|
|
Line 1,341: |
Line 1,341: |
| covering layer of trophoblast (Deckschicht, Kauber's layer) | | covering layer of trophoblast (Deckschicht, Kauber's layer) |
| is absent and there is no entypy of the primary germ-layers | | is absent and there is no entypy of the primary germ-layers |
| (cf. p. 111). | | (cf. p. 111). |
| | |
| | |
| ==Chapter V. - Some Early Stages op Perameles and Macropods==
| |
| | |
| The early material of Perameles and Macropus at my
| |
| disposal comprises only a small number of stages, but is of
| |
| special importance, since it enables me to demonstrate that
| |
| so far as these particular stages are concerned, the early
| |
| developmental phenomena in these forms are essentially the
| |
| same as in Dasyurus, and thus affords ground for the belief
| |
| that there is one common type of early development throughout the series of the Marsupialia. Moreover, it is of interest
| |
| since it reveals the. existence of what might be termed
| |
| | |
| | |
| 75
| |
| | |
| | |
| THE EAELY DEVELOPMENT OP THE MAESUPI ALIA.
| |
| | |
| specific differences in the early development of these Marsupials, especially in regard to the time of appearance of the
| |
| entoderm. In Dasyurus, it will be remembered, the primitive
| |
| entoderm cells first become definitely recognisable as internally situated cells in vesicles 4‘5 mm. in diameter. In
| |
| Perameles they occur in vesicles just over 1 rnm. in diameter,
| |
| while in Macropus they are already present in a blastocyst
| |
| only -35 mm. in diameter, so that it would appear that the
| |
| entoderm is differentiated much earlier in the higher, more
| |
| specialised types than in the more generalised forms. This
| |
| difference in time of appearance of the entoderm is perhaps
| |
| to be correlated with a difference in size of the ovarian ova
| |
| in the three genera mentioned.
| |
| | |
| | |
| 1. Perameles.
| |
| | |
| The earliest material of Perameles I possess consists of two
| |
| eggs of P. obesula, which I owe to the skill and enthusiasm
| |
| of my friend Mr. S. J. M. Moreau, of Sydney. Egg -Ameasures '23 mm. in diameter, and egg B, ‘24 x ‘23 mm.
| |
| The former consists of thirty-two cells, the latter of thirty. In
| |
| both the shell-membrane has partially collapsed, but the general
| |
| plan of arrangement of the blastomeres can still fairly readily
| |
| be made out. Fig. 51, PI. 3, represents a micro-photograph
| |
| of a section of egg B, the better of the two. It shows the
| |
| .shell-membrane (nearly '005 mm. thick) externally, considerable remains of the albumen between that and the
| |
| deeply stained zona, and then, closely applied to the inner
| |
| surface of the latter, the blastomeres arranged in the form of
| |
| an inverted D, so as to enclose a central space, open below
| |
| as the figure stands. This latter opening extends through
| |
| the series, and it seems probable that there was a corx*esponding one opposite to it in the intact egg. Evidently we
| |
| have hei'e a stage in the formation of the blastocyst, in which
| |
| the blastomeres are in course of spreading towards one or
| |
| both of the poles of the sphere formed by the egg-envelopes.
| |
| | |
| | |
| 76
| |
| | |
| | |
| J. r, HILL,
| |
| | |
| | |
| â– just as liappeus in the corresponding' stage of Dasyurus (cf.
| |
| fig. 51 with fig. 31j though the latter represents a somewhat
| |
| older stage in Dasyurus). The blastocyst-wall here appears
| |
| relatively more extensive than in the 32-celled stage of
| |
| Dasyurus, an apparent difference which may perhaps be accounted for by the difference in size of the respective eggs
| |
| (•24 mm. as compared with '36 mm.) . The blastomeres situated
| |
| adjacent to the opening and those on the right side of the
| |
| figure tend to be more flattened and of greater superficial extent than the remainder, but I can recognise no
| |
| difference in the cytological characters of the cells. The
| |
| space or cleavage cavity enclosed by the blastomeres is partly
| |
| occupied by a granular coagulum, and towards the opening
| |
| there is present a lightly staining reticular mass, which
| |
| i*ecalls the yolk-body of Dasyurus, though I am not prepared
| |
| to affirm that it is of that significance. The fixation of the
| |
| specimen is not quite perfect.
| |
| | |
| My next stage of Perameles is constituted by a blastocyst
| |
| of P. nasuta, for which I am again indebted to Mr. Moreau
| |
| measuring in the preserved condition '29 x '26 mm. Pig. 52,
| |
| PI. 3, shows a section of this blastocyst. Structurally,
| |
| it corresponds in all essential respects with the '43 mm.
| |
| blastocyst of Dasyurus, figured on the same plate (fig. 33).
| |
| The blastocyst Avail is complete and unilamiuar throughout.
| |
| It is distinguishable into tAvo regions, a more extensive region
| |
| over Avhich the cells are large and flattened and a less extensive,
| |
| composed of smaller but thicker cells (left side of fig. 52).
| |
| In the early blastocysts of Dasyurus, it may be recalled, the
| |
| evidence showed that the region of more flattened cells is
| |
| formative in significance, that of more bulky cells, non-formative. It is possible the same holds good for this Perameles
| |
| blastocyst. On the other hand, the structural condition of
| |
| the stage next to be described rather supports the vieAv that
| |
| the smaller region, composed of plumper cells, is in this case
| |
| formative. That view seems to me the more probable of the
| |
| two, but there is a considerable difference in size betAveen the
| |
| present blastocyst and those next available, so that it is
| |
| | |
| | |
| THE EAKLy DEVELOPMENT OP THE MARSUPIALIA.
| |
| | |
| | |
| 77
| |
| | |
| | |
| impossible to decide this point witli certciinty. The blastocyst cavity is partly occupied by coagulnm. There are no
| |
| cells present in it, but the question of the presence of a yolkbody must remain open. The shell-membrane (‘0045 mm. in
| |
| thickness) and zona are in close apposition.
| |
| | |
| Following this early blastocyst, I have three vesicles of
| |
| P. nasuta, two of them measuring 1‘3 mm. in diameter,
| |
| the other PI mm. In their stage of development they
| |
| agree pretty closely with the 4'5-5 mm. vesicles of Dasyurus,
| |
| referred to in the preceding pages under the designation
| |
| 6, '04, the entoderm being in process of differentiation. The
| |
| formative region was readily distinguishable in the intact
| |
| vesicles as a darker patch occupying about three eighths of
| |
| the surface extent of the wall. In section (PI. 8, figs. 80, 81)
| |
| it is characterised by its greater thickness as compared with
| |
| the non-formative or trophoblastic region, and by the
| |
| presence below it of numbers of primitive entodernial cells.
| |
| Compared with the corresponding stage in Dasyurus, the
| |
| chief difference consists in the relatively much greater thickness of the cells of the formative region in the Perameles
| |
| vesicle. The latter cells are here already more or less definitely cubical in shape, their thickness varying from '09
| |
| mm. to '015 mm., and altogether they form a layer of a much
| |
| more uniformly thickened character than that of the 6, '04
| |
| vesicles of Dasyurus. The trophoblastic ectoderm (figs. 80,
| |
| 81, tr. ect.) is composed of somewhat flattened cells, .varying
| |
| in thickness from ‘005 to '008 mm.
| |
| | |
| The primitive entodermal cells (figs. 80, 81, ent.) are
| |
| present below the formative region in fair abundance, more
| |
| especially around the periphery of the same, which may thus
| |
| appear somewhat thickened (fig. 81). 4'he cells vary in size
| |
| from ‘01 X '007 mm. to '024 x '009 mm., and they stain on the
| |
| whole somewhat more deeply than the formative cells, to
| |
| whose under-surface they are closely applied. They occur
| |
| groups. Mitotic figures are frequently met
| |
| with in the cells of the formative ai'ea (observe the obliquely
| |
| disposed figure in one of the formative cells in fig. 81), and
| |
| | |
| | |
| 78
| |
| | |
| | |
| J. r. HILL.
| |
| | |
| | |
| â– they also occur in the primitive entodermal cells. Examination of the sections leaves no doubt in one's mind as to the
| |
| source of the entodermal cells. They are undoubtedly derived
| |
| from the formative region of the vesicle wall. The 'shellmembrane has a thickness of about '0027 mm.
| |
| | |
| 2. Macro pus.
| |
| | |
| Of Macropus the earliest stage I have examined is a blastocyst of M. ruficollis, -25 x *21 mm. in diameter. It is not
| |
| in a quite perfect state of preservation, but is in a sufficiently
| |
| good condition to enable me to say that the wall is complete
| |
| and unilaminar throughout, just as in the ‘29 x "26 mm.
| |
| blastocyst of Perameles. The shell-membrane has a thickness
| |
| of about -005 mm., and there are still remains of the albumen
| |
| between it and the zona.
| |
| | |
| My next stage (figs. 82-85) is a blastocyst of the same
| |
| species, *35 mm. in diameter. It unfortunately suffered in
| |
| preparation, but practically the whole of the formative area
| |
| of the blastocyst wall and part of the trophoblastic ectoderm
| |
| are comprised in the sections (PI. 9, fig. 82), so that it is still
| |
| possible to make out its chief structural features. In its stage
| |
| of development this blastocyst closely agrees with the last
| |
| described blastocysts of Perameles. The formative area of
| |
| the wall is perfectly distinct in the sections because of its
| |
| greater thickness and the presence below it of the primitive
| |
| entodermal cells. It attains its gi-eatest thickness (*027 mm.)
| |
| peripherally, whilst it is thinnest centrally (*006 mm.), so that,
| |
| taken as a whole, it is not quite such a uniformly thickened
| |
| layer as is that of the Perameles blastocysts. Primitive entodermal cells are present below it, but not in great abundance
| |
| (figs. 82, 84, 85, ent.). In fig. 83, a formative cell is seen in
| |
| division, the axis of the spindle being oblique to the surface.
| |
| The trophoblastic ectoderm (figs. 82, 83, tr. ect.) is composed
| |
| of the usual flattened cells, and varies in thickness from
| |
| *005 to *0067 mm.
| |
| | |
| In the blastocyst cavity, adjacent to the trophoblastic
| |
| | |
| | |
| THE EARLY DEVELOPMENT OP TliE MARSDPIALIA.
| |
| | |
| | |
| 79
| |
| | |
| | |
| ectoderm on the left side of fig. 82, there is visible a small
| |
| spherical cell similar to the degenerate cells met with in
| |
| blastocysts of Dasyurus.
| |
| | |
| My last stage of M. ruficollis comprises an excellently
| |
| preserved blastocyst, measuring '8 mm. in diameter, in which
| |
| the embryonal ectoderm and the entoderm are definitely
| |
| established. It thus corresponds to the 8, '01 stage of
| |
| Dasyurus (blastocysts o - 5'5 mm. diameter). The embryonal
| |
| area is circular and measures '468 mm. in diameter. Its
| |
| constituent cells are cubical and from '008 to ‘OlS mm. in
| |
| thickness, Avhilst the trophoblastic ectoderm is formed of
| |
| flattened cells, -006 ram. in thickness. The entoderm is
| |
| present as a continuous layer of attenuated cells below the
| |
| embryonal ectoderm, and it probably also forms a continuous
| |
| layer below the trophoblastic ectoderm. Entodermal cells are
| |
| certainly pi*esent over the lower polar region of the vesicle,
| |
| but it is difficult to be certain from the sections whether or not
| |
| they form a perfectly continuous layer. The shell membrane
| |
| has a thickness of •0026 mm.
| |
| | |
| I have a corresponding blastocyst of Petrogale penicillata •915 mm. in diameter, with an oval, embryonal area
| |
| •525 X ^45 mm. in diameter, and a later blastocyst of M.
| |
| ruficollis P46 mm. in diameter, with a circular embryonal
| |
| area '57 mm. in diameter.
| |
| | |
| 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
| |
| | |
| | |
| 80
| |
| | |
| | |
| 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
| |
| | |
| | |
| THE EARLY DEVELOPMENT OF THE MARSUPIALIA. . »1
| |
| | |
| 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
| |
| | |
| | |
| 82
| |
| | |
| | |
| J. P, HILL.
