Difference between revisions of "Paper - Contributions to the embryology of the marsupialia 4-6"

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(Created page with "{{Hill1910 header}} ==Chapter VI. - General Summary and Conclusions== The observations recoi'ded in the pi'eceding pages and the conclusions deducible therefrom may be su...")
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this question further, though I would fain express my conviction that had the observations recorded in this paper been  
this question further, though I would fain express my conviction that had the observations recorded in this paper been  
earlier available, much vain speculation as to the phytogeny  
earlier available, much vain speculation as to the phytogeny  
of the trophoblast might possibly have been avoided.
of the trophoblast might possibly have been avoided.
==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
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 doinff 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
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
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
J. r. HILL.
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, foi'nied 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
* We should further he justified in concluding that the entoderm is
similar in its mode of origin in all three mammalian sub-classes.
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).
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 Avith 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
' 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.
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 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
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
t.C.TTV. (€cj
emJb. ect.
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 eai'lv 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
“ chez tons 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
* 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.
trophoblasb 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] ”).
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
J. p. mi,L.
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.
J. r. HILL.
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
.T. P. HlIiL.
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
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
homologneof 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
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
^ “ 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).
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.
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.
,T. r. HILL.
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 tlie 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 i-egard 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 pro
ceecling- 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
* 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
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 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
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
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 tlie 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.
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.”
.T. P. HILL.
To this pi'ocess 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.
List op References.
'94. Assheton, R.  -  “ A Re-investigation into the Early Stages of the
Development of the Rabbit,” ‘ Quart. Journ. Micr. Sci.,' vol. 34.
'98. “ The Development of the Pig during the Pirst Ten Days,”
‘ Quart. Journ. Micr. Sci.,' vol. 41.
'98. “ The Segmentation of the Ovum of the Sheep, with Obser
vations on the Hypothesis of a Hypoblastic Origin for the
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'08. “ The Blastocyst of Capra, with Some Remarks upon the
Homologies of the Germinal Layers of Mammals,” ‘Guy's
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'09. “Professor Hubrecht's Paper on the Early Ontogenetic
Phenomena in Mammals ; An Appreciation and Criticism,”
‘ Quart. Journ. Micr. Sci.,' vol. 54.
'97. Bonnet. R.  -  “ Beitriige zur Embvyologie des Himdes,” ‘ Anatomische Hefte,' Bd. ix.
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'87. Caldwell, W. H. -  “ The Erabiyology of Monotremata and Marsnpialia,” Part I, ‘ Phil. Trans. Roy. Soc.,' vol. clxxviii B.
'95. Duval, M. -  “Etudes sur I'embryologie des Oliciropteres,” ‘ Joura.
de I'Anat. et de la Pliysiol.,' t. xxxi.
'86. Heape, W.  -  “ The Development of the Mole (Talpa Europea), the
Ovarian Ovum, and Segmentation of the Ovum,” ‘Quart. Joum.
Micr. Sci.,' vol. 26.
'97. Hill, J. P. -  “ The Placentation of Perameles,” ‘ Quart. Journ.
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'00. “ On the Foetal Membranes, Placentation and Parturition of
theNative Cat(Dasyurus viverrinus),” ‘Anat. Anz.,'Bd.xviii.
'88. Hubrecht, A. A. W.  -  “ Keimbliitterbildung und Placentation des
Igels,” ‘ Anat. Anz.,' Bd. iii.
'89. “ Studies in Mammalian Embryology : (1) The Placentation
