Paper - Contributions to the embryology of the marsupialia 4-7

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Hill JP. The Early Development of the Marsupialia, with Special Reference to the Native Cat (Dasyurus Viverrinus). (1910) Quart. J. Micro. Sci. 56(1): 1-134.

  Contents: 1 Review of Previous Observations | 2 The Ovum of Dasyurus | 3 Cleavage and Blastocyst | 4 Blastocyst Growth Ectoderm Entoderm | 5 Early Stages of Perameles and Macropus | 6 Summary and Conclusions | 7 Early Mammalia Ontogeny | Explanation of Plates
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Eastern quoll
Eastern quoll
Mark Hill.jpg
This historic 1910 paper by James Peter Hill describes marsupial development in the native cat (Dasyurus Viverrinus)



Note that native cat, eastern native cat, are historic names for the eastern quoll Dasyurus Viverrinus (D. viverrinus). The eastern quoll is a medium-sized carnivorous marsupial native to Australia.

  • Dasyurus - "hairy tail"

dasyurid

Modern Notes:

Australian Animal: echidna | kangaroo | koala | platypus | possum | Category:Echidna | Category:Kangaroo | Category:Koala | Category:Platypus | Category:Possum | Category:Marsupial | Category:Monotreme | Development Timetable | K12
Historic Australian Animal  
Historic Embryology: 1834 Early Kangaroo | 1880 Platypus Cochlea | 1887 Monotremata and Marsupialia | 1910 Eastern Quoll | 1915 The Monotreme Skull | 1939 Early Echidna

The Hill Collection contains much histology of echidna and platypus embryonic development.

Embryology History | Historic Disclaimer

Other Marsupials  
Monito del Monte Development | Opossum Development
Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Chapter VII. - The Early Ontogeny of the Mammalia in the Light of the Foregoing Observations

In entering on a discussion of the bearings of the results of my study of the early development of Marsupials on current interpretations of early Mammalian ontogeny, and especially of the homologies of the germ-layers, I desire at the outset to emphasise my conviction that, specialised though the Marsupials undoubtedly are in certain features of their anatomy, e. g. their dentition, genital ducts, and mammary apparatus, the observations recorded in the preceding pages of this paper afford not the slightest ground for the supposition that their early ontogeny is also of an aberrant type, devoid of signiffcance from the point of view of that of other mammals. On the contrary, I hope to demonstrate that the Marsupial type of early development not only readily falls into line with that of Eutheria, and with what we know of the early development of the Prototheria, but furnishes ns with the key to the correct interpretation of that extraordinarily specialised developmental stage, the Eutherian blastocyst. In particular I hope to show that the description which I have been able to give of the mode of formation of the' Marsupial blastocyst, bridges in the most satisfactory fashion the great gap which has till now existed in our knowledge of the way in which the transition from the Monotrematous to the Eutherian type of development has been effected.

1. The Early Development of the Monotremata

Our knowledge of the early development of the oviparous mammals is admittedly still far from complete. Nevertheless it is not so absolutely fragmentary that it can be passed over in any general discussion of early mammalian ontogeny, and I certainly cannot agree with the opinion of Assheton ('08, p. 227) that from it “we gain very little help towards the elucidation of Eutherian development.” On the contrary, I think that the combined observations of Semon ('94), and Wilson and Hill ('07) shed most valuable light on the early ontogenetic phenomena in both the Metatheria and Eutheria. I propose therefore to give here a very brief resume of the chief results of these observers,^ and at the same time to indicate how the knowledge of early Monotreme ontogeny we possess, limited though it be, does help us to a better understanding of the phenomena to which I have just referred.

The ovum, as is well known from the observations of Caldwell. ('87), is Reptilian in its character in all but size. It is yolk-laden and telolecithal, the yolk consisting of discrete yolk-spheres, and it is enclosed outside the zona (vitelline membrane) by a layer of albumen and a definite shell.

In so doing I have largely utilised the phraseology of Wilson and Hill's paper ('07).


At the moment of entering the oviduct it has a diameter of 3‘5-4 mm. (2‘5-3 mm. according to Caldwell), and is therefore small relatively to that of a reptile of the same size as the adult Monotreme, but large relatively to those of other mammals, being about twelve times larger than that of Dasyurus, and about eighteen times larger than that of the rabbit.


Cleavage is meroblastic. The first two cleavage planes are at right angles to each other, as iii the Marsupial, and divide the germinal disc into four approximately equal-sized cells (Semon, Taf. ix, fig. 30). Each of these then becomes subdivided by a meridional furrow into two, so that an 8-celled stage is produced, the blastomeres being arranged symmetrically, or almost symmetrically, on either side of a median line, perhaps corresponding to the primary furrow (Wilson and Hill, p. 37, text-figs. 1 and 2). Imagine the yolk removed and the blastomeres arranged radially, and we have at once the open ring-shaped 8-celled stage of Dasyurus. The details of the succeeding cleavages are unknown. Semon has described a stage of about twenty-four cells (Semon, Taf. ix, fig.31),inwhich the latter formed a one-layered circular plate with no evidence of bilateral symmetry, and this is succeeded by a stage also figured by Semon (figs. 32 and 33, cf. also Wilson and Hill, PI. 2, fig. 2), in which the blastoderm has become sevei'al cells thick, though it has not yet increased in surface extent. It is bi-convex lens-shaped in section, its lower surface being sharply limited from the underlying white yolk. No nuclei are recognisable in the latter, either in this or any subsequent stage, nor is there ever any trace of a syncytial germ-wall, features in which the Monotreme egg differs from the Sauropsidan.


The next available stage, represented by an egg of Ornithorhynchus, described by Wilson and Hill ('07, p. 38, PI. 2, fig. 4), and by an egg of Echidna, described by Semon ('94, p. 69, figs. 22 and 33), is separated by a considerable gap from the preceding, and most unfortunately so, since it belongs to the period of commencing formation of the germ-layers. The cellular lens-shaped blastoderm of the preceding stage has now extended in the peripheral direction so as to enclose about the upper half of the yolk-mass, and in so doing it has assumed the form, almost exclusively, of a unilaminar thin cell-membrane, composed of flattened cells and closely applied to the inner surface of the zona. At the embryonic pole, however, in the region of the white yolk-bed, there are present in the Ornithorhynchus egg a few plump cells, immediately subjacent to the unilaminar blastoderm, but separate and distinct from it, whilst in the Echidna egg Semon's figure (fig. 33), which is perhaps somewhat schematic, shows a group of scattered cells, similar to those in the Ornithorhynchus egg but placed considei'ably deeper in the white yolk-bed. Unfortunately we have no definite evidence as to the significance of these internally situated cells. One of two possible interpretations may be assigned to them. Either they represent the last remaining deeply placed cells of the blastodisc of the preceding stage, which have not yet become intercalated in the unilaminar blastodermic membrane believed by Semon to be the condition attained in eggs of about this stage of development, or they are cells which have been proliferated off from this unilaminar blastoderm, to constitute the parent cells of the future yolk-entoderm. As regards Echidna, Semon expresses a definite enough opinion ; he holds that these deeply placed cells actually arise by a somewhat diffuse proliferation or ingrowth from a localised depressed area of the blastoderm at the embryonic pole, and that they give origin to yolk-entoderm. This interpretation of Semon seems probable enough in view of the mode of origin of the entoderm in the Metatheria and Eutheria. Moreover in the next available stage, an egg of Ornithorhynchus, just â– over 6 mm. in diameter, described by Wilson and Hill, the blastoderm is already bilaminar throughout its extent, so that we might veiy Avell expect to find the beginnings of the entoderm in the somewhat younger eggs.