| |
| | |
| | |
| 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.
| |
| | |
| | |
| THE EARLY DEVELOPMENT OP THE MAllSUPIALIA
| |
| | |
| | |
| 83
| |
| | |
| | |
| | |
| imposed cell-viiigs, respectively and non-formative cell-rings of
| |
| formative (emlDryonal) and non- the Metatherian.
| |
| formative (extra-embryonal) in
| |
| significance.
| |
| | |
| | |
| 84
| |
| | |
| | |
| J. P. HILL
| |
| | |
| | |
| 3
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| |
| | |
| | |
| THE EARLY DEVELOPMENT OP THE MARSUPIALIA.
| |
| | |
| | |
| 85
| |
| | |
| | |
| 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.
| |
| | |
| Chapter VII. - The Early Ontogeny op the Mammalia in
| |
| THE Light op 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
| |
| | |
| | |
| 86
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| falls into line with that of Eutheria, and with what we know
| |
| of the early development of the Prototheria, but furnishes
| |
| ns with the key to the correct interpretation of that extraordinarily specialised developmental stage, the Eutherian
| |
| blastocyst. In particular I hope to show that the description
| |
| which I have been able to give of the mode of formation of
| |
| the' Marsupial blastocyst, bridges in the most satisfactory
| |
| fashion the great gap which has till now existed in our
| |
| knowledge of the way in which the transition from the
| |
| Monotrematous to the Eutherian type of development has
| |
| been effected.
| |
| | |
| 1. The Early Development of the Monotremata.
| |
| | |
| Our knowledge of the early development of the oviparous
| |
| mammals is admittedly still far from complete. Nevertheless
| |
| it is not so absolutely fragmentary that it can be passed over
| |
| in any general discussion of early mammalian ontogeny, and
| |
| I certainly cannot agree with the opinion of Assheton ('08,
| |
| p. 227) that from it “we gain very little help towards the
| |
| elucidation of Eutherian development.†On the contrary, I
| |
| think that the combined observations of Semon ('94), and
| |
| Wilson and Hill ('07) shed most valuable light on the early
| |
| ontogenetic phenomena in both the Metatheria and Eutheria.
| |
| I propose therefore to give here a very brief resume of the
| |
| chief results of these observers,^ and at the same time to
| |
| indicate how the knowledge of early Monotreme ontogeny
| |
| we possess, limited though it be, does help us to a better
| |
| understanding of the phenomena to which I have just
| |
| referred.
| |
| | |
| The ovum, as is well known from the observations of
| |
| Caldwell. ('87), is Reptilian in its character in all but size.
| |
| It is yolk-laden and telolecithal, the yolk consisting of
| |
| discrete yolk-spheres, and it is enclosed outside the zona
| |
| (vitelline membrane) by a layer of albumen and a definite shell.
| |
| | |
| * In so doinff I have largely utilised the phraseology of Wilson and
| |
| Hill's paper ('07).
| |
| | |
| | |
| THE EARLY DEVELOPMENT OP THE MARSUPIALIA. 87
| |
| | |
| | |
| At the moment of entering the oviduct it has a diameter of
| |
| 3‘5-4 mm. (2‘5-3 mm. according to Caldwell), and is therefore
| |
| small relatively to that of a reptile of the same size as the
| |
| adult Monotreme, but large relatively to those of other
| |
| mammals, being about twelve times larger than that of
| |
| Dasyurus, and about eighteen times larger than that of the
| |
| rabbit.
| |
| | |
| Cleavage is meroblastic. The first two cleavage planes are
| |
| at right angles to each other, as iii the Marsupial, and divide
| |
| the germinal disc into four approximately equal-sized cells
| |
| (Semon, Taf. ix, fig. 30). Each of these then becomes subdivided by a meridional furrow into two, so that an 8-celled
| |
| stage is produced, the blastomeres being arranged symmetrically, or almost symmetrically, on either side of a median line,
| |
| perhaps corresponding to the primary furrow (Wilson and Hill,
| |
| p. 37, text-figs. 1 and 2). Imagine the yolk removed and the
| |
| blastomeres arranged radially, and we have at once the open
| |
| ring-shaped 8-celled stage of Dasyurus. The details of the
| |
| succeeding cleavages are unknown. Semon has described a
| |
| stage of about twenty-four cells (Semon, Taf. ix, fig.31),inwhich
| |
| the latter formed a one-layered circular plate with no evidence
| |
| of bilateral symmetry, and this is succeeded by a stage also
| |
| figured by Semon (figs. 32 and 33, cf. also Wilson and Hill,
| |
| PI. 2, fig. 2), in which the blastoderm has become sevei'al
| |
| cells thick, though it has not yet increased in surface extent.
| |
| It is bi-convex lens-shaped in section, its lower surface being
| |
| sharply limited from the underlying white yolk. No nuclei
| |
| are recognisable in the latter, either in this or any subsequent
| |
| stage, nor is there ever any trace of a syncytial germ-wall,
| |
| features in which the Monotreme egg differs from the
| |
| Sauropsidan.
| |
| | |
| The next available stage, represented by an egg of Ornithorhynchus, described by Wilson and Hill ('07, p. 38, PI. 2, fig.
| |
| 4), and by an egg of Echidna, described by Semon ('94, p. 69,
| |
| figs. 22 and 33), is separated by a considerable gap from the
| |
| preceding, and most unfortunately so, since it belongs to the
| |
| period of commencing formation of the germ-layers. The
| |
| | |
| | |
| 88
| |
| | |
| | |
| 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
| |
| | |
| | |
| 89
| |
| | |
| | |
| THE EARLY DEVELOPMENT OF THE MARSUPIALIA.
| |
| | |
| 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
| |
| | |
| | |
| 90
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| 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.
| |
| | |
| | |
| THE EAHLY DEVELOPMENT OF THE MARSUPIALIA. 91
| |
| | |
| | |
| 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 authorsâ€
| |
| (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
| |
| | |
| 92
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| 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.
| |
| | |
| | |
| THE EARLY DEVELOPMENT OP THE JIARSUPIALIA. 93
| |
| | |
| | |
| 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
| |
| | |
| | |
| 94
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| 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
| |
| | |
| | |
| THE EARLY DEVELOPMENT OF THE MARSUPIALIA. 95
| |
| | |
| | |
| 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
| |
| | |
| | |
| 96
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| must assume to have taken place gi-adually and in correlation
| |
| with the longer retention of the egg in the oviduct, the
| |
| elaboration of the uterine portion of the same as an actively
| |
| secretory organ, and the evolution of the mammary apparatus.
| |
| The Monotremes thus render concrete to us one of the first
| |
| great steps in mammalian evolution so far as developmental
| |
| processes are concerned, viz. the substitution for intra-ovular
| |
| yolk of nutrient material furnished directly by the mother to
| |
| the developing egg or embryo. We see in them the beginnings of that process of substitution of uterine for ovarian
| |
| nutriment which reaches its culmination in the Eutheria with
| |
| their microscopic yolk-poor ova and long intra-uterine period
| |
| of development. The Marsupials show us in Dasyurus an
| |
| interesting intervening stage so far as the ovum is concerned,
| |
| in that this, though greatly reduced as compared with that
| |
| of the Monotreme, still retains somewhat of its old tendencies
| |
| and elaborates more yolk-material than it can conveniently
| |
| utilise, with the result that it has to eliminate the surplus
| |
| before cleavage begins. But as coucerns their utilisation of
| |
| intra-uterine nutriment, they have specialised along their
| |
| own lines, and instead of exhausting the possibilities implied
| |
| by the presence of that, they have extensively elaborated
| |
| the mammary apparatus for the nutrition of the young, born
| |
| in a relatively immature state, after a short period of intrauterine life (cf. Wilson and Hill [T7, p. 580]).
| |
| | |
| In view of the fact that the young Monotreme enjoys three
| |
| developmental periods, viz. intra-uterine, incubatory, and
| |
| lactatory, the question might be worthy of consideration
| |
| whether it may not be that the Marsupial has merged the
| |
| incubatory period in the lactatory, the Eutherian the same in
| |
| the intra-uterine.
| |
| | |
| | |
| 2. The Early Development of the Metatheria and
| |
| | |
| Eutheria.
| |
| | |
| It will have become evident Horn the foregoing that the
| |
| Metatherian mode of early development is to be regarded as
| |
| | |
| | |
| THE EARLY DEVELOPMENT OP THE MAESUPIALIA.
| |
| | |
| | |
| 97
| |
| | |
| | |
| 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
| |
| | |
| VOL. 56, PART 1. NEW SERIES. 7
| |
| | |
| | |
| 98
| |
| | |
| | |
| t.C.TTV. (€cj
| |
| | |
| trect.
| |
| | |
| | |
| i.c.nv.ffo.)
| |
| | |
| | |
| | |
| tr.ect.
| |
| | |
| | |
| cunrvTh.c.
| |
| 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).
| |
| | |
| | |
| THE EAltLY l.)E VET;01â– '^[ENâ– T OF THE MARSUFIALIA. 99
| |
| | |
| | |
| 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,â€
| |
| 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.â€
| |
| The latter layer he regards as corresponding to the extraembryonal ectoderm of the Sauropsida, and points out that
| |
| | |
| | |
| 100
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| “ 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.
| |
| | |
| | |
| THE EARLY DEVELOPMENT OP THE MARSHPIALIA. 101
| |
| | |
| | |
| 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] â€).
| |
| | |
| 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,â€
| |
| 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
| |
| | |
| | |
| 102
| |
| | |
| | |
| 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 â€
| |
| 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.
| |
| | |
| | |
| THE EARLY DEVELOPMENT OF THE MARSUPFALIA. 103
| |
| | |
| 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.
| |
| | |
| | |
| 104
| |
| | |
| | |
| 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
| |
| | |
| | |
| THE EARLY EEVELOrMENT OF THE MARSUPIALIA. 105
| |
| | |
| | |
| 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.â€
| |
| 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
| |
| | |
| | |
| 106
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| 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 â€
| |
| | |
| | |
| THE EAKLY HEVELOrMENT OL<' THE MAESOPIALIA. 107
| |
| | |
| {'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 noticedâ€
| |
| ('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
| |
| | |
| | |
| 108
| |
| | |
| | |
| .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
| |
| layerâ€). It is, of course, this envelojDing layer or trophoblast which Hubrecht interprets as a larval membrane.
| |
| It fulfils the conditions, and were the Eutheria the only
| |
| Vertebrates known to us, the idea might be plausible
| |
| enough.
| |
| | |
| Turning now to the Metatheria, and I'emembering that these,
| |
| according to Hubrecht, are descended from the Eutheria, we
| |
| should naturally expect to find the supposed larval membrane
| |
| fully developed, with all its ancestral relations ; and so we do
| |
| if we are content to accept Hubrecht's interpretation of
| |
| Selenka's results and figures in the case of Didelphys. The
| |
| “ urentodermzelle †of Selenka is for Hubrecht “ undoubtedly
| |
| the mother-cell of the embryonic knob,†the ectoderm of
| |
| Selenka is manifestly the trophoblast - a complete larval
| |
| layer. It is no doubt unfortunate that Hubrecht had to rely
| |
| on the work of Selenka as his source of information on the
| |
| early development of Marsupials, but it must be remembered
| |
| that he reads his own views into Selenka's figures. On the
| |
| basis of my own observations on the early ontogeny of Marsupials, I have no hesitation in affirming that a larval membrane, in the sense of Hubrecht, does not exist in any of the
| |
| forms (Dasyurus, Perameles, Macropus) studied by me. The
| |
| observations recorded in the preceding pages of this paper
| |
| demonstrate, in the case of Dasyurus without the possibility
| |
| of doubt, the entire absence of any cellular layer external
| |
| to the formative region of the blastocyst, i.e. in a position
| |
| corresponding to that occupied by Rauber's layer in Eutheria,
| |
| whilst in the case of Perameles and Macropus, they yield not
| |
| | |
| | |
| THE EAULY DEVELOPMENT OP THE MAESUPIALTA. 109
| |
| | |
| | |
| 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
| |
| | |
| | |
| 110
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| 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,â€
| |
| 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
| |
| | |
| | |
| THE EAELY DEVELOPMENT OP THE MAllSUPIALIA. Ill
| |
| | |
| | |
| 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
| |
| | |
| Blastocyst.