of Erinaceus europaeus, with Remarks on the Physiology of
the Placenta,” ‘ Quart. Joura. Micr. Sci.,' vol. 30.
'95. “ Die Phylogenese des Amnions und die Bedeutung des
Trophoblastes,” ‘ Verhand. Kon. Akad. v. Wetensch. Amsterdam,'
vol. iv.
'02. “ Fiirchung und Keimblattbildung bei Tarsius Spectrum,”
‘ Yerhand. Kon. Akad. v. Wetensch. Amsterdam,' vol. viii.
'04. “ The Ti'ophoblast,” ‘ Anat. Anz.,' Bd. xxv.
'08. “ Early Ontogenetic Phenomena in Mammals, and their
Bearing on oim Intei'pretation of the Phylogeny of the Vertebrates,” ‘ Quart. Joura. Micr. Sci.,' vol. 53. .
'09. “The Foetal Membranes of the Vertebrates,” ‘ Proc.
Seventh Interaational Congress, Boston Meeting,' August 19th
to 24th, 1907.
'00. Jenkinson, J. W.  -  “A Re-investigation of the Early Stages of the
Development of the Mouse,” ‘ Quart. Journ. Micr. Sci.,' vol. 43.
'06. “ Remarks on the Germinal Layers of Vertebrates and on
the Significance of Germinal Layers in General,” ‘ Mem. and
Proc. Manchester Lit. and Philos. Soc.,' vol. 1.
'01. Keibel, F.  -  “Die Gastrulation und die Keimblattbildung der
Wirbeltiere,” ‘ Ergebnisse der Anatomie und Entwickelungsgeschichte ' (Merkel u. Bonnet), Bd. x.
“ Die Entwickelung der Rehes bis zui* Anlage des Meso
blast,” ‘ Arch, fiir Anat. u. Physiol. Anat. Abth.'
' 02 .
J. r. Hii,L.
0/. Lams, H., and Doonne, J.  -  “ Nouv^elles recheivhes sur la Maturation et la Fecondation de I'cenf des Maminiferes,” ‘ Arch de Biol.,'
t. xxiii.
03. Lee, T. Gr. ‘Implantation of the Ovum in Sf)ermoi)hilus
tridecemlineatus, Mitcli.,” ‘ Mark Anniv. Vol.,' Art. 21.
'99. Lillie, F. R. -  ‘ Adaptation in Cleavage,” ‘Biol. Lect. Wood's
Holl.,' 1897 - 98 (Ginn & Co., Boston).
'09. MacBride, E. W. -  “ The Formation of the Layers in Amphioxus
and its bearing on the Interjiretation of the Eai'ly Ontogenetic
Processes in other Vertebrates,” ‘ Quart. Journ. Micr. Sci.,' vol. 54.
03. Robinson, A. Lectures on the Early Stages in the Development
of Mammalian Ova and on the Formation of the Placenta in
Different Groups of Mammals,” ‘ Journ. of Anat. and Physiol.,'
vol. xxxviii.
86. Selenka, E. ‘ Studien iiber Entwickelungsgeschichte der Thiere,'
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'91. ‘‘ Beutelfuchs und Kiinguruhratte ; zur Entsteliungs
geschichte der Amnion der Kantjil (Tragulus javanicus) ;
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'00. ‘ Studien hber Entw. der Tiere,' H. 8, Menschenaffen.
“ III, Entwickelung des Gibbon (Hylobates und Sianianga),”
Wiesbaden : 0. W. Kreidel.
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‘ Zool. Forschungsreisen iin Australien, etc.,' Bd. ii. Lief 1.
'95. Sobotta, J. “ Die Befruchtung und Furchung des Eies der Mans,”
‘ Arch, fiir Mikr. Anat.,' Bd. xlv.
'75. Van Beneden, E.  -  ” La Maturation de I'cEuf, la fecondation et les
Iiremieres phases du develoiipement embryonnaire des Mammiferes d'apres les recherches faites sur Je Lapin,” ‘ Bull, de I'Acad.
roy. des sciences, des lettres, et des beauxaits de Belgique,' t. xl.
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tion des feuillets chez le Lapin,” ‘ Arch, de Biologie,' t. i.
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Murin (Vespertilio murinus),” ‘Anat. Anz.,' Bd. xvi.
'03 Van der Stricht, O.  -  ‘‘La Structure et la Polarite de I'ceuf de
Chauve-Souris (V. noctula),” ‘ Comptes rendus de I'Association
des Anatomistes, V“ Session, Liege.'
“ La Structure de I'ceuf des Maminiferes. Premiere partie,
L'oocyte an stade de I'accroissement,” “Arch, de Biologic,'
t. xxi.
'05 Van cler Stvidit, O. -  “ La Stvuctnre de I'ceuf des MammifOTes.
Denxieine partie, Structure de I'ceuf ovarique de la femme,” ‘ Bull,
de I'Acad. Roy. de Medicine de Belgique,' Seance du 24 J uin, 1905.
'97 Wilson, J. T., and Hill, J. P. -  “ Observations upon the Development and Succession ot the Teeth in Perameles; togethei with
a Contribution to the Discussion of the Homologies of the Teeth
in Marsupial Animals,” ‘ Quart. Journ. Micr. Sci., vol. xxxix.
'03 “ Primitive Knot and Early Gastrnlation Cavity co
existing with independent Primitive Streak in Ornithorhynchus,”
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Illustrating Prof. J. P. Hill's paper on “ The Early Development of the Marsupialia, with Special Reference to the
Native Cat (Dasyurus vi verrinus).”
[All figures are from specimens of Dasyurus, unless otherwise indicated. Drawings were executed with the aid of Zeiss's camera lucida,
except figs. 61-63, which were drawn from photographs.]
List of Common Reference Letters.
Ab7i. Abnormal blastomei'e, fig. 37. alh. Albumen, eg. Coagulum.
d. p. Discus proligerus. d. z. Deutoplasmic zone. emb. a. Embryonal
area. emb. ect. Embiyonal ectoderm, ent. Entoderm. /. ep. Follicular
epithelium. /. a. Formative area of blastocyst wall. /. c. Formative
cell. /. z. Formative zone. i. c. Internal cell, fig. 34. Z. eat. Limit of
extension of entoderm. Z. p. Incomjilete ai'ea of blastocyst wall at lower
pole. p. b'. First polar body. p. b'. s. First polar spindle, p. V. s.
Second polar spindle, p. s. Perivitelline space, s. m. Shell-membrane.