In the 6 mm. egg just referred to, the peripheral portion of the utjilaminar blastoderm of the preceding stage has grown so as to enclose the entive yolk-mass in a complete ectodeimal envelope, whilst iiiteimally to that a complete lining of yolkentoderm has become established. As tlie result of these changes, and of the imbibition of fluid from the uterus, the solid yolk-laden egg has become converted into a relatively thin-walled vesicle or blastocyst, possessed of a bilaminar wall surrounding the partly fluid vitelline contents of the egg. Throughout the greater part of its extent the structure of the vesicle wall is very simple. It consists externally of an extremely attenuated ectodermal cell - membrane closely adherent to the deep surface of the vitelline membrane (zona), and within that of a layer of yolk-entoderm, composed of large swollen cells, containing each a vesicular nucleus, and a number of yolk-spheres of varying size. Over a small area, overlying the white yolk-bed, however, the ectodermal layer of the wall presents a different character to that described above. Its constituent cells are here not flattened and attenuated, but irregnlai'ly cuboidal in form and much more closely packed together; moreover they stand in proliferative continuity with a subjacent mass of cells, also in process of division. The irregular superficial layer and this latter mass together form a thickened lenticular cake, "5 mm. in greatest diameter, projecting towards the white yolk-bed but separated from it by the yolk-entoderm, which retains its character as a continuous cell-membrane. This differentiated, thickened area of the wall, situated as it is at the upper pole of the egg, as marked by the white yolk-bed, must be held to represent a part of the future embryonal region. Wilson and Hill incline to regard it as in some degree the equivalent of the “primitive plate” of Eeptiles and as the initial stage in the formation of the primitive knot of latex; eggs. This question, however, does ixot closely concern us here : the point I wish to emphasise is the relative inactivity of the cells composing the embryonal region of the blastoderm in the Monotreme as compared with the marked activity displayed by those constituting the peripheral (extra-embryonal) region of the same. It is these latter cells which by their rapid growth complete the envelopment of the yolk-mass and so constitute the lower hemisphere of the blastocyst.


Ihe bilaminar blastocyst of the Monotreme, formed in the manner indicated above, is entirely comparable with the Marsupial blastocyst of the same developmental stage. There are differences in detail certainly (e.g. in the characters, time of formation, and rate of spreading of the entoderm, in the mode of formation of the blastocyst cavity and in its contents, in the apparent absence in the Monotreme of any well-marked line of division between the embryonal aud extraembryonal regions of the ectoderm, in the relatively earlier appearance of differentiation in the embryonal region in the Monotreme as compared with the Marsupial), but the agreements are obvious and fundamental ; in particular, I would emphasise the fact that in both the embryonal region is superficial and freely exposed, and forms part of the blastocyst wall just as that of the reptile forms part of the general blastoderm. Moreover, should future observations confi^rm the view of Semon that the primitive entodermal cells of the Monotreme are proliferated off from the embryonal region of the unilaminar blastoderm, then we should be justified in directly comparing the latter with the unilaminar wall of the Marsupial blastocyst, and in regarding it also as consisting of two differentiated regions, viz. a formative or embryonal region, overlying the white yolk-bed, and giving origin to the embryonal ectoderm and the yolk-entoderm, and a nonformative region which rapidly overgrows the yolk-mass so as to eventually completely enclose it, just as does the less rapidly growing extra-embryonal ectoderm of the Sauropsidan blastoderm.^ Meantime I see no reason for doubting that this rapidly growing peripheral portion of the unilaminar blastoderm of the Monotreme is anything else than extraembryonal ectoderm homogenous with that of the reptile. Indeed, I am not aware that any embryologist except Hubrecht thinks otherwise. Even Asshetou is, I believe, content to regard the outer layer of the Monotrerae blastocyst ns ectodermal. Hubrecht's view is that the primitive eiitodermal cells of Semon give origin, not to yolk-entoderm, but to the equivalent of the embryonal knot of Eutheria, whilst the uuilaminar blastodermic membrane itself is a larval layer - the trophoblast - that portion of it overlying the internally situated cells representing the covering layer (Rauber's layer) of the Eutherian blastocyst. ‘'For this view,” remarks Assheton [^09, p. 283), “1 can see no reason derivable from actual specimens described and figured by those four authors” (Caldwell, Semon, Wilson and Hill), with which criticism I am in entire agreement, as also with the following statement, which, so far as the Metatheria are concerned, is based on my own results: “Neither in the Prototheria [n ] or the Metatheria is there really any tangible evidence of a trophoblast occui*ring as a covering layer over the definitive epiblast as in Eutheria” (p. 234).


We should further he justified in concluding that the entoderm is similar in its mode of origin in all three mammalian sub-classes.


In connection with the peripheral growth of the unilaminar blastoderm in the Monotreme, it is of interest to observe that this takes place, not apparently in intimate contact with the surface of the solid yolk, as is the case with the growing margin of the extra-embryonal ectoderm in the Saui'opsidan egg, but rather in contact with the inner surface of the thickened zona, perhaps as the result of the accumulation in the perivitelline space of tiuid which has diffused into the latter from the uterus. In other words, the peripheral growth of the extra-embryonal ectoderm to enclose the yolk-mass appears to take place here in precisely the same way as the spreading of the non-formative cells in Dasyurus to complete the lower pole of the blastocyst. In my view the latter phenomenon is none other than a recapitulation of the former ; on the other hand, I regard the spreading of the formative cells in Dasyurus towards the upper pole as a purely secondary feature, conditioned by the loss of the yolk-mass and the attainment of the holoblastic type of cleavage.


If it be admitted that the outer extra-embryonal layer of the Monotreme blastocyst is homogenous with the extra-embryonal ectoderm of the Keptile, then it seems to me there is no escape from tlie conclusion that these layers are also homogenous with the non-formative region of the unilaminar Marsupial blastocyst. I need only point out here that the chief destiny of each of the mentioned layers, and I might also add that of the outer enveloping layer of the Eutherian blastocyst (the so-called trophoblast), is one and the same, viz. to form the outer layer of the chorion (false amnion, serous membrane) and omphalopleure (unsplit yolk-sac wall. Hill ['97]),^ and that to deny their homogeny to each other implies the nou-homogeny of these membranes and the amnion in the Amniotan series, and consequently renders the group name Amniota void of all moi'phological meaning.


The rapidity with which the enclosure of the yolk-mass is effected, and the relative tardiness of differentiation in the embryonal region are features Avhich sharply distinguish the early ontogeny of the Monotremes from that of the Sauropsida, and which, in my view, are of the very greatest importance, since they afford the key to a correct understanding of the peculiar coenogeuetic modifications observable in the early ontogeny of the Metatheria and Eutheria. To appreciate the significance of these featui-es it is necessary to take account of the great difference which exists between the Sauropsidan and Monotreme ovum in regard to size, as Avell as of the very different conditions under Avhich the early development goes on in the two groups. The Sauropsidan egg is large enough to contain Avithin its OAvn confines the amount of yolk necessary for the production of a young one complete in all its parts and capable of leading an independent existence immediately it leaves the shell. Furthermore, it is also large enough to provide room for tlie development of an embryo without any secondary growth in size after it leaves the ovary. Moreover we have to remember that after it has become enclosed in the shelly it remains but a short time in the oviduct and receives little or no additional nutrient material from the oviducal walls. The yolk-mass in any case retains its solid character; there is no necessity for its rapid enclosure, and so enclosure is effected slowly, contemporaneously with the differentiation of the embryo.


In certain Ainniotes the layers in question appear also to participate in the formation of the inner lining of the amnion (amniotic ectoderm) (cf . Assheton ['09], pp. 248-9), but this does not affect the statement in the text. In the Saxu'opsida and Monotremata I think I am coia-ect in saying that no sharp distinction is recognisable between the embi'yonal and extra-embryonal regions of the ectoderm, hence it is difficult, if not imj)ossible, to determine with certainty their relative participation in the formation of the amniotic ectoderm.


In the Monotreme the conditions are altogether different. The ripe ovarian ovum when it enters the oviduct has a diameter of about 3-5 to 4 mm., and is thns considerably smaller than that of a Eeptile of the same size as the adult Monotreme. The amount of yolk which it is capable of containing is not anything like sufficient to last the embryo throughout the developmental period, and, moreover, it does not provide the space essential for the development of an embryo on the ancestral Reptilian lines. As Assheton ('98, p. 251) has pointed out, “ the difference in size between the fertilised ovum of a reptile or bird or of a mammal is very great ; but the difference in size between the embryo of, say, a bird with one pair of mesoblastic somites and of a mammal of the same age is comparatively small. This means that nearly the same space is required for the production of the mammalian embryo as of the Sauropsidan, and has to be provided.” In the Monotreme not only is additional room necessary, but also additional nutrient material, sufficient with that already present in the egg to last the embryo throughout the period of incubation. Both are acquired contemporaneously during the sojourn of the egg in the uterine portion of the oviduct, wherein the egg increases greatly in size. When it enters the uterus, the Monotreme egg has a diameter, inclusive of its membranes, of about 4-5 mm. ; when it is laid, it measures in Ornithorhynchus, in its greatest diameter, 16-19 mm., and somewhat less in the case of Echidna. Prior to the enclosure of the yolk the increase in diameter, due to the accumulation of fluid in the perivitelliue space and between the zona and shell, is but slight. But as soon as the yolk becomes suiTonnded by a complete cellular membrane, i.e. as soon as the egg has become converted into a thin-walled blastocyst, rapid growth sets in, accompanied by the active imbibition of the nutrient fluid, which is poured into the uterine lumen as the result of the secretory activity of the abundantly developed uterine glands. The fluid absorbed not only keeps the blastocyst turgid, but it brings about the more or less complete disintegration of the yolk-mass, its constituent spherules becoming disseminated in the fluid contents of the blastocyst cavity. Although a distinct and continuous subgerminal cavity, such as appears beneath the embryonal region of the Sauropsidan blastoderm, does not occur in the Monotreme egg, vacuolar spaces filled with fluid develop in the white yolk-bed underlying the site of the germinal disc and appear to represent it. As Wilson and Hill remark ('03, p. 317), “ one can, without hesitation, homologise the interior of the vesicle with the subgerminal cavity of a Saui'opsidan egg, extended so as to include by liquefaction the whole of the yolk itself.” In the Marsupial the blastocyst cavity has a quite different origin, since it represents the persistent segmentation cavity, whilst in the Eutheria the same cavity is secondarily formed by the confluence of intra- or intei*-cellular vacuolar spaces, but no one, so far as I know, has ever v^entured to assert that, because of this difference in mode of origin, the blastocyst cavity in the series of the Mammalia is a nonhomogenous formation.