| |
| | |
| If, now, on the basis of the homologies I have ventm-ed to
| |
| advocate in the preceding pages, we proceed to compare the
| |
| Metatherian with the Eutherian blastocyst, we have to note
| |
| that, whereas in the latter the extra-embryonal or trophoblastic ectoderm alone forms the blastocyst wall in early
| |
| stages and completely encloses the embryonal knot, in the
| |
| former, the homologous parts, viz. the non-formative or exti'aembryonal and the formative or embryonal regions, both
| |
| enter into the constitution of the unilaminar blastocyst
| |
| wall, there being no such enclosure of the one by the
| |
| other as occurs in the Eutherian blastocy.st (Text-fig. 2, p. 98).
| |
| It is characteristic of the Marsupial as of the Monotreme that
| |
| the embryonal region is from the first superficial and freely
| |
| exposed. It is spread out as a cellular layer and simply
| |
| forms part of the blastocyst wall or blastoderm. It is equally
| |
| characteristic of the Eutherian that the homologous part, the
| |
| embryonal knot, has at first the form of a compact mass,
| |
| which is completely enclosed by the trophoblastic ectoderm.
| |
| | |
| | |
| 112
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| 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).
| |
| | |
| | |
| THE EARLY DEVELOILMENT OP THE MARSUriAl.IA, 113
| |
| | |
| | |
| 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.
| |
| | |
| VOL. 56, PART 1. NEW SERIES.
| |
| | |
| | |
| 8
| |
| | |
| | |
| 114
| |
| | |
| | |
| ,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
| |
| | |
| | |
| THE EARLY DEVELOPMENT OP THE MAESUPIALIA. 115
| |
| | |
| | |
| 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.
| |
| | |
| | |
| 116
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| 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
| |
| | |
| THE EARLV DEVELOPMENT OF THE MARSUPIALIA. 117
| |
| | |
| 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
| |
| ectoderm.
| |
| | |
| | |
| 118
| |
| | |
| | |
| J. P. HILL.
| |
| | |
| | |
| 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
| |
| | |
| | |
| THE EARLY DEVELOPMENT OF THE MARSUPIALIA. 119
| |
| | |
| | |
| enveloping layer which produces this peculiar entypic condition in the Eutherian blastocyst, I would interpret, then, as
| |
| a purely adaptive phenomenon, which in the given circumstances effects in the simplest possible way the early completion
| |
| of the blastocyst wall, and whose origin is to be traced to
| |
| that reduction in size and in its envelopes which the Eutherian
| |
| ovum has suffered in the course of phylogeny, in adaptation
| |
| to the conditions of intra-uterine development. In particular,
| |
| starting with a shell-bearing ovum, already minute and
| |
| undergoing its development in utero, I see in the loss of
| |
| the shell such as has occurred in the Eutheria an intelligible
| |
| explanation of the first origin of those adaptations which
| |
| culminate in the condition of entypy. I am therefore wholly
| |
| unable to accept the view of Hubrecht (^08, p. 78), that " what
| |
| Selenka has designated by the name of Entypie is - from
| |
| our point of view - no secondary phenomenon, but one
| |
| which repeats very primitive featui*es of separation between
| |
| embryonic ectoderm and larval envelope in invertebrate
| |
| ancestors.â€
| |
| | |
| 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
| |
| | |
| | |
| 120
| |
| | |
| | |
| J. P, HILL.
| |
| | |
| | |
| Prozess auch in solclieu Eiblasen dei- Saugetiere vorkommen
| |
| kanii, die iiberhaupt nichb, odei- erst spiiter mifc dem Uterus
| |
| verwachsen, so kaiiu die Keimfeld-Entypie zwar durch die
| |
| frube Verwacbsung veraiilasst, aber nicht ausscldiesslich
| |
| liervorgerufeii werclen.†He goes on to remark that - “Die
| |
| Vorbedingimgeti zur Eutypie miissen in der Struktur der verwachseuden Eiblase gesucht werden/^ and expi-esses his
| |
| agreement with the views of Van Beneden as to tlie significance to be attributed to the early cleaviige phenomena in
| |
| Eutheria.
| |
| | |
| The attitude of the illustrious Belgian embryologist whose
| |
| loss ws have so recently to deplore, towards this problem is
| |
| clearly set forth in the last memoir which issued from his
| |
| hand. “Je suis de ceux,^' he wrote (T9, p. 332), “qui pensent
| |
| que toute Pembryologie des Mammiferes placentaires temoigue
| |
| quTls derivent d'animaux qui, comme les Sauropsides et les
| |
| Mouotremes, produisaieut des oeufs meroblastiques. Je ne
| |
| puis a aucun point de vue me rallier aux idees contraires formulees eb defendues par Hubrecht. L^hypothese de Hubrecht
| |
| se heurte a des difiicultes morpliologiques et physiologiques
| |
| insurmontables : elle laisse inexpliquee Pexistence, chez les
| |
| Mammiferes placentaires, d'une vesicule ombilicale et dTne
| |
| foule de caracteres commnns a tons les Amniotes et distiuctifs
| |
| de ces auimaux.'^ Holding this view of 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.â€
| |
| | |
| 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 EAELY DEVELOPMENT UE THE MAKSUPJALIA. 121
| |
| | |
| | |
| the uterus. . . . The embryonic evidence of the common
| |
| | |
| origin of Mammalia and Sauropsida, both as concerns the
| |
| formation of the layers and of the embryonic membranes is
| |
| as clear as it can be.'''
| |
| | |
| That view of tlie derivation of the Mammalia receives, I
| |
| venture to think, striking confirmation from the observations
| |
| and conclusions set forth in the preceding pages of this
| |
| memoir, and from it as a basis all attempts at a phylogenetic
| |
| interpretation of the early ontogenetic phenomena in the
| |
| Mammalia must, I am convinced, take their origin. Such an
| |
| attempt I have essayed in the foregoing pages, with what
| |
| success the reader must judge.
| |
| | |
| | |
| Addendum.
| |
| | |
| The memoir of Prof. 0. Van der Stricht, entitled “La structure de I'cBuf des Mammiferes (Chauve-souris, Vesperugo
| |
| noctula) : Troisieme Partie†(‘Mem. de PAcad. roy. de
| |
| Belgique,' 2nd ser., t. ii, 1909), came into my hands only
| |
| after my own paper had readied its final form, and therefore
| |
| too late for notice in the body of the text. In this extremely
| |
| valuable contribution, Van der Stricht gives a detailed
| |
| account of the growth, maturation, fertilisation, and early
| |
| cleavage-stages of the ovum of Vesperugo, illustrated by a
| |
| superb series of drawings and photo-micrographs. All I can
| |
| do here, however, is to direct attention to that section of the
| |
| paper entitled “ Phenomeues de deutoplasmolyse an pole
| |
| vegetatif de I'ceuf†(pp. 92 - 96), in which the author describes
| |
| the occurrence in the bat's ovum of just such a process of
| |
| elimination of surplus deutoplasmic material as I have
| |
| recorded for Dasyurus. Van der Stricht's interpretation of
| |
| this phenomenon agrees, I am glad to find, with my own.
| |
| He writes (pp. 92-93): “ Ce deutoplasme rudimentaire, i\
| |
| peine ebauche dans I'ovule des Mammiferes, parait etre
| |
| encore trop abundant dans I'oeuf de Chauve-souris, car ces
| |
| materiaux de reserve, en partie inutiles, sont partiellement
| |
| elimines, expulses de la cellule.â€
| |
| | |
| | |
| 122
| |
| | |
| | |
| .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,â€
| |
| | |
| ‘ 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
| |
| Trophoblast,†‘ Quart. Journ. Micr. Sci.,' vol. 41.
| |
| | |
| '08. “ The Blastocyst of Capra, with Some Remarks upon the
| |
| | |
| Homologies of the Germinal Layers of Mammals,†‘Guy's
| |
| Hospital Reports,' vol. Ixii.
| |
| | |
| '09. “Professor Hubrecht's Paper on the Early Ontogenetic
| |
| | |
| Phenomena in Mammals ; An Appreciation and Criticism,â€
| |
| ‘ Quart. Journ. Micr. Sci.,' vol. 54.
| |
| | |
| | |
| 123
| |
| | |
| | |
| THE EAELY DEVELOPMENT OF THE MARSUPIALIA.
| |
| | |
| '97. Bonnet. R. - “ Beitriige zur Embvyologie des Himdes,†‘ Anatomische Hefte,' Bd. ix.
| |
| | |
| '01. “ Erste Fortsetzimg,†‘ Anatomisclie Hefte,' Bd. xvi.
| |
| | |
| '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.
| |
| Micr. Sci.,' vol. 40.
| |
| | |
| '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,â€
| |
| | |
| ‘ 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 .
| |
| | |
| | |
| 124
| |
| | |
| | |
| 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,'
| |
| IV (1 and 2), “ Das Opossum (Didelphys virginianaj,†Wiesbaden.
| |
| | |
| '91. ‘‘ Beutelfuchs und Kiinguruhratte ; zur Entsteliungs
| |
| geschichte der Amnion der Kantjil (Tragulus javanicus) ;
| |
| Att'en Ost-Indiens,†‘ Studien fiber Entw. der Tiere,' H. 5, Erste
| |
| Hiilfte.
| |
| | |
| '00. ‘ Studien hber Entw. der Tiere,' H. 8, Menschenaffen.
| |
| | |
| “ III, Entwickelung des Gibbon (Hylobates und Sianianga),â€
| |
| Wiesbaden : 0. W. Kreidel.
| |
| | |
| '94. Semon, R. - “Zur Entwickelungsgeschichte der Monotremen,â€
| |
| ‘ Zool. Forschungsreisen iin Australien, etc.,' Bd. ii. Lief 1.
| |
| | |
| '95. Sobotta, J. “ Die Befruchtung und Furchung des Eies der Mans,â€
| |
| ‘ 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.
| |
| | |
| '80 “ Recherches sur I'emliryologie des Maminiferes, la forma
| |
| tion des feuillets chez le Lapin,†‘ Arch, de Biologie,' t. i.
| |
| | |
| '99 “ Recherches sur les premiers Stades du developpement du
| |
| | |
| 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.
| |
| | |
| | |
| '04
| |
| | |
| | |
| THE EARLY DEVELOEMENT OF THE MARSTJriALIA. 125
| |
| | |
| | |
| '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,â€
| |
| ‘ Proc. Roy. Soc.,' vol. Ixxi.
| |
| | |
| '07 “ Observations on the Development of Ornithorhyn
| |
| chus,†‘ Phil. Trans. Roy. Soc.,' Series B, vol cxcix.
| |
| | |
| | |
| EXPLANATION OF PLATES 1-9,
| |
| | |
| Illustrating Prof. J. P. Hill's paper on “ The Early Development of the Marsupialia, with Special Reference to the
| |
| Native Cat (Dasyurus vi verrinus).â€
| |
| | |
| [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.
| |
| | |
| PLATE 1.
| |
| | |
| 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
| |
| iron-haematoxylin.)
| |
| | |
| 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
| |
| toxylin.)
| |
| | |
| 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,
| |
| iron-hsematoxylin.)
| |
| | |
| PLATE 2.
| |
| | |
| 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
| |
| zone.
| |
| | |
| 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.
| |
| | |
| | |
| PLATE 3.
| |
| | |
| 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
| |
| iron-hsematoxylin.)
| |
| | |
| 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
| |
| pole.
| |
| | |
| 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.
| |
| thick.
| |
| | |
| 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
| |
| fixation.
| |
| | |
| 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.
| |
| | |
| PLATE 4.
| |
| | |
| 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.
| |
| Picro-nitro-osmic.)
| |
| | |
| 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.)
| |
| | |
| PLATE 5.
| |
| | |
| 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.
| |
| | |
| PLATE 6.
| |
| | |
| 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.)
| |
| | |
| | |
| PLATE 7.
| |
| | |
| 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.
| |
| | |
| | |
| PLATE 8.
| |
| | |
| 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
| |
| blastocyst.
| |
| | |
| 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
| |
| Lelafield.)
| |
| | |
| 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.
| |
| Tropho-ectoderm.
| |
| | |
| | |
| PLATE 9.
| |
| | |
| 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.
| |
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.