sp. Sperm in albumen. Zr. ect. Non-formative or trophoblastic ectoderm (tropho-ectoderm). y.b. Yolk-body. z. p. Zona.
Fig. 1.  -  Photo-micrograph (x 150 diameters) of the full-grown
ovarian ovum, '27 X ‘26 mm. diameter. The central deutoplasmic
zone (cZ. z.) and the peripheral formative zone (/. z.), in which the vesicular nucleus ('QS X '03 mni. diameter) is situated, are clearly distinguishable. The zona (z. p.) measures •0021-'0025 mm. in thickness.
Outside it are the follicular epithelial cells of the discus proligerus
(d.p.), which is thickened on the upper side of the figure, where it
becomes continuous with the membrana granulosa. (D. v i v., 21 . vii .
'04, Hermann's fluid and iron-hsematoxylin.)
Fig. 2.  -  Photo-micrograph ( X. 150) of ripe ovarian ovum (in which
first polar body is separated and second polar spindle is present, though
neither is visible in figure), '29 X '23 mm. maximum diametei'. FoUicle
1'4 X IT mm. diameter. The ovum exhibits an obvious polarity.
Deutoplasmic zone {d. z.) in upper hemisphere ; formative zone (/. z.)
foi-ming lower. (D. v i v., 14, 26 . vii . '02, Flemming's fluid and
Fig. 3.  -  Photo-microgi'aph ( x 150) of ripe ovarian ovum ('28 x '24
mm. diameter) with first polar body (p. bK) and second polar spindle.
First polar body, •026-‘03 x '01 mm. Second polar spindle, '013 mm.
in length. (D. v i v., 14, 26 . vii . '02, Flemming's fli;id and ironhaematoxylin.)
Fig. 4.  -  Photo-micrograph (x 256) of ovarian ovum in process of
growth (“pseudo-alveolar” stage). Ovum, ‘26 X '20 mm. diameter.
Zona, •0017-‘002 mm. in thickness. (D. v i v., 14, 26 . vii . '02,
Hermann, iron-haematoxylin.)
Fig. 5.  -  Photo-microgi-aph (X 1250) of peripheral i-egion of ripe
ovarian ovum ('28 X T26 mm. diameter) with first polar spindle ('015
X '013 mm.). (D. v i v., 23 . vii . '02, Ohlmaicher's fluid, iron-haema
Fig. 6. -  Photo-micrograph (x 1250) of peripheral region of ripe
ovarian ovum ('26 X T8 mm.), showing first polar body (p. b'.) ('03 X
•006 mm.). (D. v i v., 14, 26 . vii . '02, Flemming, iron-hfematoxylin.)
Fig. 7. -  Photomicrograph ( X 1250) of periplieral region of ovum, fig.
3, showing portion of first polar body (p. 5'.), and the second polar
spindle. The dark body lying between p. 5'. and the surface of the
ovum is a displaced red blood-corpuscle.
Figs. 8 and 9. -  Photo-micrographs ( X about 84) of unsegmented ova,
respectively '33 mm. and '35 mm. in diameter, from the uterus, taken
immediately after their transference to the fixing fluid (picro-nitroosmic acid), showing the shell-membrane (s. m.), laminated albumen
{alb.), with sperms (sp.), the zona (z. p.), perivitelline space {p. s.), and
the body of the ovum, with its formative (/. z.), and deutoplasmic {d. z.)
zones. (D. v i v., 15, 19 . vii . '01.)
Fig. 10. -  Photo-micrograph ( X 150) of section of imsegmented ovum
almost immediately after its passage into the uterus, showing the very thin sliell-inembvane externally (s. m.) (about '0016 mm. in thickness),
the albumen {alb.), zona (z-i?.), and the deutoplasmic {d. z.) and formative
(/. z.) zones of its cytoplasmic body. The male pronucleus is visible in
the formative zone. Diameter of entire egg about '29 mm. (D. viv.,
15, 19 . vii . '01, Picro-nitro-osmic and iron-hffimatoxylin.)
Fig. 11.  -  Photo-micrograph ( X 150) of section of unsegmented ovum
from the uterus, slightly older than that of fig. 10. Diameter of entire
egg in fresh state •34-'35 mm., of the ovum proper '3 X ‘28 mm. ; thickness of shell, -0024 mm. In the figure the female pronucleus is visible
near the centre of the formative zone (/. z.), and the male pronucleus
lies a little above it and to the right. The perivitelline space (jJ.s.)
is pai-tiaUy occupied by coagulum. (D . viv., 21 . v . '03, f. Hermann,
Fig. 12.  -  Photo-micrograph ( X 150) of an unsegmented ovum from
the irterus, of the same batch as that of fig. 11, and '34 mm. in diameter.
The two pronuclei are visible in the central region of the formative
Fig. 13.  -  Photo-microgi-aph ( X 330) of uterine ovum. Stage of first
cleavage spindle. Diameter, '315 mm. (D. viv., 1, 15 . vii . '01, f.
Picro-nitro-osmic, iron-hiematoxylin.)
Fig. 14.  -  Photo-micrograph ( X about 78) of egg in the 2-celled stage,
taken immediately after its transference to the fixing fluid. Lateral
view. y. b. Yolk body. Diameter of entire egg about "34 mm. (D . viv.,
1, 15 . vii . '01. Picro-nitro-osmic.)
Fig. 15.  -  Photo-microgi'aph (x about 78) of another 2-celled egg,
seen from lower pole. Diameter, '35 mm. (D. viv., 4 B, 23 . vi . '02.
Perenyi's fluid.)
Fig. 16.  -  Photo-micrograph (x about 78) of another 2-celled egg,
of the same batch as preceding. End view, showing one of the two
blastomeres and the yolk -body (y. b.).
Fig. 17.  -  Photo-micrograph (x 150) of vertical section of 2-celled
egg, "34 mm. in diameter, showing the shell-membrane ('0064 mm. thick),
traces only of the albumen, the zona (z.p.), and the two blastomeres (the
left one measuring, from the sections, T6 x T8 x TO mm., its nucleus
‘031 X ‘027 mm. ; the right one, T6 x T9 X "09 mm., its nucleus, '03 x
•028 mm.). Note the differentiation in their cytoplasmic bodies.