To return to the matter under discussion, it appeal's to me that the necessity which has arisen, consequent on the I'eduction in size of the ovum, for rapid growth of the same in order to provide room for the development of an embryo and for the storage of nutrient material furnished by the maternal uterus, affords a satisfactory explanation of the much more marked activity of the extra-embryonal I'egion of the blastoderm as compared with the embryonal, Avhich is such a striking feature in the early ontogeny of the Monotremes, and not only of them, but, as Assheton has pointed out ('98, p. 251), of the higher mammals as well (cf. the process of epiboly and the inertness at first displayed by the formative cells of the embryonal knot as compared with the activity of the nonformative or tropho-ectodermal cells), an activity which results in the rapid completion of that characteristically mammalian developmental stage - the blastocyst or blastodermic vesicle.


The necessity for the early formation of such a stage, capable of rapidly growing in a nutrient fluid medium provided by the mother, has profoundly influenced the early ontogeny in all three mammalian subclasses, and natui*ally most of all that of the Eutheria, in which reduction of the ovum, both as regards size and secondary envelopes, has reached the maximum. And I think there can be little doubt but that it is this necessity which has induced that early separation of the blastomeres into two categories, respectively formative and non-formative in significance, which has long been recognised as occurring in Eutheria, and which I have shown also occurs amongst the Metatheria. This early separation of the blastomeres into two distinct groups is not recognisable in the Sauropsida, and the idea that it is in some way connected with the loss of yolk which the mammalian ovum has suffered in the course ofphylogeny, was first put forward, I believe, by Jenkinson. In his paper on the germinal layers of Vertebrata ('06, p. 51) he writes: “ Segmentation therefore is followed in the Placentalia by the separation of the elements of the trophoblast from those destined to give rise to the embryo and the remainder of its foetal membranes, and this ^precocious segregation' seems to have occurred phylogenetically during the gradual loss of yolk which the egg of these mammals has undergone.” Whether or not such a precocious segregation ” has already become fixed in the Monotremes,future investigation must decide (cf . ante, p.90).


Ihe loss of yolk, with resulting reduction in size which the Monotreme ovum has suffered in the course of phylogeny, we must assume to have taken place gi-adually and in correlation with the longer retention of the egg in the oviduct, the elaboration of the uterine portion of the same as an actively secretory organ, and the evolution of the mammary apparatus. The Monotremes thus render concrete to us one of the first great steps in mammalian evolution so far as developmental processes are concerned, viz. the substitution for intra-ovular yolk of nutrient material furnished directly by the mother to the developing egg or embryo. We see in them the beginnings of that process of substitution of uterine for ovarian nutriment which reaches its culmination in the Eutheria with their microscopic yolk-poor ova and long intra-uterine period of development. The Marsupials show us in Dasyurus an interesting intervening stage so far as the ovum is concerned, in that this, though greatly reduced as compared with that of the Monotreme, still retains somewhat of its old tendencies and elaborates more yolk-material than it can conveniently utilise, with the result that it has to eliminate the surplus before cleavage begins. But as coucerns their utilisation of intra-uterine nutriment, they have specialised along their own lines, and instead of exhausting the possibilities implied by the presence of that, they have extensively elaborated the mammary apparatus for the nutrition of the young, born in a relatively immature state, after a short period of intrauterine life (cf. Wilson and Hill [T7, p. 580]).


In view of the fact that the young Monotreme enjoys three developmental periods, viz. intra-uterine, incubatory, and lactatory, the question might be worthy of consideration whether it may not be that the Marsupial has merged the incubatory period in the lactatory, the Eutherian the same in the intra-uterine.


2. The Early Development of the Metatheria and Eutheria

It will have become evident Horn the foregoing that the Metatherian mode of early development is to be regarded as but a slightly modified version of the Prototherian, such differences as exist between them being interpretable as coenogeuetic modifications, induced in the Metatherian by the practically complete substitution of uterine nutriment for intra-ovular yolk, a substitution which has resulted in the attainment by the marsupial ovum of the holoblastic type of cleavage. In tlie present section I hope to demonstrate how the early ontogeny of the Metatlieria enables us to interpret that of the Eutheria in terms of that of the Prototheria.

If we proceed to compare the early development in the Metatlieria and Eutheria, we encounter, from the 4-celled stage onwards, such obvious and profound differences in the mode of formation of the blastocyst, and in the relations of its constituent parts, that the differences seem at first sight to far outweigh the resemblances. Nevertheless, apart from their common possession of the same holoblastic mode of cleavage, there exists one most striking and fundamental agreement between the two in the fact that in both there occurs, sooner or later during the cleavage process, a separation of the blastomeres into two distinct, pre-determined cellgroups, whose individual destinies are very different, but apparently identical in the two subclasses. In tlie Marsupial, as typified by Dasyurus, the fourth cleavages are, as we have seen, unequal and qualitative, and result in the separation of two differentiated groups of blastomeres, arranged in two superimposed rings, viz. an upper ring of eight smaller, less yolk-rich cells, and a lower of eight larger, more yolk-iuch cells. The evidence justifies the conclusion that the former gives origin directly to the formative or embryonal region of the vesicle wall, the latter to tlie non-formative or extraembryonal region.


Amongst the Eutheria the evidence is no less clear. It has been conclusively shown by various observers (Van Beneden, Duval, Assheton, Hubrecht, Heape, and others) that, sooner or later, there occui's a separation of the blastomeres into two distinct groups, one of which eventually encloses the other completely. The two groups may be clearly distinguishable


Diagrams illustrating the mode of formation of the blastocyst in Metatheria (a-d) and Eutheria (1-3). b.c. Blastocyst cavity. i.c.m. Inner cell-mass, 'pr.amn.c. Primitive amniotic cavity. r.l. Rauber's layer. s.c. Segmentation cavity. For other reference letters see explanation of plates (p. 125).


in early cleavage stages, owing to diffecences in the characters and staining reactions of their cells, and in such cases there is definite evidence of the occurrence of a process of overgrowth or epiboly, whereby one group gradually grows round and completely envelops the other, so that in the completed morula a distinction may be drawn between a central cellmass and a peripheral or enveloping layer (rabbit. Van Beneden; sheep, Assheton). In other cases, where it has been impossible to recognise the existence of these two distinct cell-groups in the cleavage stages, we nevertheless find, either in the completed moimla or in the blastocyst, that a more or less sharp distinction may be drawn between an enveloping layer of cells and an internally situated cell-mass (inner cell-mass).