Online Editor
|
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.
dasyurid
Modern Notes:
|
Historic Disclaimer - information about historic embryology pages
|
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 IV. - Growth oe the Blastocyst and Differentiation OF THE Embryonal Ectoderm and the Entoderm
1. Growth of the Blastocyst.
In the preceding chapter we have seen that the cleavage
process in Dasyurus results in the formation of a small
spherical vesicle, about '4 mm. in diameter, Avhich consists,
internally to the investment formed by the apposed zona and
shell-membrane, simply of a cellular wall, unilaminar throughout its entire extent, and enclosing a fluid-filled cavity
normally devoid of any cellular elements. The stage of the
just completed blastocyst is followed by a period of active
growth of the same, and it is a noteworthy featui'e in the
development of Dasyurus that during this time the blastocyst
undergoes no essential structural change, but remains unilaminar until it has reached a diameter of from 4'5 to 5'5 mm.
Even during cleavage, the egg of Dasyurus increases in
diameter, partly owing to the thickening of the shell membrane, partly, and, indeed, mainly, as the result of the accumulation of uterine fluid under pressure within the egg-envelopes,
but the increase due to these causes combined is relatively
insignificant, being only about '1 mm. As soon, however, as
the cellular wall of the blastocyst is completed, rapid growth
sets in, under the influence of the hydrostatic pressure of the
fluid, which tensely fills the blastocyst cavity, with the result
that the small relatively thick-walled blastocyst becomes
convei'ted into a large extremely thin-walled vesicle, but
beyond becoming very attenuated, the cellular wall during
this period of actjve growth uudei'goes no essential change,
and retains its unilaminar character until the blastocyst, as
already mentioned, has reached a diameter of from 4'5 to 5‘5
mm. In vesicles of about this size there become differentiated
from the formative cells of the upper hemisphei-e the embryonal ectoderm and the entoderm, and this latter layer then
gradually spreads round inside the non-formative (extraembiwonal ectodermal) layer of the lower hemisphere so as to
44
J. P. HILL.
form a complete lining' to tlie blastocyst, whicli thereby
becomes bilaminar. Sucli a marked enlargement of the blastocyst prior to the differentiation of the embryonal ectoderm
and entoderm as is here described for Dasyurus does not
apparently occur, so far as known, in other Marsupials : in
Perameles, for example, the embryonal ectoderm and the
entoderm are in process of differentiation in vesicles a little
over 1 mm. in diameter (v. p. 77), in Macropus these two layers
are already fully established in a vesicle only *8 mm. in
diameter (v. p. 79), and much the same holds good for Ti'ichosurus and Petrogale. It is pai'alleled by the marked growth
which in the Monotremes follows the completion of the blastocyst and which precedes the appearance of embryonal diffei-entiatiou. It must be remembered, however, that the growing
blastocyst in the Monotreme is bilaminar and not unilaminar
as in Dasyurus, owing to the fact that the entoderm is established as a complete layer at a very much earlier period than
is the case in the latter. I am nevertheless inclined to regard
the attainment by the Dasyurus blastocyst of a large size,
prior to the differentiation of the embi'yonal ectoderm and the
entoderm, as a more primitive condition than that found in
other Marsupials. The pronounced hypertrophy which the
uteri of Dasyurus undergo during the early stages of gestation, an hypertrophy which appears to be proportionately
greater than that met with in other forms,^ is no doubt to be
correlated with the presence in them of such a considerable
number of actively growing blastocysts.
Selenka states (Heft 5, p. 180) that he examined seven
blastocysts of Dasyurus “-f mm.†in diameter, taken from a
female fifteen days after copulation. He describes their
structure as follows : “ Man unterscheidet (1) eine sehr
zarte aussere, homogene Haut (Granulosamembran), (2)
' Por example, the uteri of a female (5, 18 . vii . '01) from which 1
obtained twenty-one normal vesicles, 4'5-6 mm. in diameter, with the
embryonal area definitely established, measured as follows : Left uterus,
4'5 X 4'7 X 1'4 cm. (fourteen vesicles) ; right uterus, 4'5 X 4'2 x 1‘45 cm.
(seven vesicles and one shrivelled).
THE EAELY DEVELOPMENT OF THE MARSHPIALIA. 45
darmiter ein Lagei' von Ektodermzellen, welche im Gebiete
des Embryonalschildes prismafcich, am gegeniiberliegenden
Pole nahezu kubisch, im iibrigen abgeplattet erscbeinen, (3)
ein inneres zusammenliangeudes Lager von abgeflacbten Entodermzellen.†This description, apart from the reference to
the thin shell-membrane, is entii'ely inapplicable to blastocysts
of Dasyurus of the mentioned size which I have studied.
I have examined a practically complete series of vesicles of
Dasyinms ranging from '4 mm. to 4 mm. in diameter and all of
them without exception are unilaminar.
Of vesicles under 1 mm. diameter I possess serial sections
of more than two dozen, I'anging from '5 mm. to '8 mm. in
diameter, and obtained from three different females. These
differ structurally in no essential respect from the just completed blastocysts. A surface view of a blastocyst '6 mm. in
diameter is shown in fig. 63, PI. 6; in this the difference in
the cytoplasmic chai'acters of the cells of opposite hemispheres
is clearly brought out, the non-formative cells of the lower
hemisphere having much more marked perinuclear zones of
dense cytoplasm (deutoplasm) than the formative cells of the
upper hemisphere ; moreover, the former cells tend to be of
larger superficial extent than the latter. Pig. 34, PI. 3,
represents a section of a blastocyst '57 mm. in diameter, and
fig. 35 a section of one '73 mm. in diameter. These blastocysts differ in no essential way from the '43 mm. blastocyst
represented in fig. 33. As in the latter, the cellular wall is
unilaminar throughout, but both it and the shell-membrane
have undergone considerable attenuation. Moreover in these
blastocysts, apart from the clue afforded by the shrivelled
yolk^body, it is practically impossible to determine from the
sections which is morphologically the upper hemisphere and
which the lower. In fig. 36, from a '6 mm. blastocyst, on the
other hand, the cells of the hemisphere opposite the yolk-body
(y.b.) are larger than those of the hemisphei'e adjacent to
which that body is situated. In the '57 mm. blastocyst the
shell-membrane has a thickness of ‘0052 mm., in the -73 mm.
blastocyst it measures -0045 rnrh., and in a -84 mm. blastocyst
46
J. P. HILL.
•0026 mm. The zona is now no longer recognisable as an
independent membrane. In blastocysts of this stage of
growth a variable number of small spherical cells or cellfragments are frequently met with in the blastocyst cavity,
usually lying in contact Avith the inner aspect of the cellular
wall (fig. 34, i.c.). In some blastocysts such structures are
absent, in others one or two may be present, in yet others
numbers of them may occur. They raa,y be definitely nucleated,
but this is exceptional; more usually they contain one or more
deeply staining granules (of chromatin ?), or are devoid of
such. They ai'e of no morphological importance, and I think
thei*e can be no doubt that they represent cells or fragments
of cells which have been separated off from the cellular wall
during the process of active growth. They are of common
occurrence in later blastocysts, and it is possible the so-called
“ yolk-balls †observed by Selenka in Didelphys are of the
same nature.
If we pass now to vesicles from 1 to 3 or 3'5 mm. in
diameter, we find the wall still unilaminar, but considerably
more attenuated than it is in the blastocysts last referred to.
In a vesicle with a diameter of 1'24 mm. the shell-membrane
has a thickness of about '0015 mm., whilst the cellular wall
has a thickness of only '0045 mm. In a 3'5 mm. vesicle the
shell-membi'ane measures about •0012 mm., Avhilstthe cellular
wall ranges from •OOlS to •OOIS mm. in thickness. A small
portion of the wall of a vesicle, 2^4 mm. in diameter, is shown
in PI. 6, fig. 64. In these later vesicles I have failed to detect,
either in surface examination of the vesicles in to to or in
sections, any regional differences between the cells indicative
of a differentiation of the wall into upper or formative, and
lower or non-formative, hemispheres. Everywhere the wall
is composed of flattened, exti'emely attenuated cells, polygonal
in surface view, and all apparently of the same character. It
might therefore be supposed that the polarity, which is recognisable in early blastocysts, and which is dependent on the
pronounced differences existent between the cells of the
upper and lower rings of the 16-celled stage, is of no funda
THE EARLY DEVELOPMENT OF THE MARSUPIALIA.
47
mental importance, since it apparently becomes lost at an
early period during the growth of the blastocyst. Such an
assumption, however, would be very wide of the maxk, as I
hope to demonstrate in the next section of this paper, and,
indeed, in view of the facts already set forth, is an altogether
improbable one.
Reappearance of Polar Differentiation in the
Blastocyst Wall. - Following on the period of what may
be termed the preliminary growth of the blastocyst, in the
course of which the original polar differentiation in the
blastocyst wall apparently becomes obliterated, is an
extremely interesting one, during which that differentiation
again becomes manifest. In view of the fact (1) that the
fourth cleavage in Dasyurus is of the nature of a qualitative
cytoplasmic division, and (2) that approximately one half or
rather less of the unilaminar vosicle wall is formed from the
eight smaller and less yolk-rich cells of the upper ring of the
16-celled stage, and its remainder from the eight larger
more yolk-rich cells of the lower ring, it thus becomes a
question of the first importance to determine if we can the
significance of that differentiation.
Amongst the Eutheria, it has been conclusively shown by
various observers (Van Beneden, Heape, Hubrecht, Assheton,
and others) that there occurs during cleavage an early
separation of the blastomeres into two more or less distinctly
differentiated groups, one of which eventually, by a process
of overgrowth, completely encloses the other. The peripheral
cell-group or layer forms the outer extra-embryonal layer of
the wall of the later blastocyst (the trophoblast of Hubrecht,
or trophoblastic ectgderm as I prefer to term it). It therefore
takes no direct part in the formation of the embryo, and may
be distinguished as non-formative. The enclosed cell-group,
termed the inner cell-mass or embryonal knot, gives rise, on
the other hand, to the embryonal ectoderm as well as to the
entire entoderm of the vesicle, and may accordingly be distinguished as formative. May it not be, then, that we have
here at the fourth cleavage in Dasyurus a separation of the
48
J. P. HIPL.
blastomeres into two determinate cell-groups, respectively
foi'mative and non-formative in significance, entirely compar-,
able with, and, indeed, even more distinct than that which
occurs during cleavage in the Eutheria ? I venture to think
that the evidence brought forward in this paper conclusively
justifies an answer in the affirmative to that question.
If we assume that the upper cell-ring of the 16-celled stage
in Dasyurus is formative in destiny and the lower cell-ring
non-formative, then we might naturally expect to find in the
unilaminar wall of the later blastocyst some differentiation
indicative of its origin from two distinct cell-groups, and
indicative at the same time of the future embryonal and
extra-embryonal regions. Now just such a differentiation,
does, as a matter of fact, become evident in vesicles 3'5 to
4'5 mm. in diameter. We have already seen that the wall in
early blastocysts '4 to '8 mm. in diameter exhibits a wellmarked polar differentiation in correspondence with its mode
of oi'igin from the diffei-entiated cell-rings of the 16-celled
stage, its upper hemisphere or thereabouts consisting of
smaller cells, poor in deutoplasm, its remainder of larger
cells, rich in deutoplasm. .In later blastocysts, 1-3 mm. or,
more in diameter, it is no longer possible to recognise this
distinction - at all events I have failed to observe i't - but if
we pass to blastocysts 4-5 mm. in diameter, in which the wall
is still unilaminar, we find on careful examination of the
entire vesicle under a low power that there is now present a
definite continuous line^ which encircles the vesicle in theequatorial region so as to divide its wall into two hemi-,
spherical areas (PI. 4, fig. S8,j.L). If we remove and stain;
a portion of the wall of such a vesicle, including this line,)
and examine it microscopically (figs. ,42-46.), it becomes
apparent at once, from the .disposition of the cells on either
side of the bns, that we have to do with a sutural line or line
of junction produced by the meeting of twp sets- of cells,'
which are pursuing their .own, independent courses of growth
and division. ; The, cells never cross the demax'cation line
from the one side tn the other, but remain strictly confined
49
THE EAELY DEVELOPMENT OF THE MARSUPIAL [A.
to their own territory, so that we are justified in regarding
the vesicle wall as composed of two independently growing
zones. Now tlj^ existence of two such independent zones in
the unilaminar wall is, to my mind, only intelligible on the
view that they are the products of two originally distinct,
predetermined cell'groups, and if this be admitted, then I
think we are justified in concluding, in view of the facts
already set forth, that tlie two zones in question are derived,
the one from the upper cell-ring of the 16-celled stage, the
other from the lower ring ; that, in other words, they represent respectively the upper and lower hemispheres of the
early blastocysts.