(D . viv., 6, 21 . vii . '01, Picro-nitro -osmic and iron-hsematoxylin.)
Fig. 18.  -  Photo-micrograph (x 150) of vertical section of 2-celled
egg, '32 mm. in diameter, with shell-membrane '005 mm. thick, showing
the two blastomeres, and enclosed between their upper ends the yolk body {y. b.). (D . viv., 1, 15 . vii . '01, f. Picro-nitro-osmic, iron-htematoxylin.)
Figs. 19 and 20.  -  Photo-micrographs ( x about 70) of 4-eelled eggs
taken immediately after transference to Perenyi's fluid. Fig. 19, side
view, showing yolk-body (y. h.) ; fig. 20, polar view. Diameter of entire
egg about -35 mm. (D . viv., 14 b, 18 . vi . '02. Perenyi.)
Fig. 21. -  Photo- micrograph (x about 70) of another 4-celled egg,
from the same batch as the preceding, seen from lower pole.
Fig. 22. -  Photo-micrograph (x 150) of section of 4-ceUed egg of
same batch as those of figs. 19 and 20. The two right and the two
left blastomeres respectively form pairs, so that the plane of the first
cleavage is parallel with the sides of tlie plate, that of the second with
the top and bottom of the same. The two left blastomeres are still
connected by a narrow cytoplasmic bridge. Thickness of shell,
•0072 mm.
Fig. 23. -  Photo-micrograph ( x 150) of a vertical section through
a 4-celled egg. ‘35 mm. in diameter, showing two of the blastomeres
and a small portion of the yolk-body {y. b.). Note, as in fig. 22, the
marked diflierentiation in the cytoplasm of the blastomeres. (D. viv.,
4, 27 . vi . '01. Picro-nitro-osmic, iron-hsematoxylin.)
Figs. 24 and 25.  -  Photo-micrographs ( x 140) of horizontal sections
through a 16-celled egg, '38 mm. diameter, fig. 24 showing the eight
larger, more yolk-rich cells of the lower (non-formative) ring, and fig. 25
the eight smaller, less yolk-rich cells of the upper (formative) ring.
Shell ‘0075 mm. in thickness, yolk-body (not included in the figures)
'll X TO mm. in diameter. (D. viv., 3 b, 26 . vi . '01; 15, f and |.
Picro-nitro-osmic and iron-hsematoxylin.)
Fig. 26.  -  Photo-micrograph (x 140) of a vertical section of an egg
of the same batch and size as that represented in figs. 24 and 25, but
with seventeen cells  -  formative = 9 (6 + [1 X 2] + 1) in division ;
non-formative = 8. Two of the formative cells (/. c.) of the upper ring
are seen enclosing between them the faintly mai'ked yolk-body {y. b.),
and below them two of the much more opaque non-formative cells
{tr. ect.) of the lower ring.
Fig. 27.  -  Photo-micrograph (x about 76) of the just completed
blastocyst, '39 mm. in diameter. From a spirit specimen. The dark
spherical mass (eg.) in the blastocyst cavity is simply coagulum, produced by the action of the fixative (picro-nitro-osmic acid) on the
albuminous fluid which fills the blastocyst cavity. (D. viv., 2 b,
16 . vii . '01.)
Fig. 28. -  Plioto-anicrogi-apli ( X about 76) of a blastocyst of the same
batch as the preceding, •45 mm. in diameter. From a spirit specimen.
eg. Coagulum.
Fig. 29.  -  Photo-micrograph (x about 75) of another blastocyst,
•45 mm. diameter, of the same batch as the preceding, but taken
immediately after transference to the fixative. Viewed from the upper
pole. y. b. Tolk-body seen through the unilaminar wall.
Fig. 30.  -  Photo-micrograph ( X about 75) of a blastocyst of the same
batch as the preceding, about '39 mm. in diameter, in which the cellular
wall has not yet been completed over the lower polar region.
Fig. 31.  -  Photo-micrograph ( X 140) of a section of a blastocyst,
•39 mm. diameter, of the same batch as the preceding and at precisely
the same developmental stage, the cellular wall having yet to be completed over the lower polar region (l.p.). In the blastocyst cavity is
seen the yolk-body (y. b.) partially surroixnded by a mass of coagulum
(eg.). (D. viv., 2 B, 16 . vii . '01, m. = '39, Picro-nitro-osmic and
Fig. 32.  -  Photo-micrograph ( X 140) of another blastocyst, ^41 mm.
in diameter, of the same batch as the preceding, also 'with the cellular
wall still absent over the lower polar region. Shell-membrane ‘0075 mm.
in thickness, y. b. Tolk-body. c. g. Coagulum. The cellular wall
comprises about 130 cells.
Fig. 33.  -  Photo-micrograph ( X 140) of a blastocyst of the same batch
as the preceding, with a complete unilaminar cellular wall. y. b. Yolkbody, in contact with inner surface of wall, in the region of the upper
Fig. 34.  -  Photo-micrograph (x 100) of a section of a blastocyst
•57 mm. in diameter, i. c. Internal ceU. (D . vi v., 29 . vi . '04, y . Pici^onitro-osmic.)
Fig. 35.  -  Photo-micrograph (x 100) of a section of a blastocyst, '73
mm. diameter, of the same batch as the pi^eceding, shell, ^0045 mm.
Fig. 36.  -  Photo-micrograph (x 100) of a section of a blastocyst -66
mm. diameter, of the same batch as the pi-eceding. Lower hemisphere
opposite yolk-body {y. b.) formed of larger cells than upper. Hermann
Fig. 37. -  Photo-micrograph (x 140) of section of an abnormal
vesicle, 397 mm. diameter of the same batch as the normal vesicles
represented in figs. 27-33. abn. large binucleate cell, regarded as a
blastomere of the lower hemisphex^e which has failed to divide in noi^mal