E. van Beneden, in his classical paper on the development of the rabbit, published in 1875, was the first to recognise definitely the existence of two categories of cells in the segmenting egg of the Eutherian mammal. In this form he showed how in the morula stage a cap of lighter blastomeres gradually grows round and envelops a mass of more opaque cells by a process of overgrowth or epiboly. In his more recent and extremely valuable paper on the development of Yespertilio ('99), he again demonstrated the existence of two groups of blastomeres as well in the segmenting egg as in the completed morula, but failed to find evidence of epiboly in all cases. Nevertheless he holds fast to the opinion which he expressed in 1875 : “ Que la segmentation s'accompagne, chez les Mammiferes placentaires, d'un enveloppement progressif d'une partie des blastomeres par une couche cellulaire, qui commence a se differencier des le debut du developpement,” and states that “dans tons les oeufs arrives a la fin de la segmentation et dans ceux qui moutraient le debut de la cavite Blastodermique j'ai constamment rencontre une couche peripherique complete, eutourant de toutes parts un amas cellulaire interne, bien separe de la couche enveloppante.” The latter layer he regards as corresponding to the extraembryonal ectoderm of the Sauropsida, and points out that âsschertons les Choi'des les premiers blastomeres qui se differencient et qui avoisinent le pole animal de I'oeuf sont des elements epiblastiqnes. C'est par la couolie cellulaire qui resulte de la segmentation ulterieure de ces premiers blastomeres epiblastiqnes que se fait, cbez les Sauropsides, benveloppement du vitellus. Dans Toeuf reduit a n'etre plus qu'une sphere microscopiquej bepibolie a pu s'achever des la fin de la segmentation, voire meme avant bachevement de ce phenomene.” The “ amas cellulaire interne ” (embryonal knot, inner cell mass). Van Beneden shows, differentiates secondarily into “ un lecithophore et un bouton embryonnaire. The former is the entoderm of other authors, the latter the formative or embryonal ectoderm. Hubrecht, in the forms studied by him (Sorex, 'I'upaia, Tarsius^) finds a corresponding differentiation. In Tupaia he describes the morula stage as consisting of a single central lightly staining cell, which he regards as the parent cell of the inner cell-mass of later stages, and of a more darkly staining peripheral layer which forms the unilaminar wall of the blastocyst. Here, then, the parent cells of the two cell-groups would appear to be separated at the first cleavage. Hubrecht, like Van Beneden, holds that the inner cell-mass furnishes the embryonal ectoderm and the entire entoderm of the blastocyst. The peripheral layer he has termed the trophoblast ('88, p. 511), and in his paper on the placentation of the hedgehog ('89, p. 298) he defines the term as follows: “I propose to confer this name to the epiblast of the blastocyst as far as it has a dix'ect nutritive significance, as indicated by proliferating processes, by immediate contact with maternal tissue, maternal blood, or secreted material. The epiblast of the germinal ai-ea - the formative epiblast - aud that which will take part in the formation of the inner lining of the amnion cavity is, ipso facto, excluded from the definition. Thus the name trophoblast was originally employed by Hubrecbt as a convenient term designatory of what he at the time regarded as the extra-embryonal ectoderm of the mammalian blastocyst. In the course of his speculations on the oingin of this layer, however, he has reached the conclusion that it is really of the nature oP'a larval envelope, an Embryonalhiille (^08, p. 15), inherited by the mammals, not from the reptiles (which have no direct phylogenetic I'elationship to the latter), but from their remote invertebrate ancestors ('Vermiform pi'edecessors of coelenterate pedigree, provided with an ectodermal larval investment [Laiwenhiille] ”).


In Erinacens the entoderm, from Hubrecht's observations, appears to be precociously differentiated, prior to the separation of the embryonal ectoderm fi'om the overlying trophoblast, but the details of the early development in this form are as yet only incompletely known.


Assheton, again, although he was unable to convince himself ('94) of the correctness of van Beneden's account of the occurrence of a process of epiboly in the segmenting eggs of the rabbit, finds in the sheep ('98) that a differentiation into two groups of cells is recognisable “ perhaps as early as the eight segment stage,” and that one of the groups gradually envelops the other. “Let it be noted,” he writes ('98, p. 227), “ that we have now to face the fact, based on actual sections, that there is in certain mammals a clear separation of segments at an early stage into two groups, one of which eventually completely surrounds the other,” and instances Van Beneden's observations on the rabbit (of the correctness of which he, however, failed to satisfy himself, as noted above), Duval's observations on the bat, Hubrecht's on Tupaia, and his own on the sheep. Assheton thinks this phenomenon “ must surely have some most profound significance,” but finds himself unable to accept the interpretations of either Van Beueden or Hubrecht, and puts forward yet another view, “ based on the appearance of some segmenting eggs of the sheep ” ('08, p. 233), “that in cases where this differentiation does clearly occur, it is a division into epiblast and hypoblast, the latter being the external layer” ('98, p. 227). Assheton thus differs from all other observers in holding that the inner cell-mass or embryonal knot of the Eutherian blastocyst gives origin solely to the formative or embryonal ectoderm, and I believe 1 am correct in stating that he also differs from all other observers in holding that the outer enveloping layer of the same is entodermald


The fact, then, of the occurrence amongst Eutheria of a “precocious segregation ” of the blastomeres into two distinct groups, one of which eventually surrounds the other completely, is not in dispute, though authorities differ widely in the intei'pretation they place upon it. In the Eutherian blastocyst stage, the enveloping layer forms the outer unilaminar wall of the vesicle, and encloses the blastocyst cavity as well as the other internally situated group. This latter typically appears as a rounded cell-mass, attached ac one spot to the inner surface of tlie enveloping layer, but more or less distinctly marked off from it. It is genei-ally termed the inner cell-mass or embryonal knoc (“ amas cellulaire interne ” of Van Beneden). For the enveloping layer Ilubrecht's name of “ trophoblast ” is now generally employed, even by those who refuse to adopt the speculative views with which its originator has most unfortunately, as I think, enshrouded this convenient term.


I have demonstrated the occurrence of an apparently comparable “precocious segregation^^ of the blastomeres into two distinct groups in one member of the Metatheria which there is no reason to regard as an abeirant type, and I have shown beyond all shadow of doubt that from the one group, which constitutes what I have termed the formative region of the unilaminar vesicle-wall, there arise the embi*youal ectoderm and the entire entoderm of the vesicle, both embryonal and extra-embryonal, and that the other group, which constitutes the non-formative region of the vesicle-wall, directly furnishes the extra-embryonal ectoderm, i.e. the ectoderm of the omphalopleui'e and chorion."


Assheton states ('08, p. 233, cf. also '98, p. 220) that his interpretation “ owes ranch also to the theoretical conclusions of Minot and Robinson.” However that may be, both Minot and Robinson in their most recent writings continue to speak of the chorionic ectoderm.

^ Whether or not it participates in the formation of the ainniotic ectoderm future investigation must decide.


As resrards Eutheria, we have seen that Van Beneden and Hubrecht, though their views in otlier respects are widely divero-ent, both ag'ree that the inner cell-mass of the blastocyst furnishes the embryonal ectoderm (as well as the amniotic ectoderm wholly or in part) and the entire entoderm of the vesicle. That, in fact, is the view of Mammalian embryologists generally (Duval and Assheton excepted),^ and if we may assume it to be correct, then it would appear that the later history of the formative region of the Marsupial blastocyst and that of the inner cell-mass of the Eutherian are identical. That being so, and bearing in mind that both have been shown, at all events in certain Mammals, to have an identical origin as a group of precociously segregated blastotneres,^ I can come to no other conclusion than that they are homogenous formations. If that be accepted, then this fact by itself renders highly probable the view that the so-called trophoblast of the Eutherian blastocyst is homogenous with the non-formative region of the Metatherian vesicle, and v?hen we reflect that both have precisely the same structural and topographical (not to mention functional) relations in later stages, inasmuch as they constitute the ectoderm of the chorion and omphalopleure (with or without participation in the formation of the amniotic ectoderm;, and that both have a similar origin in those Mammals in which a precocious segregation of the blastomeres has been recognised, their exact

The view of Duval ['95], based on the study of Vespertilio, that the inner cell-mass gives rise solely to entoderm, and that the enveloping layer furnishes not only the extra-embryonal but also the embryonal ectoderm, is shown by Van Beneden's observations on the same form to be devoid of any basis of fact. Assheton's views are referred to below (p. 110).

The fact that the phenomenon of the “ precocious segregation” of the blastomeres into two groups with deteiminate destinies has already become fixed in tlie Marsupial lends additional weight to the view of Van Beneden that such a segregation will eventually be recognised as occurring in all Eutheria without exception. Without it, it is difficult to understand how the entypic condition, characteristic of the blastocysts of Ml known Eutheria, is attained, imless by differentiation in situ, which .seems to me highly improbable.


homology need no longer be doubted. In the preceding section of this paper (ante, pp. 91, 92) I have shown reason for the conclusion that the non-formative region of the Marsupial blastocyst is the homologue of the extra-embryonal ectoderm of the Monotreme and Reptile, and if that conclusion be accepted it follows that the outer enveloping layer of the Eutherian blastocyst, the so-called trophoblast of Hubrecht, is none other than extra-embryonal ectoderm, as maintained by Van Beneden, Keibel, Bonnet, Jenkinson, Lee, MacBride and others, the homologue of that of Reptilia.