If, now, we find that the embryonal ectoderm and the entoderm arise from one of these two regions of the unilaminar
wall, whilst the other directly forms the outer extra-embryonal
layer of the later (bilaminar) vesicle, then we must designate
the former region as the upper or formative, and the latter as
the lower or non-formative. Further, bearing in mind the
characters of the cells of the two rings of the 16-celled stage,
T think we are justified in holding that the formative region
is derived from the ring of smaller, less yolk-rich cells, and
the non-formative region from the ring of larger, more yolkrich cells, even if it is impossible to demonstrate an actual
genetic continuity between the constituent cells of these two
rings and those forming the independently growing areas of
the later blastocyst. I have recently re-examined a series of
vesicles, measuring 1'5-1'8 mm. in diameter, obtained from a
female killed in 1906, and I have so far found it impossible,
either in the entire vesicle or in portions of the wall stained
and mounted on the flat, to distinguish between the cells over
opposite hemispheres. Thus the only actual guide Ave have
for the determination of the poles in such vesicles is the
yolk-body, and though the latter is liable to- displacement, it
is Avorthy of record that I have several times found it in
relation to the formative area in vesicles 4‘5-6 mm. in
diameter, but never in relation to the non-formative region.
This evidence is, therefore, so far as it goes, confirmatory of
VOL. 56, PART 1. - NEAV SERIES. 4
50
J. P. HILL.
the conclusion reached above, viz, that the formative hemisphere is derived from the smaller-celled ring of the 16-celled
stage. On that conclusion is based my interpretation of the
poles in the unsegmented ovum, and of the two cell-rings o£
the 16-celled stage as respectively upper and lower.
Of vesicles ov'er 1 mm. in diameter, the smallest in which I
have been able to detect the sutural line above referred to
measure 3'25 mm. in diameter. In three lots of vesicles, 3'5
mm. in diameter from three different females, I have failed to
X'ecognise it, whilst in two other lots, respectively 3'75 mm.
(average) and 4 mm. in diameter, the line appears to be in
course of differentiation as in the 3'25 mm. vesicles. A
portion of the wall of one of the 3'5 mm. vesicles just referred
to is shown in PL 4, fig. 41, and a portion of the wall of the
3'25 mm. stage, including the sutural line, in fig. 42. Both
vesicles were fixed in the same fluid, viz. picro-nitro-osmic
acid. Comparison of the two figures reveals the existence, quite
apart from the presence of the junctional line in fig. 42, and its
absence in fig. 41, of certain more or less obvious differences
between them. In fig. 41 the cells are larger, and their cytoplasmic bodies are inconspicuous, being fairly homogeneous
and lightly staining. In fig. 42, on the contrary, the cellbodies are strongly marked, the cytoplasm being distinguishable into a lighter-staining peripheral zone, and a much more
deeply staining perinuclear zone, showing evidence of intense
metabolic activity. This latter zone is more or less vacuolated,
and contains, besides larger lightly staining granules, numerous
smaller ones of varying size, stained brown by the osmic acid
of the fixative. In the 4 ram. vesicles the cells show pi-ecisely
the same characters; in the 3'75 mm. vesicles, which were
fixed in a picro-corrosive-acetic fluid, the granules ax'e absent
from the cytoplasm, otherwise the cells are similar to those
of the other two. Mitotic figures are common. The sutural
line is recognisable in all three sets of vesicles (3'25, 3'75, and
4 mm.) (fig. but I cannot be certain that it runs con
tinuously round, and it appears to have a rather more sinuous
course than in later blastocysts. The cells of the two regions
THE EARLY DEVELOPMENT OF THE MARSUPIALIA.
51
of the bliistocyst wall, separated by the sutural line, differ
somewhat in tlieir characters. On one side of the line (fig.
42, tr.ect.) the cells appear to be on the whole slightly larger,
and of more uniform size than they are on the other, and they
also stain somewhat more deeply. Comparison with later
blastocysts shows that the region of more uniform • cells is
non-formative, that of less uniform, formative. At^this stage,
however, the differences between the cells of the two regions
are as yet so little pi'onounced that it is practically impossible
in the absence of the sutural line to say to which hemisphere
an isolated piece of the wall should be referred.
I am inclined to regard the sutui'al line in these vesicles as
being in course of differentiation, and judging from the disposition of the cells on either side of it, I think its appearance
is to be correlated with the marked increase in the mitotic
activity of the cells of the two hemispheres which sets in in
vesicles of 3-4 mm. diameter. The preliminary increase in
size of the blastocyst up to about the 3 mm. stage might be
described as of a passive character, i.e. it does not appear
to be effected as the result of the very active division of the
wall-cells, but is characterised rather by a minimum of mitotic
division and a maximum of increase in surface extent of the
cells, due to excessive stretching consequent on the rapid
imbibition of uterine fluid. Once, however, the requisite size
has been attained, the cells of the unilaminar wall commence
to divide activel}', and doubtless as the outcome of that
wave of activity, the sutural line makes its appeai-ance
between the two groups of independently growing cells.
On the inner surface of the blastocyst wall, especially in
the region of the formative hemisphere, there are present
in these vesicles numbers of small deeply staining cells of
spherical form, and containing osmicated granules similar
to those in the wall-cells. They may occur singly or in groups,
and appear to me to be of the same nature as the inteimal cells
of the earlier blastocyst. In addition to these cells, there are
present clusters of cytoplasmic spheres, staining similarly to
the spherical cells, and apparently of the nature of fragmeiita
52
J. P, HILL.
tion products formed either directly from the â– \vall-cells or
from these internal cells.
2. Differentiation of the Embryonal Ectoderm and
the Entoderm.
After the preliminary growth in size of the blastocyst is
completed, the next most important step in the progressive
development of the latter is that just dealt with, involving
the appearance of the sutural line, with resulting re-establishment of polar differentiation in the blastocyst wall. Following
on that, we have the extremely important period during
which the embryonal ectoderm and the entoderm become
definitely established.
For the investigation of the earlier phases of this critical
period I have had at my disposal a large number of
unilaminar blastocysts derived from three females, distinguished in my notebooks as (3, 25 . vii . '01, with fifteen
vesicles of a maximum diameter of 4‘5 mm. ; 8 . vii . '99, with
twelve vesicles, 4‘6 .mm. in diameter ; and 6 . vii . '04, with
twfenty-two vesicles, 4‘5 and 5 mm. in diameter. These three
lots of vesicles may for descriptive purposes be designated
as '01, '99, and '04 respectively.
The '01 vesicles are distinctly less advanced than the
other two. The sutural line is now, at all events, definitely
continuous, and can readily be made out in the intact vesicle
with the aid of a low-power lens (PI. 4, fig. 38, j.L), but
the differences between the cellular constituents of the two
hemispheres which it separates are much less obvious than
they are in the '99 and '04 vesicles. Here, again, one
hemisphere forming half or perhaps rather more of the entire
vesicle is distinguished from the other by the greater uniformity and the slightly deeper staining character of its
constituent cells (figs. 43 and 44, tr. ecL). This hemisphere,
subsequent stages show, is the lower or non-formativ^
hemisphere. It is characterised especially by the striking
'uniformity in the size of its cells. Over the opposite hemisphere, the upper or formative one (figs. 43 and 44, the
THE EARLY DEVELOPMENT. OF- THE MAR8UPIALIA.
53
cells are more variable iu size, the nuclei thus appearing less
uniformly and less closely arranged, and they stain,. on the
whole, somewhat less deeply than those of the lower hemisphere. The non-formative cells are on the average smaller
than the largest of the formative cells, but they are more
uniform iu size, and their nuclei thus lie at more regular
distances apart, and appear more closely packed. They are
also richer in deutoplasmic material, and so stain rather more
deeply than the formative cells. Sections show that the
cellular wall is unilaminar throughout its extent, and that,
whilst it is somewhat thicker than that of 3‘5 mm. vesicles,
it is still very attenuated, its thickness, including the shellmembrane, ranging-from ‘004 to '008 mm. I have examined
a number of series of sections taken through portions of the
wall known to include the sutural line, and find it quite
impossible to locate the position of the- latter; indeed, I
cannot certainly distinguish between the formative and nonformative regions.
In the blastocyst cavity, lying in contact with the inner
surface of the wall, and most abundant in the region of the
formative hemisphere, there are present numbers of deeply
staining spherical cells with relatively small nuclei similar to
those described in connection with the 3'25 mm. vesicles.
They occur singly or in groups, and may appear quite normal
or may show more or less evident signs of degeneration.
Their nuclei may stain deeply and homogeneously, or may be
represented by one or two deeply staining granules, vacuoles
may occur in their cytoplasm, and spherical cytoplasmic masses
of very variable size, with or without deeply staining granules
of chromatin) may occur along with them. In sections and
preparations of the wall of these, and other 4*5 mm. vesicles
there are to be found, in both the formative and non-formative
hemispheres, small localised areas from which such spherical
cells are being proliferated off in numbers together. PI. 5,
fig. 47, from the formative hemisphere of an ^04 vesicle shows
One of the most marked examples of such proliferative. activity
that I have encountered. A similar but smaller proliferative
54
J. ?. HILL.
area occurs on the non-formative hemisphere of the same
vesicle.
These spherical cells are, I am convinced, of no morphological importance, and are destined sooner or later to degenerate. They have certainly nothing to do with the
entoderm, the parent-cells of that layer arising exclusively
from the formative hemisphei'e and not from cells such as
these, which are budded ofE from both hemispheres. The fact
that they are, in unilaminar vesicles, more numerous over the
formative hemisphere may perhaps be taken as an indication
of the greater mitotic activity of the formative as compared
with the non-formative cells.
The Primitive Entodermal Cells. - Following closely
on the stage represented by these '01 blastocysts is the extremely important one constituted by the '99 and '04 vesicles
before referred to. This stage is the crucial one in primary
germ-layer formation, and marks the transition from the unilaminar to the bilaminar condition, since in it the entodermal
cells are not only distinctly recognisable as constituents of the
formative region, but are to be seen both in actual process of
separation from the latter and as definitely internal cells, frequently provided with, and even connected together by,
pseudopodial-like processes of their cell-bodies. Such cells
are already present in the '01 vesicles (fig. 71), and probably
also in the blastocysts in which the sutural line first makes
its appearance, but are much less conspicuous than in these
older blastocysts.
The '99 blastocysts are distinctly more advanced than the
'01 batch and are just a little earlier than the '04 lot. The
former measui'ed, as already mentioned, 4'5 mm. in diameter,
the latter 4'5 and 5 mm. (the majority being of the latter
size). In my notes, on the intact '99 vesicles I find it stated
that one hemisphere, forming rather less than half of the
entire extent of the vesicle wall, appeared somewhat denser
than the other, the sutural line marking the division between
the two. I naturally inferred at the time that the denser
hemisphere corresponded to the embryonal region of the
55
THE EARLY DEVELOPMENT OF THE MARSUPIALIA.
Eutherian blastocyst and the less dense to the extra-embryonal region of the same, but just the reverse proves to hold
true for the '04 vesicles, the formative hemisphere in these
appearing less dense than the non-formative. I cannot now
test my former inference by direct observation since I do not
appear to have any of the '99 vesicles left intact, but amongst
my in toto preparations of the vesicle wall I find one
labelled as from the “ lower pole †which unmistakably
belongs to the formative hemisphere, hence I conclude that
the denser and slightly smaller region which I originally
regarded as formative is really non-formative, a conclusion
which brings the '99 vesicles into agreement with the '04
batch.
