fig. 120) illustrating a longitudinal section of a late gastrular or rather post- gastrular stage of Amphioxus in which blastopore-closure is well advanced, he writes : ' In it we see the region marked pp. singled out by Legros as part of the original entoderm of the wide-mouthed gastrula, which in Amphioxus is formed—in contradistinction to all other V ertebrates—by invagination and not by delamination '. The region which Hubrecht here designates by the letters pp, signifying protochordal plate, is part of the so-called primary entoderm which is formed by the invagination of the primitive entodermal plate of the flattened or bun-shaped blastula, and which in the post-gastrular stage constitutes the antero-ventral wall of the archenteron, as contrasted with the remainder of the entoderm, the secondary entoderm so-called, which is laid down during the closure of the blastopore, as the result of the growth-activity of the blastoporic lip. As is well known through the work of Lwoff, Legros, Cerfontaine, MacBride, and others, the primary entoderm is distinguishable from the secondary not only by its position but by the fact that it is composed, at all events at first, of larger cells, richer in yolk-granules.
Now Hubrecht's view is that the protochordal plate in the Craniata is the representative of the invaginated or primary entoderm of Amphioxus, and although the germ of this interpretation occurred to him so far back as 1902 it is a remarkable fact that he not only took no pains to substantiate it but so failed to lay emphasis on it, even in his paper of 1908, that it would appear to have escaped the notice of all subsequent workers in this field. As a matter of fact, we oursslves only came across the paragraphs we have quoted above after we had written the first draft of this section, and indeed with some surprise, since one of us has for years past advocated just this very view in his lectures and had looked upon it as Jtn original On this question we are glad to find ourselves ir. complete agreement with our late friend, the illustrious Dutch embryologist. With him, we believe that the prochordal plate of the Craniate embryo is the representative of that ps,rt of the primary entoderm of the Amphioxus gastrula which bounds the anterior end of the archenteron.
It is from this region of the archenteron that tie anterior eoelomic sacs of Amphioxus take their origin, and if we accept the homology of these eoelomic sacs with the premandibular head-cavities of the Craniata, as maintained by Goodrich (22), then it necessarily follows that the entodermal areas from which they arise are also homologous.
The prochordal plate is thus an integral constituent of that most anterior region of the head which forms noi; only the extreme anterior end of the embryo but also its phylo genetically oldest part, and which has been termed by Hubrecht the cephalogenetic, and by Brachet the acrogenetic, region of the embryonic body. The prochordal plate is accordingly a structure which carries us right back to the dawn of vertebrate evolution.
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