I am therefore wholly unable to accept the highly speculative conclusions of Hubrecht, set forth with such brilliancy in a comparatively recent number of this Journal ('08), as to the significance and phylogeny of this layer. These conclusions, on the basis of which he has proceeded to formulate such far-reaching and, indeed, revolutionary ideas not only on questions embryological, but on those pertaining to the phylogeny and classification of vertebrates, have already been critically considered by Assheton ('09) and MacBride ('09), also in the pages of this Journal, and found wanting, and they are, to my mind, quite irreconcilable with the facts I have brought to light in regard to the early development of Marsupials. I yield to no one in my admiration for the epoch-making work of Hubrecht on the early ontogeny and placentation of the Mammalia, and I heartily associate myself with the eulogium thereanent so admirably expressed by Assheton in the cx'itique just referred to (p. 274), but I am bound to confess that as concerns his views on the phylogeny of this layer, which he has termed the “ trophoblast,” he seems to me to have forsaken the fertile field of legitimate hypothesis for the barren waste of unprofitable speculation, and to have erected therein an imposing edifice on the very slenderest of foundations.


Before I proceed to justify this, my estimate of Hubrecht's views on the phylogeny of the trophoblast, let me first set forth his conception so far as I understand it. He starts with the assumption that the vertebrates (with the exception of Ainpliioxus, the CyclostoineSj and the Elasraobi'anclif!) are descended from “vermiform predecessors of coelenterate pedigree” possessed of free-swimming larvte, in which there was present a complete larval membi'ane of ectodermal derivation, and of the same order of differentiation “as the outer larval layer which in certain Nemertines, Gephyreans, and other worms often serves as a temporaiy envelope that is stripped off when the animal attains to a certain stage of development.” When, for oviparity and larval development, viviparity and embryonic development became established in the Protetrapodous successors of the ancestral vermiform stock, the larval membrane did not disappear. On the contrary, it is assumed that it merely changed “its protective or locomotor function into an adhesive one,” and so, development now taking place in utero, it is quite easy to understand how tlie larval membrane could gradually become transformed into a trophic vesicle, containing the embryo as before, and functional in the reception of nutriment from the walls of the maternal uterus. The final stages in the evolution of this trophic vesicle constituted by the old larval membrane are met with amongst the mammals, since in them it became vascularised so as to constitute a “yet more thorough system of nourishment at the expense of the maternal circulatory system.” Such, then, is the phylogeny of the trophoblast according to Hubrecht. The Eutheriau mammals, which it is held trace their descent straight back to some very early Protetrapodous stock, viviparous in habit and with small yolk-poor, holoblastic eggs, exhibit the trophoblast in its most perfect condition. Hubrecht therefore starts with them, and attempts to demonsti'ate the existence of a larval membrane, or remnants of such, externally to the embryonal ectoderm in all vertebrates with the exceptions already mentioned. There is no question of its existence in the Meta- and Eutherian mammals. “We may,” writes Hubrecht ('08, p. 12), . . . “insist upon the fact that . . . all Didelphia and Monodelphia hitherto investi gated show at a very early moment the didermic stage out of which the embryo will be built up enclosed in a cellular vesicle (the troplioblast), of which no pai‘t ever enters into the embryonic organisation.” The common possession by the Metatheria and Eutheria of a larval membi'ane is after all only what might be expected, “since after Hill's ('97) investigations, we must assume that the didelphian mammals are not descended from Ornithodelphia but from monodelphian placental ancestors.” As concerns the Prototheria, although they cannot in any sense be regarded as directly ancestral to the other mammals, we nevertheless find the trophoblastic vesicle “ compax'atively distinct.” “In many reptiles and birds,” however, it is “.distinguished with great diflSculty from the embryonic shield,” and this is explained bv the fact that the Sauropsida which are assumed to have taken their origin from the same Protetrapodous stock as the mammals but along an entirely independent line, have secondarily acquired, like the Prototheria, the oviparous habit, with its concomitants, a yolk-laden egg and a shell, and this latter acquisition has naturally tended “to relegate any outer larval layer to the pension list” ('09, p. 5). “Concerning the yolk accumulation in the Sauropsidan egg, there is no trouble at all to suppose that the vesicular blastocyst of an early vivipai-ous ancestor had gradually become yolkladen. The contrary assumption, found in the handbooks, that the mammalian egg, while totally losing its yolk, has yet preserved the identical developmental featui-es as the Sauropsid, is in ideality much more difiicult to reconcile with sound evolutionary principles” ('09, p. 5).


Amongst the lower Vertebrates the larval membrane is clearly enough recognisable in the so-called Deckschicht of the Teleostomes, Dipnoans, and Amphibians. It is frankly admitted that Amphioxus, the Cyclostomes, and the Elasmobranchs “ show in their early development no traces of a Deckschicht” (larval layer, troiDhoblast), but there is no difficulty about this, since it is easy enough to suppose, in view of other characters, that “ the Selachians may very well have descended from ancestors without any outer larval layer {'08, p. 151), and ‘'for Cyclostomes tlie same reasoning holds good” (p. 152).


The trophoblast, then, is conceived of by Hubrecht as a larval membrane of ectodermal derivation, which invests the embryonal ahlage in all Vertebrates with the exceptions mentioned, 'which is subject to secondary reduction, and which is homologous throughout the series. As I understand the conception, what is ordinarily called extra-embryonal ectoderm in the Sauropsida is not trophoblast, otherwise Hubrecht could hardly write - “in reptiles and birds traces of the larval layer have in late years been unmistakably noticed” ('09, p. 5) ; nevertheless what other writers have termed embryonal and extra-embryonal ectoderm in the Prototheria is claimed by Hubrecht as trophoblast (at all events that is my interpretation of his statement that a trophoblastic vesicle is present in these forms), and yet some years ago Hubrecht ('04, p. 10) found it diflBcult “ to understand that the name has been misunderstood both by embryologists and gynecologists.” My own feeling is that the more recent developments in his views have tended to obscure rather than to clarify our ideas as to the trophoblast, especially if we must now hold that the chorion or serosa of the Sauropsida is not homologous with that of the Prototheria, which necessarily follows if the extra-embi'yonal ectoderm of the Sauropsidan is not the same thing as that of the Monotreme.


Assuming that we have formed a correct conception of the trophoblast as a larval membrane, and bearing in mind that it is best developed in the Metatheria and Eutheria, since these alone amongst higher Vertebrates have retained unaltered the viviparous habits of their Protetrapodous ancestors, let us see what basis in fact there is for the statement of Hubrecht ('08, p. 68) that “before the ectoderm and the entoderm have become differentiated from each other there is in mammals a distinct larval cell-layer surrounding (as soon as cleavage of the egg has attained the morula stage) the mother-cells of the embryonic tissues.” Now that statement as it stands, I have no hesitation in characterising as entirely misleading, inasmuch as it is applicable not to the Mammalia as a whole, but, so far as it refers to matters of undisputed fact, to one only of the three mammalian subclasses, viz. the Eutheria. So far as the latter ai'e concerned, practically all observers, as we have seen, are agreed that there is present during at least the early stages of development a complete outer layer of cells which encloses the embryonal anlage or inner cell-mass (that portion of it immediately overlying the latter being termed the “ Deckschicht ” or “Rauber's layer”). It is, of course, this envelojDing layer or trophoblast which Hubrecht interprets as a larval membrane. It fulfils the conditions, and were the Eutheria the only Vertebrates known to us, the idea might be plausible enough.