fashion, cf . text, p. 42.
Fig. 38 -  Photo-micrograpli ( x 10) of entire blastocyst 4'5 mm. diameter to show the junctional line {j. 1.) between formative and nonformative regions. From a spirit specimen. (D . viv., /3, 25 . vii . '01.
Fig. 39. -  Photo-microgi-aph ( x about 10) of an entire blastocyst,
4'5 mm. diameter with distinct embryonal area {emh. a.). (D. viv., 5,
18 . vii . '01.)
Fig. 40.  -  Photo-micrograph { X 10) of entire blastocyst about 5 mm.
diameter showing embryonal area' {emh. a.), peripheral limit of entoderm (1. ent.), and the still unilaminar region of the wall {tr. ect.). (D.
viv., 8 . vi . '01.)
Fig. 41.  -  Photo-micrograph ( x 150) of an in toto preparation of the
wall of a blastocyst of 3'5 mm. diameter. (D . viv., 16, 21 . vii . '01.)
Fig. 42.  -  Photo-micrograph (x 150) of an in toto preparation of the
wall of a blastocyst of 3'25 mm. diameter, j. 1. Junctional line between
the formative (/. a.) and non-formative {tr. ect.) regions of the wall.
(D. viv., 24 . vii . '01.)
Figs. 43 and 44.  -  Photo-micrographs (x 150) of in toto preparations
of the wall of 4'5 mm. blastocyst showing the jimctional line between
the formative (/. a.) and non-formative {tr. ect.) regions. (D. viv.,
P, 25 . vii . '01. Picro-nitro-osmic and Ehrlich's hsematoxylin )
Fig. 45.  -  Photo-micrograph ( x 150) of a corresponding preparation
of the wall of a more advanced 4'5 mm. blastocyst ('99 stage), in which
the two regions of the wall are now clearly distinguishable. (D. viv.,
8.7. '99. Picro-nitro-osmic, Ehrlich's hsematoxylin.)
Fig. 46.  -  Photo -micrograph ( x 150) of a corresponding preparation
of a slightly more advanced blastocyst ('04 stage). (D. viv., 6 . 7 . '04.
Picro-nitro-osmic, Ehrlich's hsematoxylin.)
Fig. 47.  -  Photo-micrograph (x 150) of an in toto preparation of the
formative region of a 6 . 7 . '04 blastocyst, showing the proliferation
of spherical interaal cells refeiTed to in the text, p. 53.
Fig. 48.  -  Photo-micrograph ( X 150) of an in toto preparation of the
wall of a vesicle of the same batch as that represented in fig. 39, in
which a small part of the junctional line between the embryonal ectodenn and the extra-embryonal {tr. ect.) is visible, the free edge of the
entoderm {ent.) not having reached it. (D. viv., 5, 18 . vii . '01. Picronitro-osmic, Ehrlich's hsematoxylin.)
Fig. 49. -  Photo-micrograpli ( X 150) of a con-esponding preparation
of a vesicle of the same batch as the preceding, in which the wavy and
irregularly thickened free edge of the entoderm {ent.) practically
coincides with the junctional line and so conceals it from view.
Fig. 50. -  Photo-micrograph (x 150) of an in to to preparation of a
vesicle (8 . vi . '01 batch) viewed from the inner surface as in the corresponding preceding figures. The entoderm in the region of the embryonal
ax-ea has been removed, so that one sees the inner surface of the embryonal
ectoderm [emh. ect.) ; it is still in situ, though not in a quite intact condition over the adjoining portion of extra-embryonal ectoderm. The
entoderm has not yet extended over the region indicated by the reference
line to tr. ect., so that here the extra-embryonal ectoderm is cleai-ly
visible. The jimctional line is apparent. (D. viv., 8 . vi . '01. Picronitro-osmic. Ehrlich's hsematoxylin.)
Fig. 51 (Plate 3).  -  Photo-microgi-aph ( X 310) of a section of a 30celled egg of Perameles obesula; egg b, '24 X '23 mm. diameter,
showing the xinilaniinar layer formed by the blastomeres.
Fig. 52 (Plate 3).  -  Photo-micrograph (x 240) of a section of a
blastocyst of P. nasuta '29 X •26 mm. diameter, showing the shellmembrane {s.vi.), zona (z.p.), and the unilaminar celhxlar waU. The
portion of the latter adjacent to the reference lines is composed of
smaller but thicker cells than the remainder.
Figs. 53 and 54.  -  Drawings ( X 84) of a 6-celled egg '34 mm. diameter,
fig. 53 showing a side view and fig. 54 a view from the lower pole.
Observe the characteristic I'ing-shaped arrangement of the blastomeres.
y. b. Yolk -body, the shell-membrane, albumen layer with sperms included, and the zona are readily distinguishable. Outlines drawn with
the aid of the camera lucida immediately after transference of the egg
to the fixing fluid. (D . viv., 22, 16 . vii . '01.)
Figs. 55 and 56.  -  Drawings ( X about 88) of a 16-ceUed egg (about ‘37
mm. diameter) as seen fx'om the side and lower pole respectively, from
the same batch as the eggs represented in figs. 24, 25, and 26. The charactei'istic aii'angement of the blastomex'es in two sxxpex'imposed, open
x'ings (each of eight cells) and the diffex'ence in size between the cells of
the two riixgs are evident. The ix'x-egxxlar body (c.g.) seen ixx the cleavage
cavity in fig. 56 is a mass of coagxxluixx. Dx'aunx from a spix'it specimen.
The albumen layer as represented in fig. 56 is too thick. (D. viv.,
3 B, 26 . vi . '01.)
Figs. 57 and 58.  -  Drawings (x about 85) of a 12-celled egg (-38 xixm.
diameter) as seen from the side axxd lower pole respectively. Four of the blastomeres of the 8-ceHed stage have already divided (4 + 4x2)