In these latter vesicles the sutural line and the two regions
of the wall can be quite readily made out on careful examination under a low power with transmitted light. The one
region appears slightly denser (darker) and has more closely
arranged nuclei (i. e. is composed of smaller cells) than the
other. On the average this denser region appeal's to be
rather the less extensive of the two ; the two regions may be
about equal ; on the other hand the denser may be the smaller.
Examination of stained preparations of the wall demonstrates
that the darker hemisphere is non-formative, the lighter,
formative. It would therefore seem that in certain of these
'04 vesicles the formative region has grown more rapidly than
the non-formative.
In stained preparations of the wall both of the '99 and '04
vesicles, the differences between the two hemispheres are now
so well marked that there is no diflBculty in referring even an
isolated fragment to its proper region. The non-formative
hemisphere differs in no essential way from that of the '01
vesicles, and as in these, is readily distinguishable from the
formative by the much greater uniformity in the size and
staining properties of its cells (fig. 45), as well as by the fact
that there are no primitive entodermal cells such as occur in
relation to the formative hemisphere, in connection with it.
Its constituent cells are on the average distinctly smaller than
56
J. P. HILL.
the largest of the formative ; their nuclei lie nearer each other,
with the result that in surface examination of the blastocyst
the non-formative region appears rather denser than the
formative. In in toto preparations of the wall the former
usually stains darker than the latter (fig. 45), but this is not
always the case ; in fig. 46, from an '04 vesicle, there is
practically no difference in this respect between the two
regions ; in yet others of my preparations of '99 vesicles the
formative region has stained more deeply than the nonformative.
The formative hemisphere in the earlier blastocysts of this
particular developmental stage was described (ante, p. 51) as
differing from the non-formative in that its constituent cells
were much less uniform in chai*acter than those of the latter.
This same feature, but in much enhanced degree, characterises
the formative region of the vesicles under consideration, for it
can now be definitely stated that the latter I'egion is constituted by cells of two distinct varieties, viz. (1) moi*e lightly
staining cells which form the chief constituent of the formative region, its basis so to speak, and which are on the
average larger than those of the other variety, and (2), a less
numerous series of cells, distinctly smaller than the largest
cells of the former variety, and with denser, more granular and
more deeply staining cytoplasm, and frequently met with in
mitotic division (cf. PI. 6, fig. 65). The two varieties of cells are
intermingled promiscuously, the smaller cells occurring singly
and in groups but in a quite irregular fashion, so that here
and there we meet with patches of the wall composed exclusively of the larger cells.
The evidence presently to be adduced shows that the larger
cells furnish the embryonal ectoderm, and that the smaller
cells give origin to the primitive entodermal cells from which
the definitive entoderm arises. The smaller cells may therefore be regarded as entodermal mothei'-cells. Whether these
latter cells are progressively formed from the larger cells
simply by division, or whether the two vaifieties become
definitely differentiated from each other at a particular stage in
THE EAHLY DEVELOPMENT OP THE MARSUPIALTA.
57
development, must for the present be left an open question. Of
the actual existence in tlie unilaminar formative region of these
'99 aud '04 blastocysts of two varieties of cells, respectively
ectodermal and entodermal in significance, there can be no
doubt. In preparations of the formative region, however,
whilst one can without hesitation identify certain cells as
being in all probability of ectodermal significance and others
as prospectively entodermal (cf. figs. 65, 66), it must be
admitted that one is often in doubt as to whether one is
dealing with small ectodermal cells or with genuine entodermal mother-cells. It is, therefore, hardly to be wondered
at that I have not yet been able to satisfactorily determine
at what precise period the entodermal mother-cells first
become differentiated, though judging from the facts that
in the eai-liest vesicles in which the sutural line is recognisable one region of the wall already differs from the other in
the less uniform size of its constituent cells, and that internally
situated entodermal cells are already present in small numbers
in the '01 vesicles (fig. 71), I incline to the belief that it
will probably be found to about coincide with the first
appearance of the sutural line. To this question I may
perhaps be able to return at some future time.
In addition to the presence of these entodei'mal mothercells, which enter directly into its constitution, the formative
region of the '99 and '04 blastocysts is. characterised by the
occurrence on its inner surface of definitely iuteimal cells,
which generally agree with the former cells as regards size
and staining properties and are evidently related to them. It
is these internally situated cells which directly give origin to
the definitive entoderm of the later blastocysts, and one need,
therefore, have no hesitation in applying to them the designation of primitive entodermal cells. They are exclusively found
in relation to the formative hemisphere, and appear in in toto
prepai'atious as flattened, darkly staining cells closely applied
to the inner surface of the unilaminar wall, and disposed quite
irregularly, singly, and in groups. They vary greatly in
number in blastocysts of even the same batch, but on the
58
J. r. HILL.
wholo are most abundant in the ^04 series, and they also
exhibit a remarkable range of variation in shape. They may
have a perfectly distinct oval or rounded outline (figs. 67, 71,
72), or, as is more frequently the case, they may lack a
determinate form and appear quite like amoeboid cells owing
to their possession of cytoplasmic processes of markedly
pseudopodial-like character (fig. 69). Frequently, indeed,
the cells are connected together by the anastomosing of these
processes, so that we have formed in this way the beginnings
at least, of a cellular reticulum (figs. 68, 69,70).
The question now arises. How do these primitive entodermal cells originate from the small, darkly staining cells of
the unilaminar formative region designated in the foregoing
as the entodermal mother-cells ? I can find no evidence that
the primitive entodermal cells are formed by the division of
the mother-cells in planes ta.ngential to the surface ; on the
contrary, all the evidence shows that we have to do here with
an actual inward migration of the mother-cells, with or without previous mitotic division, such inward migration being
the outcome of the assumption by the mother-cells, or their
division products, of amoeboid properties ; in other words, the
evidence shows that the formation of the entodei'm is effected
here not by simple delamination (using that term in the sense in
which it was originally employed by Lankester), but by a process involving the inward migration, with or without previous
division, of certain cells (entodermal mother-cells) of the unilaminar parent layer, a process comparable with that found in
certain Invertebrates (Hydroids) and distinguished by Metschnikoff as '^gemischte Delaminatiou.â€
In this connection it has to be remembered that the cells of
the unilaminar wall of the blastocyst are under considei'able
hydrostatic pressure, and, in correlation therewith, tend to
be tangentially flattened, though the flattening in this stage
is much less than in the earlier blastocysts. From a series of
measurements made from an '04 vosicle, I find that over the
formative region the ratio of the breadth to the thickness of
the cells varies Horn 6 : 1 to 2 : 1, and even to 3 : 2. On the
THE EARLY DEVELOPMENT OF THE MAESUPIALIA. 59
whole cells of the type indicated by the ratio 6 : 1 predominate,
and we should hardly expect to find such cells dividing tangentially. In fact, the only undoubted examples of such division I
have met with occur in the single abnormal vesicle present in
the '04 batch. In this particular vesicle, which had a diameter
of 3 mm. and was thus smaller than the others, thei'e was
present on what appeared to correspond to the formative
hemisphere of the normal blastocyst a well-defined and conspicuous ovalish patch, 1'23 x '99 mm. in diameter.^ Sections
show that over this area the cells of the unilaminar wall are
much enlarged and , more or less cubical in form, their thickness varying from ‘012 to ‘019 mm. These cubical cells
exhibit distinct evidence of tangential division, both past and
in progress. But in normal vesicles, whilst mitotic figures are
quite commonly met with in the cells of the formative region
(in which, indeed, they are more numerous than in those of
the non-formative region), I have failed to find in my sections
after long-continued searching even a single spindle disposed
directly at right angles to the shell-membrane ; the mitotic
spindles lie disposed either tangentially to the surface or
obliquely thereto.
For the determination of the mode of origin of the
primitive entodermal cells, it is absolutely necessary to
study both in to to preparations of the formative region,
i.e. small portions of the unilaminar wall stained and
mounted on the flat, and sections of the same. Sections alone
are, on the whole, distinctly disappointing so far as the
question under discussion is concerned, and, indeed, give one
an altogether inadequate idea of the primitive entodeimial cells
themselves, seeing that practically all one can make out is that
1 Curiously enough, amongst the '99 vesicles there also occurred
a single small one, likewise 3 mm. in diameter, and with a thickened
patch 1-28 X 1 mm. in diameter, quite similar in its character to that
described in the text. I am as yet uncertain whether the thickened
area in these two vesicles represents the whole of the formative hemisphere of normal blastocysts or only a hypertrophied part of the same,
or whether, indeed, it may not represent the I'etarded non-formative
hemisphere.
60
J. P. HILL.
there are present, in close apposition with the inner surface of
the unilaininar wall, small, darkly staining cells, apparently
quite isolated from each other and usually of flattened form
(figs. 73, 74, 76, ent.). One has only to glance at a wellstained in to to preparation of the formative region (cf.
fig. 70) to realise how inadequate such a description of the
primitive entoderm cells really is.
Sections nevertheless do yield valuable information on
certain points. Besides affording the negative evidence of
the absence of tangential divisions and the positive evidence
that the primitive entodermal cells are actually internal (figs.
73, 74, 76), they show that growth of the wall iu thickness
has already set in, and that it is most marked over the
formative region, though the thickness attained by the cells
is as yet very unequal (figs. 73-76). Measurements takeu
from an '04 vesicle show that over the non-formative region
(fig. 77) the cells vary in thickness from *006 to '009 mm.,
whilst over the formative region the range of variation is
greater, viz. from ‘006 to ‘013 mm., so that we may conclude
that the latter region is on the average thicker than the
former (cf. figs. 73-76, with fig. 77 depicting a small portion
of the non-formative region). It is still impossible to determine the position of the sutural line, even in sections of
fragments of the wall known to contain it.
The entodermal mother-cells are not very readily recognisable in sections. In fig. 75, however, which is drawn
from an accurately transverse section through the formative
region of an '04 vesicle, there is depicted what is undoubtedly
an entodermal mother-cell {ent.). The interesting point
about this particular cell is that its cell-body, whilst still
intercalated between the adjoining cells of the unilaminar
wall, has extended inwards so as to directly underlie one of
the wall-cells. ' Division of such a cell as this would necessarily result in the production of an internally situated cell
with all the relations of one of the primitive entodermal type.
The inwardly projecting spheroidal cell situated immediately
to the left (in the figure) of the one just refeiTed to, I also
THE EARLY DEVELOPMENT OF THE MARSUPIALIA. 61
regard as an entodermal mother-cell. Cells of this type are
not infrequently met with in sections; they nsually stain
somewhat deeply, and are often found in mitosis.
The evidence obtainable from the study of in to to preparations conclusively proves that some at all events of the
primitive entodermal cells are actually derived from the entodermal mother-cells, much in the-way suggested above, whilst
others of the primitive entodermal cells are directly formed
from mother-cells which bodily migrate inwards.
Fig. 65, PI. 6, represents a small portion of the formative
region of an '04 vesicle viewed fPom the inner surface. In
the centre of the figure, surrounded by the larger, lighter
staining (ectodermal) cells of the wall, is a smaller cell in the
telophases of division, the cytoplasm of which is granular and
stains deeply. That cell unmistakably forms a constituent of
the unilaminar wall. I regard it as an entodermal mothercell. Fig. 66 shows another cell of the same character in the
anaphases of division, which likewise forms a constituent of
the unilaminar wall, but which differs from the corresponding
cell in fig. 65 in that its cytoplasmic body has extended out
on one side (lower in the figure), so as to directly underlie
part of an adjacent ectodermal cell. In other words we have
here a surface view of the condition represented in section in
fig. 75, only the entodermal mother-cell depicted therein is not
actually in process of division. Fig. 67, taken from the same
preparation as fig. 65, shows what I take to be the end result
of the division of such a cell as is i-epresented in the two
preceding figures. Here we see two small deeply staining
cells towards the centre of the figure, which from their disposition and agreement in size and cytological characters
are manifestly sister-cells, and the products of division of
just such an entodermal mother-cell as is represented in fig.