Turning now to the Metatheria, and I'emembering that these, according to Hubrecht, are descended from the Eutheria, we should naturally expect to find the supposed larval membrane fully developed, with all its ancestral relations ; and so we do if we are content to accept Hubrecht's interpretation of Selenka's results and figures in the case of Didelphys. The “ urentodermzelle ” of Selenka is for Hubrecht “ undoubtedly the mother-cell of the embryonic knob,” the ectoderm of Selenka is manifestly the trophoblast - a complete larval layer. It is no doubt unfortunate that Hubrecht had to rely on the work of Selenka as his source of information on the early development of Marsupials, but it must be remembered that he reads his own views into Selenka's figures. On the basis of my own observations on the early ontogeny of Marsupials, I have no hesitation in affirming that a larval membrane, in the sense of Hubrecht, does not exist in any of the forms (Dasyurus, Perameles, Macropus) studied by me. The observations recorded in the preceding pages of this paper demonstrate, in the case of Dasyurus without the possibility of doubt, the entire absence of any cellular layer external to the formative region of the blastocyst, i.e. in a position corresponding to that occupied by Rauber's layer in Eutheria, whilst in the case of Perameles and Macropus, they yield not the slightest evidence for the existence of any such layer. The formative region of the Marsupial blastocyst, which is undoubtedly the homologue of the inner cell mass of the Eutheria, forms from the first part of the unilarninar blastocyst wall, and is freely exposed. The remainder of the latter is constituted by a layer of non-formative cells, the destiny of which is the same as that of the so-called trophoblast of the Eutheria. I have therefore ventui'ed to suggest that they are one and the same. If, then, the trophoblast is really a larval membrane, we must assume, in the case of the Marsupial, either that its “ Deckschicht portion has been completely suppressed (but why it should have been I fail to understand, unless, perhaps, it is a result of the secondary acquisition by the Marsupials of a shell-membrane, these mammals being even now on the, way to secondarily assume the oviparous habit !), or that the non-formative region of the Marsupials is not the homologue of the trophoblast, in which case the Marsupials must be held to have entirely lost the larval membrane, since there is no other layer present which could possibly represent it. These considerations may well give us pause before we calmly accept Hubrecht's conception of the trophoblast as a larval membrane present in all mammals without exception.


Coming now to the Prototheria, we find, according to Hubrecht, the trophoblastic vesicle . . . yet compara tively distinct,” and so it is if we accept the interpretation of Hubrecht of the observations and figures of Semon, Wilson and Hill. The unilarninar blastoderm of these authors is unmistakably the trophoblast. The cells situated internally to that in the region of the white yolk-bed are not entodertnal, as suggested by Semon, but constitute for Hubrecht “ the mother cells of the embryonic knob.” I need only quote again the opinion of Assheton thereanent and express my agreement therewith; he writes (^09, p. 233) : For this view


I can see no reason derivable from actual specimens described and figured by those four authors” (Caldwell, Semon, Wilson and Hill). It would appear, then, that the assumption of Hubreclit of the presence of a larval membrane of the nature postulated in the Prototheria and Metatheria is devoid of foundation in fact, so that there but remains the question of the significance of the outer enveloping layer of the Eutherian blastocyst. As regards that, I venture to think that the alternative interpretation of E. van Beneden and other investigators, which I have attempted to develop in the pages of this paper, affords a simpler and more satisfying explanation of its significance and phylogeny than that advocated by Prof. Hubrecht, an interpretation, moreover, which is more in accordance, not only with all the known facts, but with sound evolutionary principles and with the conclusions arrived at by the great majority of comparative anatomists and palaeontologists as to the origin and intei-relationships of the Mammalia.


And I also venture to think that what has just been said holds true with reference to the views advocated by Mr. Assheton. These views owed their origin to certain appearances which he found in some segmenting ova of the sheep (but, be it noted, not in all those he examined), and he has attempted to re-intei pret not only his own earlier observations, but those of other workers on the early ontogeny of the Eutheria in the light of his newer faith, and not only so, he holds that it is also possible to apply that in the interpretation of the early ontogeny of Marsupials (v. '08, p. 235, and '09, p. 229). He maintains that the inner cell-mass of Eutheria is purely ectodermal, aud that the enveloping trophoblast layer of the blastocyst arises in common with the entodermal lining of the same and is therefore also entodei'mal. " On the theory I advocate,” he writes ('09, p. 235), " the trophoblast is of Eutherian mammalian origin only and is not homologous to any form of envelope outside the group of Eutherian mammals.” These views of Assheton are not only at variance with those of all other investigators who have worked at the early ontogeny of Eutheria, but they are quite irreconcilable with my observations on the development of Dasyurus herein recorded. I claim to have shown in that Marsupial that the formative region, the homologue of the inner cell-mass, gives origin not only to the embryonal ectoderm, but to the entire entoderm, whilst tlie non-formative region, whose homology to the trophoblast of Eutheria is admitted by Assheton, arises quite independently of the entoderm and a long time before the latter inakes its appearance. There is, then, in Dasyurus no question of a common origin of the entoderm and the non-forrnative or trophoblastic region of the blastocyst wall. And exception inay be taken to Assheton's views on quite other grounds (e. g. the question of the homologies of the foetal membranes in the series of the Amniota), as he himself is well awai'e, and as Jenkinson ('00) has also emphasised. I feel, however, I can leave further discussion of Assheton's views until such time as my observations on Dasyurus are shown to be erroneous or inapplicable to other Marsupials.

3. The Entypic Condition of the Eutherian Blastocyst

If, now, on the basis of the homologies I have ventm-ed to advocate in the preceding pages, we proceed to compare the Metatherian with the Eutherian blastocyst, we have to note that, whereas in the latter the extra-embryonal or trophoblastic ectoderm alone forms the blastocyst wall in early stages and completely encloses the embryonal knot, in the former, the homologous parts, viz. the non-formative or exti'aembryonal and the formative or embryonal regions, both enter into the constitution of the unilaminar blastocyst wall, there being no such enclosure of the one by the other as occurs in the Eutherian blastocy.st (Text-fig. 2, p. 98). It is characteristic of the Marsupial as of the Monotreme that the embryonal region is from the first superficial and freely exposed. It is spread out as a cellular layer and simply forms part of the blastocyst wall or blastoderm. It is equally characteristic of the Eutherian that the homologous part, the embryonal knot, has at first the form of a compact mass, which is completely enclosed by the trophoblastic ectoderm.


The latter alone constitutes the unilaminar wall of the blastocyst and has the embryonal knot adherent at one spot to its inner surface. The formative cells which compose the knot thus take at first no part in the constitution of the outei wall of the blastocyst^ and may or may not do so in later stages according as the covering layer of the trophoblast (the Deckschicht or Rauber's layer) is transitory or permanent. This peculiar developmental condition, characterised by the internal position of the formative or embryonal cells within the blastocyst cavity, has been termed by Selenka (TO) “entypy” (Entypie des Keimfeldes).^ It is a phenomenon exclusively found in the Eutheria and characteristic of them alone, amongst the mammals. In the Marsupial, as in the Monotreme, the formative cells are freely exposed, and constitute from the first part of the blastocyst wall just as those of the Sauropsida form a part of the general blastoderm. Limited as entypy thus appears to be to the higher mammals, the probability is that we have to do here with a purely secondary, adaptive feature.


If we proceed to inquire what is the significance of this remarkable difference in the early developmental phenomena of the lower and higher mammals, it seems to me that we have to take account, in the first place, of the differences in the structure of their respective eggs, and especially we have to bear in mind that the Eutherian ovum is considerably more specialised than even the Metatherian. It is on the average smaller than the latter, i.e. it has suffered in the course of phytogeny still further reduction in size, and has lost, to an even greater extent than the Marsupial ovum, the store of foodyolk ancestrally present in it. Moreover, it has suffered a still further i-eduction in respect of its secondary egg-membranes. The Metatherian ovum still retains in its shell-membrane a vestigial representative of the shell of the presumed oviparous common ancestor of the Metatheria and Eutheria. The Eutherian ovum, on the other hand, has lost all trace of the shell in correlation with its more complete adaptation to the conditions of intra-nterine development. The albumen layer is variable in its occurrence, being present in some (e.g. rabbit) and absent in others (e.g. pig, Assheton), whilst the zona itself, though always present, is variable both as to its thickness and the length of time it persists.


^ “ Unter Entypie des Keimfeldes mdcbte ich dalier verstanden wissen : Die nicht dm-cli Bildung typischer Anmionfalten geschehende, sondern durcli eine schon wiihrend der Gastrulation erfolgende Absclinurung des Keimfeldes ins Innere der Eiblasenbnlle (Oborion) ” ('00, p. 203).


Strangely enough, although the prevaling opinion amongst mammalian embryologists is that the Eutherian ovum has been derived phylogenetically from an egg of the same telolecithal and shell-bearing type as is found in the Monotremes, no one, so far as I am aware, has ever taken the shell into account, and ventured to consider in what way its total disappearance from an ovum already greatly reduced in size, might affect the course of the early developmental phenomena. That is what I propose to do here, for iu my view it is just in the complete loss of the shell by the Eutherian ovum that we find the key to the explanation of those remarkable differences which are observable between the early ontogeny of the Eutheria and Metatheria, and which culminate in the entypic condition so distinctive of the former. The acquisition of a shell by the Proamniota conditioned the appearance of the amnion. The loss of the shell in the Eutheria conditioned the occui'rence in their ontogeny of entypy.