= 12. From a spirit specimen and from same batch as preceding.
Fig. 59. -  Drawing ( x about 88) of a 31-celled egg ('375 mm. diameter)
as seen from the lower pole. From a spirit specimen and fi-om the same
batch as the preceding. The irregular body in the blastocyst cavity is
formed by coagulnm. Formative cells = 16; non- formative = 14 + 1
in division.
Fig. 60.  -  Drawing ( X about 88) of another 31-celled egg ('375 diameter)
from the same batch as the preceding. Side view.
Fig. 61.  -  Drawing (x 100) of an entire blastocyst (‘39 mm. diameter)
from the same batch as those shown in figs. 27-29.
Fig. 62.  -  Drawing ( x about 80) of an entire blastocyst (‘4 mm.
diameter) from the same batch as the preceding.
Fig. 63.  -  Drawing (x 80 of an entire blastocyst ('6 mm. diameter)
made from a photogi'aph taken directly after transference of the specimen to the fixing fluid. Cells of lower hemisphere with imich more
marked perinuclear areas of dense cytoplasm than those of the upper.
D. viv., 2, 11 . vii . '01.)
Fig. 64.  -  Section of the wall of a blastocyst, 2'4 mm. diameter
(x 630). (D. viv., 7 . vi . '01.)
Figs. 65, 66, 67.  -  Drawings (x 630) of small portions of in toto
preparations of the formative region of 6 . 7 . '04 blastocysts to demonstrate the mode of origin of the primitive entodermal cells {ent., fig. 67).
Fig. 65 shows a dividing entodermal mother-cell in position in the
unilaminar wall, siuTounded by larger lighter staining cells (prospective
embryonal ectodermal cells). In fig. 66 is seen a corresponding cell, a
poi-tion of whose cell-body has extended inwards so as to underlie
(overlie in figure) one of the ectodermal cells of the wall. . In fig. 67
are seen two entodermal cells, evidently sister-cells, the products of the
division of such a cell as is seen in figs. 65 or 66. One of them (the
upper) is still a constituent of the unilaminar wall, the other {ent.) is a
primitive entodermal cell, definitely internal. (D . viv ., 6 . 7 . '04. Picronitro-osmic, Ehrlich's haematoxylin.)
Figs. 68, 69, 70. -  Drawings (x 630) of portions of preparations
similar to the above. For description see text. (D. viv., 6, 7, '04.)
Fig; 71. -  Drawing (x about 630) of a portion of an in toto preparation of the formative region of an '01 blastocyst showing two
primitive entodermal cells, one of them in division. (D. viv., (3,
25 . vii . '01. Picro-nitro-osmic and Ehrlich.)
Fig. 72. -  D rawing (x 630) corresponding to the above, from the
formative region of a 6 . 7 . '04 blastocyst, also showing two primitive
entodermal cells, evidently sister-cells.
Figs. 73, 74, 76.  -  Sections of the formative region of 6.7. '04 blastocysts, showing the attenuated shell-membrane, the unilaminar waU, and
in close contact with the inner surface of the latter, the primitive entodermal cells {ent.) ( X 630).
Fig. 75.  -  Section corresponding to the above, showing an entodermal
mother-cell {ent.), part of whose cell-body nndei'lies the adjacent ectodermal cell of the wall. The spheroidal inwardly projecting cell on the
left is probably also an entodermal mother-cell (x 630).
Fig. 77.  -  Section ( x 630) of the non-formative I'egion of a 6 . 7 . '04
Fig. 78.  -  Section ( X 630) of the embryonal ai'ea, and the adjoining
portion of the still imilaminar extra-embryonal region of a blastocyst of
the 5 . '01 stage, emb. ect. Embryonal ectoderm, ent. Entoderm, tr.
ect. Extra-embryonal ectoderm (tropho-ectoderm). The position of the
junctional line is readily recognisable. (D . vi v. , 5, 18 . vii . '01. Picronitro-osmic and Delafield's hsematoxylin.)
Fig. 79.  -  Section (x 630) through the corresponding regions in an
8 . vi . '01 blastocyst. Note the thickening of the embryonal ectoderm
{emb. ect.), and the peripheral extension of the entoderm {ent.) below
the tropho-ectoderm. (D. viv., 8 . vi . '01. Picro-nitro-osmic and
Fig. 80.  -  Section (x 600) through the formative (embryonal) region
of a blastocyst of P. nasuta, 1‘3 mm. in diameter. It is thicker than
that of the Dasyure blastocyst at the corresponding stage of development ; the primitive entodermal cells are well mai-ked.
Fig. 81.  -  Section ( x 600) corresponding to the above from another
1-3 mm. blastocyst of P. nasuta, of the same batch as the preceding,
but apparently very slightly earlier, the entodermal cells being stiU in
process of separating from the unilaminar wall. ent. Entoderm, tr. ect.
Fig. 82. Section (x about 430) of a section of a blastocyst of M.
ruficollis -35 mm. in diameter, showing the major portion of the
formative region (/. a.) and a small portion of the non-formative {tr. ect.).
The shell-membrane varies in thickness in the sections from (J05 min.
over the former region to '003 mm. over the latter.
Figs. 83, 84, 85.  -  Drawings ( X 630) of small portions of the formative
(and in fig. 83 of the adjoining portion of the non-formative) region of
the above blastocyst of M. ruficollis more highly magnified, ent.
Primitive entodermal cells. Note in fig. 83 a cell of the wall in division,
the axis of the spindle being oblique to the surface.
J. P. Hill, Photo.
Watbslow & Sows LiMlTiiD, Collotype.