65, or, better, fig. 66. The one cell (upper in the figure) is
more angular in form and manifestly still lies in the unilaminar wall; the other (lower in the figure) is ovalish in form
and is no longer a constituent of the unilaminar wall, but is
on the contrary a free cell, definitely internal both to the
62
J. P. HILL. â– . â– :
latter and to its sister-cell. It is, in fact, a primitive entodermal cell, as comparison with fig. 68 proves, and that it has
been formed by the division of a mother-cell situated in the
unilaminar wall can hardly, I think, be doubted. Its sistercell, which is still a constituent of the wall, would presumably
have migrated inwai-ds some time later.
It is to be noted that the primitive entodermal cell referred
to above and those depicted in figs. 71 and 72 are definitely
contoured, ovalish and I'ounded cells, entirely devoid of processes. In these respects they differ markedly from the entodermal cells shown in fig^. 68-70, which are very variable in
form owing to their possession of more or less elongated
pseudopodial-like processes. It might thex'efore be inferred
that the formation of these processes only takes place after
the entodermal cells have become definitely internal. Such
an inference, however, would be incorrect, for I have abundant
evidence showing that such processes may be given off from
the entodermal mother- cells whilst they are still constituents
of the wall. In in toto preparations, it is often difficult to
determine with certainty whether a particular entodermal cell
still enters into the constitution of the unilaminar wall or not.
In the portion of the formative region of a '04 vesicle depicted
in fig. 70, however, I am satisfied that all the entodermal
cells therein shown (they are readily distinguishable by their
smaller size and more deeply staining character) are, with the
possible exception of the one on the extreme right, at least
partially intercalated between the larger ectodermal cells of
the wall. Some of them are entirely situated in the wall ;
others have extended inwards in varying degree so as to
partially underlie the ectodermal cells. It is these latter
entodermal cells in particular which exhibit the cytoplasmic
processes above referred to. As the figure shows, these processes have all the characters of pseudopodia,; they vary in
size, form, and number from cell to cell, individual processes
may be reticulate and their finer prolongations may anastomose with those of others, and they are formed of cytoplasm,
less dense and rather less, deeply staining than that of the
THE EARLY DEVELOPMENT OF THE MARSUPIALIA. 63
cell-bodies from which they arise. Attention may be specially
directed to the cell towards the left of the hgure (mai'ked ent.).
Here we have an entodermal cell whose cytoplasmic body is
evidently still partially intercalated between the cells of the wall,
but which is, at the same time, prolonged inwards (towards
the left) so as to underlie the adjoining ectodermal cell.
From this inward prolongation there are given off two slender
processes, one short and tapering, the other very much
longer ; this latter, after becoming vei'y attenuated, gradually
widens to form an irregular fan-shaped expansion, suckerlike in appearance, and produced into several slender
threads, which is situated adjacent to the nucleus of
the ectodermal cell on the extreme left. Then from the
right side of the same cell there is given off a small inwardly
projecting bulbous lobe which may well be the start of just
such another process as arises from the left side. Processes
of the peculiar sucker-like type just described, formed of a
slender elongated stem and a distal expanded extremity from
which delicate filamentous prolongations are given off, are
abundantly met with in preparations, and strikingly recall the
pseudopodia of various Ehizopoda. They are seen in connection with other entodermal cells in fig. 70, and with many
of those in fig. 68. I regard them as veritable pseudopodia.
Towards the right side of fig. 70 the two entodermal cells
there situated stand in direct protoplasmic continuity by
means of two slender connecting threads, whilst the upper of
these two cells is again joined by a very fine process to the
irregular pseudopodial expansion which arises from one of
the two entodermal cells situated nearer the middle of the
figure, and that same expansion is directly connected with the
second of the two entodermal cells just mentioned, so that we
have here established the beginning of a cell-network, prior
to the complete emancipation of its constituent entodermal
elements from the unilaminar wall. We have, then, clear
evidence that the entodermal elements in Dasyurus, prior to
their separation from the unilaminar formative region ai*e
capable of exhibiting amoeboid activity, since not only may
64
J. r. HILL.
they send lobose prolongations of their cytoplasmic bodies
inwards below the adjacent ectodermal cells, but they may
emit more or less elongated processes of indubitable pseudopodial character, which similarly lie in contact with the inner
surface of the wall-cells. Furthermore, we have evidence
that these pseudopodial processes may anastomose with each
â– other so as to initiate the formation of an entodermal reticulum,
whilst the cells from which they arise are still constituents of
the unilaminar wall - an especially noteworthy phenomenon.
Certain of the primitive entodermal cells, as we have seen,
are at first devoid of such processes, but since they all
eventually form part of a continuous reticulum, it is evident
that the entodermal elements are capable of emitting pseudopodial processes as well after as before their separation from
the formative region.
Finally, in view of the fact that the entodermal mothei'-cells
depicted in fig. 70 are not actually in process of division, and
therein differ from those of figs. 65 and 66, we may conclude
that the formation of the primitive entodermal cells is effected
either with or without the pi*evious division of the mother-cells.
If Ave admit, as I think on the evidence we must admit,
that the entodermal cells in Dasyurus are endowed with
amceboid properties, then Ave are relieved of any further
difficulty in regard to the mechanism of their inAvard migration
from the unilaminar Avail. Doubtless, in the case of those
entodermal mother-cells Avhich do not undergo division, the
precocious formation of the above-described pseudopodial
processes which spread out from the cells like so many
suckers considerably facilitates their direct detachment from
amongst the cells of the Avail. In the case of those primitive
entodermal cells Avhich originate as the direct products of
division of the mother-cells, it no doubt depends on a variety
of circumstances (e.g. actual form of the dividing cell,
direction of the spindle, etc.) whether they exhibit amoeboid
activity precociously (i.e. before their actual i separation), or
only at a later period.
The entoderm varies considerably in its degree of diffe
THE EARLY DEVELOPMENT OF THE MARSUPIALIA.
65
rentiation iu different vesicles of this stage, and even in
different parts of the formative region of one and the same
vesicle. In some vesicles there are relatively few primitive
entodermal cells, in othei*s they are much more abundant.
Fig. 68, from the formative region of an ^04 vesicle, shows a
typical patch of them and illustrates very well the highest
stage of differentiation which they attain in these vesicles. The
entodermal cells therein depicted all appear to be definitely
internal, and it is especially worthy of note that the portion
of the unilaminar wall in relation to them is composed exclusively of the larger, lighter staining cells. It is these cells
which directly form the embryonal ectoderm of the blastocysts
next to be described. The entodermal cells are obviously
amoeboid in character (obsei've especially the cells near the
middle of the figure), and are in active process of linking
themselves together into a cellular reticulum. In fig. 69 is
shown a small portion of the formative region of another ^04
vesicle. A single entodermal mother-cell in process of
division occurs in position in the unilaminar Avail, which is
otherwise composed of ectodermal cells, whilst internally there
are present three entodermal cells, already linked together by
their pseudopodial processes. ^Jfiie two lowermost cells afford
especially striking examples of amoeboid activity, the elongated
pseudopodial process of the cell on the left terminating iu a
well-marked reticulation in definite continuity Avith the corresponding, but shorter and thicker process of the cell on the
right.
3. Establishment of the Definitive Embryonal
Area.
FolloAving directly on the stage represented by the '04
blastocysts described in the preceding section is one designated in my list as 5, 18 . vii . 01 and referred to here as 5, '01.
It comprises twenty-two blastocysts obtained from a female
killed fifteen days after coition and all normal, Avith the
exception of one Avhich Avas shrivelled, and all in precisely
VOL. 56, PAllT 1. NEW SERIES. 5
66
.T. P. HILL.
the same stag-e of development. They measured from 4‘5 to
6 mm. in diameter.
In this stage the formative region of the preceding blastocysts has become transformed into the definitive embryonal
area (embryonic shield, Hubrecht) as the result of the completion of that process of inward migration of the entodermal
mother-cells which we saw in pi-ogress in the vesicles last
described, and the consequent establishment of the entoderm
as a continuous cell-layer undeidying and independent of, the
embryonal ectoderm constituted by the larger passive cells of
the original unilaminar formative layer.
In the entii*e blastocyst (PI. 4, fig. 39) the embryonal area
is quite obvious to the naked eye as the more opaque, hemispherical region, forming rather less than half the entire
extent of the vesicle wall ; the larger remainder of the same
is formed by the much more transpai-ent, non-formative or
extra-embryonal region. Sections of the entire blastocyst
show (1) that the embryonal area is bilaminar over its entii-e
extent, its outer layer consisting of embryonal ectoderm,
already somewhat thickened, its much thinner inner layer
consisting of entoderm, partly still in the form of a cellular
reticulum, and (2) that the extra-embryonal region is still
unilaminar throughout and composed of a relatively thin
layer of flattened cells (extra-embryonal or trophoblastic ectoderm, trophoblast [Hubrecht])^ (PI. 8, fig. 78). The entoderm
is co-extensive at this stage with the embryonal ectoderm,
and terminates in a wavy, irregularly thickened, free, edge
(PI. 5, fig. 49), which over most of its extent either directly
underlies or extends very slightly beyond the line of junction
between the embryonal and extra-embryonal ectoderm. The
junctional line is thus not very easily seen. In fig. 48, however,
' In consonance witli my conviction that this layer is homologous
both Avith the so-called trophoblast of Eutheria and the exti-a-embryonal
ectoderm of Prototheria, and in view of the theoretical signification
which Hubrecht now insists should be attached to the term “ trophoblast.†and which I am wholly unable to accept, I venture to suggest as
an alteiTiative name for this layer that of “ tropho-ectoderni.
THE EARLY DEVELOPMEI^T OF THE MARSUPIALIA.
67
a small portion oP the line shows with sufficient distinctness, I
think, to demonstrate its identity with that of the preceding
stage.
The vesicle wall in all my sections of this stage appears
to be somewhat thinner than that of the '04 blastocysts, but
apart from this apparently variational difference the present
blastocysts are almost exactly intermediate between the latter
and those next to be described.
The embryonal ectoderm (fig. 78, emb. ect.) appears in
section fairly uniformly thickened, though its cells are still of
the flattened type. In surface view in in toto preparations
(cf . fig. 48), they exhibit the same polygonal form and lightly
staining qualities as the larger cells of the formative region
of the '04 blastocysts, which we have already identified as
prospective embryonal ectodermal cells. The junctional line
between the embryonal ectoderm and the extra-embryonal is
now for the first time readily distinguishable in sections
(fig. 78). The extra-embryonal ectoderm (tropho-ectoderm)
(PI. 5, figs. 48 and 49, PI. 8, fig. 78, tr. ect.) differs in no
essential respect from the corresponding layer in the '04
blastocysts.
The entoderm in these blastocysts is exceedingly closely
adherent to the inner surface of the embryonal ectoderm and
cannot be removed therefrom by artificial means. It varies
slightly in its character in different vesicles and in different
parts of its extent in the same vesicle. Mostly it appears as
a continuous thin cell-layer (figs. 49 and 78, ent.), but here and
there patches occur in which the cells form a reticulum quite
similar to that shown in fig. 68 of the preceding stage.
The next stage (designated in my list as 8 . vi . 01), and the
last of Dasyurus that need be described in the present communication, comprises eleven vesicles (5-5'5 mm. in diameter),
in which the embryonal area is conspicuous and distinctly in
advance of that of the preceding vesicles, but is still devoid
of any trace of embryonal differentiation (PI. 4, fig. 40;
PI. 8, fig. 79).