As we have seen, the mammalian ovum, already in the Monotremes greatly reduced iu size as compared with that of reptiles, and quite minute in the Metatheria and Eutheria, contains within itself neither the cubic capacity nor the food material necessary for the production of an embryo on the ancestral reptilian lines. We accordingly find that the primary object of the first developmeutal processes in the mammals has come to be the formation of a vesicle with a complete cellular wall, capable of absorbing nutrient fluid from the maternal uterus and of growing I'apidly, so as to provide the space necessary for embryonal differentiation.


In the Monotremes this vesiculai' stage is rapidly and directly attained as the result, firstly, of the rearrangement of the blastomeres of the cleavage-disc to form a unilaminar blastodermic membi'ane overlying.tbe solid yolk, and, secondly, of the rapid extension of the peripheral (extra-embryonal) region of the same, in contact with the inner surface of the firm sphere furnished by the egg-envelopes. During the completion of the blastocyst embryonal differentiation remains in abeyance, and practically does not start until after growth of the blastocyst is well initiated.


In the Marsupial, notwithstanding the fact that the ovum has become secondarily holoblastic, the mode of formation of the blastocyst is essentially that of the Monotreme. Cleavage is of the radial type, and owing to the persistence of the shell, wliicb with the zona forms a firm resistant sphere enclosing the egg, the radially arranged blastomeres ai'e able to assume the form of an open ring and to proceed directly to the formation of the unilaminar wall of the blastocyst. The enclosing sphere provides the necessary firm surface over which the products of division of the upper and lower cell-rings of the 16-celled stage can respectively spread towards opposite poles, so as to directly constitute the formative and non-formative regions of the blastocyst wall. In my opinion it is the persistence of the resistant shellmembrane round the ovum which conditions the occurrence in the Marsupial of this direct method of blastocyst formation. As in the Monotreme, so here also embryonal differentiation commences only after the blastocyst has gi'ovvn considerably in size.

^ In the Eutheria, on the other hand, in the absence of the shell-membrane, not only is the mode of formation of the blastocyst quite different to that in the Marsupial, but the relations of the constituent parts of the completed structure also differ markedly from those of the homogenous parts in the latter. The cleavage process here leads only indirectly to the formation of the blastocyst, and must be held to be csenogeneticaily modified as compared with that of lower mammals. In the cross-shaped arrangement of the blastomeres in the 4-celled stage, in the occurrence of a definite morula-stage and of the entypic condition, we have features in which the early ontogeny of the Eutheria differs fundamentally from that of the Metatheria. They are intimately correlated the one with the other, and are met "with in all Eutheria, so far as known, but do not occur either in the Prototheria or the Metatheria, so that we must regard them as secondary features which were acquired by the primitive Eutheria under the influence of some common causal factor or factoi's, subsequent to their divergence from the ancestral stock common to them and to the Metatheria. Now the crossshaped 4-celled stage and the morula-stage are undoubtedly to be looked upon simply as cleavage adaptations of prospective significance in regard to the entypic condition, so that the problem reduces itself to this - how came these adaptations to be induced in the first instance ? In view of the facts that in the Metatheria, in the presence of the shell-membrane, the formation of the blastocyst is the direct outcome of the cleavage process, and is effected along the old ancestral lines without any enclosure of the formative cells by the non-formative, whilst in the Eutheria, in the absence of the shell-membrane, blastocyst formation results only indirectly from the cleavage-process, is effected in a way quite different from that characteristic of the Metatheria, and involves the complete enclosure of the formative by the non-formative cells, I venture to suggest that the cleavage adaptations which I'esult in the entypic condition were acquired in the first instance as the direct outcome of the total loss by the already greatly reduced Eutlierian ovum of the shell-membrane.^ This view necessarily implies that the presence of a thick zona such as occurs round the ovum in certain Eutheria is secondary, and what we know of this membrane in existing Eutheria is at all events not adverse to that conclusion.

This suggestion I first put foi'ward in a course of lectures on the early ontogeny and placentation of the Mammalia delivered at the University of Sydney in 1904.


Amongst the Marsupials the zona is quite thin (about -00] 6 imn. in Dasyurus), presumptive evidence that it was also thin in the ancestral stock from which the Meta- and Eutheria diverged, whilst amongst the Eutheria themselves the zona, as Robinson ('03) has pointed out, is not only of very varying thickness, but persists round the ovum for a very varying period iu different species. It appears to be thinnest in the mouse ('001 mm.), in most Eutheria it is considerably thicker (•01 mm., bat, dog, rabbit, deer), whilst in Cavia it reaches a thickness of as much as -02 mm. In those forms in which the blastocyst early becomes embedded in, or attached to, the mucosa, the zona naturally disappears early. In the rat, mouse and guinea-pig it disappears before the blastocyst is formed. Hubrecht failed to find it in the 2-celled egg of Tupaia, and it was already absent in the 4-celled stage of Macacus nemestrinus, discovered by Selenka and described by Hubrecht. On the other hand, it may persist for a much longer period, up to the time of appearance of the primitive streak (rabbit, dog, ferret). These facts sufficiently demonstrate the variability of the zona in the Eutherian series, and its early disappearance in certain forms before the completion of the blastocyst stage shows that it can have no supporting function in regard to that.


Postulating, then, the disappearance of the shell-membrane and the presence of a relatively thin, non-resistant zona (with perhaps a layer of albumen) round the minute yolk-poor ovum of the primitive Eutherian, and remembering that the ovum starts with certain inherited tendencies, the most immediate and pressing of which is to produce a blastocyst comprising two differentiated groups of cells, the problem is how, in the absence of the old supporting sphere constituted by the eggenvelopes, can such a vesicular stage be most easily and most expeditiously attained ? The Eutherian solution as we see it in operation to-day is really a very simple one, and withal a noteworthy instance of adaptation in cleavage (Lillie, '99). In the absence of any firm supporting membrane round the egg, and the consequent impossibility of the blastomeres proceeding at once to forna the blastocyst wall, they are under the necessity of keeping together, and to this end cleavage has become adapted. For the ancestral radial arrangement of the blastomeres in the 4-celled stage, characteristic of the Monotreme and Marsupial, there has been substituted a cross-shaped grouping into two pairs, and, as the outcome of this adaptive alteration in the cleavage planes, there results from the subsequent divisions, not an open cell-ring, as in tbe Marsupial, but a compact cell-group or morula. In this we again encounter precisely the same differentiation of the blastomeres into two categories, respectively formative (embryonal) and non-formative (trophoblastic) insignificance, as is found in the 16-celled stage of the Marsupial, but, since the two groups of cells are here massed together, and in the absence of any firm enclosing sphere, cannot spread independently so as to form directly the wall of the blastocyst, there has arisen the necessity for yet other adaptive modifications. Attention has already been directed to the tardiness of differentiation in the embryonal region of the Monotreme and Marsupial blastocyst, and here in the minute Eutherian morula we find what is, perhaps, to be looked upon as a further adaptive exaggeration of this same feature in the inertness which is at tirst displayed by the formative cells, and which is in marked contrast with the activity shown by the non-formative ectodermal cells.^ It is these latter, it should be recollected, which exhibit the greatest growthenergy during the formation of the blastocyst in the Monotreme and Marsupial, and so their greater activity in the Eutherian tnoi'ula is only what might be expected. Dividing more rapidly than the formative cells, they gradually grow round the latter, and eventually form a complete outer layer enveloping the inert formative cell-group. This process oFovergrowth or epiboly is entirely comparable in its effect with the spreading of the extra-embryonal region of the unilamiiiar blastodermic membrane in the Monotreme to enclose the yolkmass, and with that of the non-formative cells in the Marsupial to complete the lower hemisphere of the blastocyst, growlh round an inert central cell-mass being here substituted for growth over the inner surface of a I'esistant sphere constituted by the egg-envelopes, such as occurs during the formation of the blastocyst in the Monotreme and Marsupial. .Just as the first objective of the cleavage process in the latter is to effect the completion of the cellular wall of the blastocyst, so hei*e the same objective recurs, and is attained in the simplest possible way in the new circumstances, viz. by the I'apid envelopment of the formative by the, non-formative cells. Thus at the end of the cleavage process in the EutheiJan we have formed a solid entypic morula in which an inner mass of formative cells is completely surrounded by an outer enveloping layer of non-formative or ti'opho-ectodermal cells, homogenous with the extra-embryonal ectoderm of the Sauropsidan and Monotreme and the non-formative region of the unilaminar blastocyst of the Marsupial. Conversion of the solid morula into a hollow blastocyst capable of imbibing fluid from the uterus and of growing rapidly now follows. Intraor intercellular vacuoles appear below the inner cell-mass, by the confluence of which the blastocyst cavity is established, and the inner cell-mass becomes separated from the enveloping layer of tropho-ectoderm, except over a small area where the two remain in contact.