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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
Online Editor  
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"


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" (textbooks, papers, people, recommendations) 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, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Chapter VI. - General Summary and Conclusions

The observations recoi'ded in the pi'eceding pages and the conclusions deducible therefrom may be summarised as follows ;

(a) Ovum. - The uterine ovum of Dasyurus is characterised (1) by its large size relatively to those of Eutheria; (2) by the presence externally to the zona of a layer of albumen and a shell-membrane, both laid down in the Fallopian tube and homologous with the corresponding structures in the Mouotreme ovum, the shell-membrane, like the shell of the latter, inci'easing in thickness in the uterus; (3) by its marked


J. r. HILL.

polarity, its lower two thirds consisting of formative cytoplasm, dense and finely granular in appearance, owing to the presence of fairly uniformly distributed deutoplasmic material, and containing the two pronuclei, its upper third being relatively clear and transparent, consisting as it does of a delicate reticulum of non-formative cytoplasm, the meshes of which are occupied by a clear deutoplasmic fluid. Study of the pi'ocess of vitellogenesis in ovarian ova demonstrates that this fluid represents surplus deutoplasmic material which has not been utilised in the upbuilding of the formative region of the ovum.

The fate of the clear non-formative portion of the ovum is a very remarkable one. Prior to the completion of the first cleavage, it is separated off from the formative remainder of the ovum as a spherical mass or yolk-body, Avhich takes no direct part in development, though it becomes enclosed iu the blastocyst cavity on completion of the blastocyst wall at the upper pole. Its contained deutoplasmic fluid is to be regarded as the product of an abortive attempt at the formation of a solid yolk-mass, such as is found in the Monotreme ovum. By its elimination the potentially yolk-laden telolecithal ovum becomes converted into a secondarily homolecithal, holoblastic one. All the evidence is held to support the conclusion that the Marsupials are descended from oviparous ancestors with ineroblastic ova.