The embryonal area is hemispherical in form (its greatest
68
J. P. HILL.
diameter varying' from 3'5 to 4 mm.) in all except two of the
blastocysts, in which it is elongate, with longer and shorter
diameters. It occupies about a third or less of the entire
extent of the vesicle wall, and thus appears relatively smaller
than that of the preceding (.5, '01) vesicles. The entoderm now
extends for a distance of about 1 mm. beyond the limits of
the area, so that in the entire vesicle (fig. 40) three zones
differing in opacity are distinguishable, viz. the dense hemispherical zone at the upper pole, constituted by the embryonal
area; below that, a less dense, narrow annular zone, formed of
extra-embryonal ectoderm and the underlying peripheral
extension of the entoderm ; and finally, the still less dense
hemispherical area, forming the lower hemisphere of the
blastocyst and constituted, solely by extra-embryonal ectoderm. Thus approximately the upper half of the blastocyst
is bilaminar, the lower half unilaminar. Sections show that
the embryonal ectoderm (fig. 79, emh. ect.) is now a quite
thick layer of approximately cubical cells, whilst the extraembryonal ectoderm {tr. ect.) is formed of relatively thin
flattened cells. The line of junction between the two is perfectly obvious, both in sections (fig. 79) and in surface view
(PI. 5, fig. 50). The embryonal ectodermal cells, though
much thicker than the extra-embryonal, are of less superficial
extent; their nuclei therefore lie closer together than those
of the latter, moreover they are larger, stain more deeply, and
are more frequently found in division, all of which facts
testify to the much greater growth-activity of the embryonal
as compai'ed with the exti-a-embryonal ectoderm at this stage
of development (cf . fig. 50, emh. ect. and tr. ect.-, in the preparation from which this micro-photograph was made the entoderm
underlying the embryonal ectoderm has been removed, whilst
it is still partially present over the extra-embryonal ectoderm).
The entoderm (fig. 79, ent.) over the region of the embrvonal area is readily separable as a quite thin membrane,
and is then seen to consist of squamous cells, polygonal in
outline, and either in direct apposition by their edges or connected together by minute cytoplasmic processes. Beyond the
THE EARLY DEVELOPMENT OE THE MAESUPIALIA.
69
embryonal area, liowever, its peripliei'al extension below the
extra-embryonal ectoderm is much less easily separable in the
intact condition (cF. fig. 50), because oF its greater delicacy
due to the fact that it has here largely the form of a cellular
reticulum. In this extra-embryonal region the entodermal
cells are frequently found in mitosis. Ic would appear, then,
that the entoderm is first laid down in the region of the embi'yonal area as a cellular reticulum, which later becomes
ii'ansformed into a continuous cell-membrane, and that its
peripheral extension over the inner surface of the extraembryonal ectoderm is the result of the growth and activity
oF its own constituent cells.
This peripheral growth continues until there is formed
eventually a complete entodermal lining to the blastocyst
cavity. The rate of growth appears to be somewhat variable.
In a series of primitive streak vesicles (6-6'75 mm. in diameter)
the lower third oF the wall is, I find, still unilaminar. In
another series of vesicles of the same developmental stage
(4'5-6 mm. in diameter) a unilaminar area is present at the
lower pole, varying from I x ‘5 mm. in diameter to as much
as 4 mm. Even in vesicles 7-7'5 mm. in diameter a unilaminar patch may still occur at the lower pole, but in vesiqles
8'5 mm. in diameter (stage of fiat embryo) the entodermal
lining appears always to be complete.
The Origin of the Entoderm in Eutheria. - The
remai'kable facts relative to the origin of the entoderm in
Dasyurus which I have been able to place on record in the
jireceding pages, thanks to the large size attained by the
blastocyst prior to the differentiation of the formative germlayers and to the circumstance that the formative cells are
not arranged, as they are in Eutheria, in the form of a more
or less compact cell-mass, but constitute a thin unilaminar
cell-layer of relatively great extent which can easily be cut
up with scissors, and which, after staining and mounting on
the fiat can be examined under the highest powers, throw, it
seems to me, a new and unexpected light on the mammalian
entoderm, and at the same time help to fill the considerable
70
J. P. HILL.
gap whicli has hitherto existed in our knowledge of its early
ontogenesis. Although the mode of origin of the entoderm
in Dasyurus would appear, in the present state of our knowledge, to find its closest parallel, not amongst vertebrates, but
in certain invertebrates (cf . the mode of origin of the entodermal cells from the wall of the blastula in Hydra as
described by Brauer^), the observations of Assheton ('94)
on the early history of the entoderm in the rabbit, when
viewed in the light of the foregoing, seem to me to afford
ground for the belief that phenomena comparable with those
hei'e recorded for Dasyui'us will eventually be recognised as
occurring also in Eutheria.
Hubrecht ('08), in his recent treatise on early Mammalian
ontogeny, deals very briefly with the question of the origin
of the entoderm in the latter group, merely stating that
“ from the inner cell-mass arises by delamination a separate
lower layer which we designate as the entoderm of the
embryo. These entoderm cells wander in radial direction
along the inner surface of the trophoblast, which in many
cases is thus soon transformed into a didermic structure.
. . . When the entoderm has separated off by delamina
tion from the embryonic knob, the remaining cells of the
latter form the ' embryonic ectodei'm,' which is thus situated
between the entoderm and the trophoblast.â€
Assheton, in the paper just referred to, has given a careful
account of the first appearance of the entodermal cells in the
rabbit, and of what he believes to be the mode of their
peripheral extension below the trophoblastic wall of the
blastocyst. He shows that the inner cell-mass, at first
spherical, gradually, as the blastocyst enlarges, fiattens out
below the “ covering layer †of the trophoblast until it forms
an approximately circular plate “ nowhere more than two
cells thick.†During the process of flattening, cells are seen
to jut out from the periphery of the mass; these eventually
separate, and appear as rounded cells scattered irregularly
over the inner surface of the trophoblast and ‘^extending
' ‘ Zeitschi'. f. wiss. Zool.,' Bd. Hi, 1891.
THE EAHLY DEVELOPMENT OF THE MAPSUPIALIA. 71
over an arc of about 60° from the upper pole in all directions.â€
These “ straggling†cells, as Assheton terms them, as well as
the innermost cells of the now flattened inner cell-mass, are
regarded as hypoblastic and the outermost cells of the same
as epiblastic (embryonic epiblast). “The hypoblast, as a
perfectly definite layer, is formed by the time the blastodermic vesicle measures '5 mm. in diameter, that is, about the
102nd hour after coition. It is not, however, as yet by any
means a continuous membrane ; it is a network or fenestrated
membrane. For this reason, in section it appears to be
represented by isolated cells lying beneath the embryonic
disc (v. fig. 29, Sy.)†(cf. Dasyurus). In considering the
question how the peripherally situated (“ straggling â€) entodermal cells, which are undoubtedly derived from the inner
cell-mass, “apparently Avander round the inside of the blastodermic vesicle,†he I'eaches the conclusion that this is not the
result of amoeboid activity or growth “in the sense of migration †on the part of these cells, but “ is only an apparent
growth round produced by the more rapid growth of a
zone of the [trophoblastic] wall of the vesicle immediately
surrounding the embryonic disc, in which zone the marginal
cells of the inner mass lie.†He is unable to find any
evidence of the production of pseudopodial processes by
these pei'ipheral entodermal cells, the majority of them
appearing at first to be quite isolated from each other and
approximately spherical. “Certain of the cells here and
there are connected by threads of protoplasm, but this, I
think, is not a sign of pseudopodic activity, but merely
indicates the final stage in division betAveen the tAvo cells.â€
By the sixth day the hypoblast of the embryonic disc has
assumed the lorm of a continuous membrane, composed of
completely flattened cells, Avhilst the peripheral hypoblast
cells have become more numerous, and “many of them,
possibly all of them, are noAV undoubtedly connected by more
or less fine protoplasmic threads.†Such, in brief, is
Assheton's account of the early history of the entodenn in
the rabbit; it presents obvious points of agreement with my
72
J. P. HILL.
own for Dasyunis, and I ventui'o to think the agreement is
even greater than would appear from Assheton's conclusions.
In adopting- the view that the more active growth of the
region of the blastocyst wall immediately surrounding the
inner cell-mass is the sole causal agent in effecting the separation and peripheral spreading of the entodermal cells, I cannot
but feel, in view of his own description and figures and of my
own results, that he has attributed a much too exclusive importance to that phenomenon and a much too passive role to the
entodermal cells themselves. In Dasyurus the inward migration and the later peripheral spreading of the entodermal
cells is effected without any such marked unequal growth of
tlie blastocyst wall as occurs, according to Assheton, in the
rabbit, as the direct outcome of their owu inherent activity,
and I believe the possession of a like activity characterises
the entodermal cells of the rabbit. The evidence of Assheton's
own fig. 40, which shows in surface view a portion of the
vesicle wall with the peripheral entodermal cells in relation
thereto, and which should be compared with my figs. 68 and
69, conclusively demonstrates, to my mind, the possession by
these cells of amoeboid properties, and thus support is
afforded for the belief that the separation of the entodermal
cells from the formative cell group (inner cell-mass) is here
also the expression of an actual migration. Whether or not
the strands of protoplasm which Assheton ('08, '09) describes
as present in the sheep, pig, ferret, and goat, connecting the
inner lining of the inner mass to the wall of the blastocyst,
and which he interprets as tending “ to show that the inner
lining of the inner mass is of common origin with the wall of
the blastocyst,†are of any significance in the present connection, I cannot certainly determine.
4. Summary.
The results and conclusions set forth in the preceding
pages of this chapter may be summarised as follows;
(1) The unilaminar wall of the blastocyst of Dasyurus con
THE EARLY DEVELOPMENT OE THE MARSUPIALIA.
73
sists of two regions distinct in origin and in destiny, viz. an
upper or formative region, derived from the upper cell-ring
of the 16-celled stage, and destined to furnish the embryonal ectoderm and the entoderm and a lower or nonformative region derived fi-om the lower cell-ring of the
mentioned stage, and destined to form directly the extraembryonal or trophoblastic ectoderm (tropho-ectoderrn) of the
bilaminar vesicle.
(2) The formative region, unlike the non-formative, is
constituted by cells of two varieties, viz. : (i) a more
numerous series of larger, lighter-staining' cells destined
to form the embryonal ectoderm, and (ii) a less numerous
series of smaller, more granular, and more deeply staining
cells, destined to give origin to the entoderm and hence
distinguishable as the entodermal mother-cells.
(3) The entodermal mother-cells, either without or subsequently to division, bodily migrate inwards from amongst the
larger cells of the unilamiuar wall and so come to lie in
contact with the inner surface of the latter. Tkey thus give
origin to the primitive entodermal cells from which the
deKnitive entoderm arises. The larger passive cells, which
alone form the unilamiuar wall after the inward migration of
the entodermal cells is completed, constitute the embryonal
ectoderm.
(4) The entodermal cells as well before as after their
migration from the unilamiuar wall are capable of exhibiting
amoeboid activity and of emitting pseudopodial processes, by
tlie anastomosing of which there is eventually formed a
cellular entodermal reticulum underlying, and at first coextensive with, the embryonal ectoderm.
(5) The definitive entoderm thus owes its character as a
connected cell-layer primarily to the formation of secondaiy
anastomoses between the pseudopodial processes emitted by
the primitive entodermal cells (or entodermal mothercells).
(6) The assumption by the entodermal cells of amoeboid
j^roperties whilst they are still constituents of the unilamiuar
74
J. P. HILL.
wall affords an intelligible explanation of the mechaiiisin of
their inwai'd migration.
(/) The entoderm is first laid down below the formative or
embryonal region of the blastocyst; thence it extends gradually by its own growth round the inner surface of the uuilaramar non-forrnative region so as to form eventually a
complete entodermal lining to the blastocyst cavity. In this
way the blastocyst wall becomes bilaminar throughout.
(8) The bilaminar blastocyst consists of two reguous, respectively embryonal and extra-embryonal. The embryonal
region (embryonal area) is constituted by an outer layer of
embryonal ectoderm and the underlying portion of the entoderm, and the extra-embryonal, of the extra-embrvonal or
trophoblastic ectoderm (tropho-ectoderm), which is separated
from the embryonal by a well-marked junctional line, together
with the underlying portion of the entoderm, which is perfectly continuous with that below the embryonal ectoderm.
(9) The formative or embryonal region of the blastocyst
in Dasyurus is from the first freely exposed, and at no time
daring the developmental period dealt with in this paper
does there exist any cellular layer externally to it, i. e. a
covering layer of trophoblast (Deckschicht, Kauber's layer)
is absent and there is no entypy of the primary germ-layers
(cf. p. 111).