The inertness of the formative cell-mass is accounted for by Assheton ('98, p. 251) as follows : “ Now, as the epiblast plays the more prominent part in the formation of the l^nlk of the embi-yo dui-ing the earliest stages, it clearly would be useless for tlie embryonic part to exhibit much energy of growth until the old conditions [in particular sufficient room for embryonal differentiation] were to a certain extent regained ; hence the lethargy exhibited by the embryonic epiblast in mammals during the first week of develoxunent. No feature of the early stages of the mammalian embryo is more striking than this inertness of the embryonic eiriblast - or, as I should nowjrrefer to call it, simply epiblast during the first few days.

  • Assheton, it should be remembered, holds that the inner cell-mass of Eutheria furnishes only the embryonal ectoderm.


The complete enclosure of the formative cells of the inner cell-mass by the non-formative ectodermal cells of the enveloping layer which produces this peculiar entypic condition in the Eutherian blastocyst, I would interpret, then, as a purely adaptive phenomenon, which in the given circumstances effects in the simplest possible way the early completion of the blastocyst wall, and whose origin is to be traced to that reduction in size and in its envelopes which the Eutherian ovum has suffered in the course of phylogeny, in adaptation to the conditions of intra-uterine development. In particular, starting with a shell-bearing ovum, already minute and undergoing its development in utero, I see in the loss of the shell such as has occurred in the Eutheria an intelligible explanation of the first origin of those adaptations which culminate in the condition of entypy. I am therefore wholly unable to accept the view of Hubrecht (^08, p. 78), that " what Selenka has designated by the name of Entypie is - from our point of view - no secondary phenomenon, but one which repeats very primitive featui*es of separation between embryonic ectoderm and larval envelope in invertebrate ancestors.


I see no reason for supposing that the intimate relationship which is early established in many Eutheria between the trophoblastic ectoderm and the uterine mucosa has had anything to do with the origination of the entypic condition. In ray view such intimate relationship involving the complete enclosui'e of the blastocyst in the mucosa only came to be established secondarily, after entypy had become the rule. On the other hand, the peculiar modifications of the entypic condition met with in rodents with “^inversion” (e.g. i-at, mouse, guinea-pig) are undoubtedly to be correlated, as Van Beneden also believed ('99, p. 332), with the remarkably early and complete enclosure or implantation of the germ in the mucosa such as occurs in these and other Eutheria. Similar views are expressed by Selenka in one of his last contributions to mammalian embryology. He writes ('00, p. 205) - “Dass die Entypie des Keimfeldes und die Blattinversion begiinstigt wil'd durch die friihzeitige Yerwachsung der Eiblase mit dem Uterus, ist nicht in Abrede zu stellen. Aber da dieser Prozess auch in solclieu Eiblasen dei- Saugetiere vorkommen kanii, die iiberhaupt nichb, odei- erst spiiter mifc dem Uterus verwachsen, so kaiiu die Keimfeld-Entypie zwar durch die frube Verwacbsung veraiilasst, aber nicht ausscldiesslich liervorgerufeii werclen.” He goes on to remark that - “Die Vorbedingimgeti zur Eutypie miissen in der Struktur der verwachseuden Eiblase gesucht werden/^ and expi-esses his agreement with the views of Van Beneden as to tlie significance to be attributed to the early cleaviige phenomena in Eutheria.


The attitude of the illustrious Belgian embryologist whose loss ws have so recently to deplore, towards this problem is clearly set forth in the last memoir which issued from his hand. “Je suis de ceux,^' he wrote (T9, p. 332), “qui pensent que toute Pembryologie des Mammiferes placentaires temoigue quTls derivent d'animaux qui, comme les Sauropsides et les Mouotremes, produisaieut des oeufs meroblastiques. Je ne puis a aucun point de vue me rallier aux idees contraires formulees eb defendues par Hubrecht. L^hypothese de Hubrecht se heurte a des difiicultes morpliologiques et physiologiques insurmontables : elle laisse inexpliquee Pexistence, chez les Mammiferes placentaires, d'une vesicule ombilicale et dTne foule de caracteres commnns a tons les Amniotes et distiuctifs de ces auimaux.'^ Holding this view of the origin of the Eutheria, Van Beneden based his interpretation of their early ontogenetic phenomena on the belief that “ la reduction progressive du volume de Poeuf d'une part, le fait de son developpement iutrauterin de hautre ont dii avoir une influence preponderante sur les premiers processus evolutifs.


Balfour, in his classical treatise, had already some eighteen years earlier expressed precisely the same view. “The features of the development of the placental Mammalia,^' he wrote (‘Mem. Edn.,^ vol. iii, p. 289), “receive their most satisfactory explanation on the hypothesis that their ancestors were provided with a large-yolked ovum like that of Sauropsida. The food-yolk must be supposed to have ceased to be developed on the establishment of a maternal nutrition through the uterus. . . . The embryonic evidence of the common origin of Mammalia and Sauropsida, both as concerns the formation of the layers and of the embryonic membranes is as clear as it can be.


That view of tlie derivation of the Mammalia receives, I venture to think, striking confirmation from the observations and conclusions set forth in the preceding pages of this memoir, and from it as a basis all attempts at a phylogenetic interpretation of the early ontogenetic phenomena in the Mammalia must, I am convinced, take their origin. Such an attempt I have essayed in the foregoing pages, with what success the reader must judge.


Addendum

The memoir of Prof. 0. Van der Stricht, entitled "La structure de I'cBuf des Mammiferes (Chauve-souris, Vesperugo noctula) : Troisieme Partie" (Mem. de PAcad. roy. de Belgique,' 2nd ser., t. ii, 1909), came into my hands only after my own paper had readied its final form, and therefore too late for notice in the body of the text. In this extremely valuable contribution, Van der Stricht gives a detailed account of the growth, maturation, fertilisation, and early cleavage-stages of the ovum of Vesperugo, illustrated by a superb series of drawings and photo-micrographs. All I can do here, however, is to direct attention to that section of the paper entitled “ Phenomeues de deutoplasmolyse an pole vegetatif de I'ceuf” (pp. 92 - 96), in which the author describes the occurrence in the bat's ovum of just such a process of elimination of surplus deutoplasmic material as I have recorded for Dasyurus. Van der Stricht's interpretation of this phenomenon agrees, I am glad to find, with my own. He writes (pp. 92-93): Ce deutoplasme rudimentaire, i\ peine ebauche dans I'ovule des Mammiferes, parait etre encore trop abundant dans I'oeuf de Chauve-souris, car ces materiaux de reserve, en partie inutiles, sont partiellement elimines, expulses de la cellule.


To this process of elimination of surplus deutoplasm he applies the name deutoplasmolyse, and states that Ce phenomene consiste dans I'apparition de lobules vitellins multiples, en nombre tres variable, a la surface du vitellus au niveau du pole vegetatif. Ces bourgeons a peu pres tous de meme grandeur, les uns etant cependant un peu plus volumineux que les autres, apparaissent dans le voisinage des globules polaires et presentent la structure du deutophisme. 11s sont formes de vacuoles claires, a I'interieur desquelles on aper^oit parfois de petits grains vitellins, dont il a ete question plus haut. . . . Ce processus de deutoplasmolyse devient manifeste surtout apres I'expulsion du second globule polaire, pendant la periode de la fecondation. 11 pent etre tres accentue, au stade du premier fuseau de segmentation et au debut de la segmentation de I'oeuf, notamment sur des ovules divises en deux et en quatre (figs. 59, 61, 62, d).” It would therefore appear that, whilst in Dasyurus the surplus deutoplasm is eliminated always prior to the completion of the first cleavage and in the form of a single relatively large spherical mass, in Vesperugo it is cast off generally, though not invariably, before cleavage begins, and in the form of a number of small separate lobules.

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Contents: 1 Review of Previous Observations | 2 The Ovum of Dasyurus | 3 Cleavage and Blastocyst | 4 Blastocyst Growth Ectoderm Entoderm | 5 Early Stages of Perameles and Macropus | 6 Summary and Conclusions | 7 Early Mammalia Ontogeny | Explanation of Plates


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