(b) Cleavage. - Cleavage begins in the uterus, is total, and at first equal and of the radial type. The first two cleavage planes are meridional and at right angles to each other. The resulting four equal-sized blastomeres lie disposed radially around the polar diameter like those of the Monotreme (not in pairs at right angles to each other as in Eutheria), and enclose a segmentation cavity open above and below, their upper ends partially surrounding the yolk-body. The third cleavage planes are again meridional, each of the four blastomeres becoming subdivided equally into two. The resulting eight cells form an equatorial ring in contact with the inner surface of the sphere formed by the egg-envelopes. They


contain deutoplasmic material, which is, however, located mainly in their lower halves. The ensuing fourth cleavages are equatorial, and in correlation with the just-mentioned disposition of the deutoplasm, are unequal and qualitative, each of the eight blastoraeres becoming subdivided into an upper smaller and clearer cell, with relatively little deutoplasm fairly uniformly dispersed through the cytoplasm, and a lower larger, more opaque cell Avith much deutoplasm, mainly located in a broad zone in the outer portion of the cell-body. A 16-celled stage is thus produced in which the blastomeres are characteristically arranged in two superimposed rings, each of eight cells, an upper of smaller, clearer cells next the yolk-body, and a lower of larger, denser cells. The former is destined to give origin to the formative or embryonal region of the blastocyst wall, the latter to the non-formative or extra-embryonal region of the same.

(c) Formation of the Blastocyst. - There is in the Marsupial no morula stage as in Butheria, the blastomeres proceeding directly to form the wall of the blastocyst. The cells of the two rings of the 16-celled stage divide at first meridionally and then also equatorially, the division planes being always vertical to the surface. The daughter-blastomeres so produced, continuing to divide in the same fashion, gradually spread towards opposite poles in contact with the inner surface of the fii-m sphere formed by the zona and the thickened shell-membrane. Eventually they form a complete cellular lining to the said sphere and it is this which constitutes the wall of the blastocyst. The latter is accordingly unilaminar at its first origin, and it remains so in Dasyurus until it has attained, as the result of active gi'owth accompanied by the imbibition of fiuid from the uterus, a diameter of 4-5 mm. It consists of two parts or regions, distinct in origin and in destiny, and clearly marked off from each other in later blastocysts by a definite junctional line approximately equatorial in position, viz. an upper, embryonal or formative region derived from the upper cell-ring of the 16-celled stage, and a lower, extra-embryonal or nonVOL. 56, PART 1. NEW SERIES. 6



formative region derived from tlie lower cell-ring of the same stage.

(d) Later History of the Two Region s of the Blastocyst Wall (for details see pp. 72-74). - From the embryonal region are derived the embryonal ectoderm and the entire entoderm of the vesicle. I conclude^ therefore, that it is tlie homologue of the inner cell-mass or embryonal knot of the Eutherian blastocyst. The extra-embryonal region directly furnishes the outer extra-embryonal layer of the vesicle wall, i. e. the outer layer of the omphalopleure and chorion of later stages. Assuming, as the facts of comparative anatomy and palaeontology entirely justify us in doing, that the Mammals are monophyletic and of reptilian origin, and further assuming that the foetal membranes are homologous structures throughout the Amniotan series (also in my view a perfectly justifiable assumption)^, then the homologies of this extraembryonal region of the Marsupial blastocyt are not far to seek. It is clearly the homologue of the extra-embryonal ectoderm of the Sauropsidan and Monotreme egg, and the homologue also of the outer enveloping layer of the Eutlierian blastocyst, to which Hubi'echt has given the special name of “ trophoblast.” In my view the trophoblast is none other than extra-embryonal ectoderm which in the viviparous mammals, in correlation with the intra-uterine mode of development, has acquired a special significance for the nutrition of the embryo.

These, then, are my conclusions, and to me they seem on general grounds perfectly obvious, viz. : (1) that the embryonal or formative region of the unilaminar Marsupial blastocyst is the homologue of the inner cell-mass or

  • How Assheton can maintain f 09, p. 266) “ that the amnion of the

rabbit is not more homologous to the amnion of the Sauropsidan than the homy teeth of Ornithorhynchns ai-e homologous to the true teeth of the mammal or reptile, which they have supplanted,” how he can hold this view and yet proceed to utilise the presence of the amnion as one of the leading charactei-s distinguishing the Amniota from the Anamnia, I fail to comprehend. Surely the presence of a series of purely analogous structures in a group is of no classificatory value.



imposed cell-viiigs, respectively and non-formative cell-rings of formative (emlDryonal) and non- the Metatherian. formative (extra-embryonal) in significance.




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embryonal knob of tlie Eutberiaii blastocyst ; and (2) that the extra-embryonal or noii-formative region of the same is the homologne of the extra-embryonal ectoderm of the Sauropsida and Monotremata and of the trophoblast of the Eutheria.

As regards conclusion (1) there is not likely to be much difference of opinion, but as regards (2), whilst perhaps the majority of embryologists support the obvious, not to say common-place view which I here advocate, it seems certain that it will prove neither obvious nor acceptable to those mammalian embryologists (I refer specifically to my friends Professor A. A. W. Hubrecht and Mr. R. Asshetou) who, with only Selenka^s account of eaidy Marsupial ontogeny before them, have formulated other and quite divergent views as to the morphological nature of the outer enveloping layer of the Eutherian blastocyst. It is therefore necessary to discuss this question further, though I would fain express my conviction that had the observations recorded in this paper been earlier available, much vain speculation as to the phytogeny of the trophoblast might possibly have been avoided.