Text-Book of Embryology 2-8 (1919)

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Kerr JG. Text-Book of Embryology II (1919) MacMillan and Co., London.

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Chapter VIII Modifications of the Envelopes and other Adaptive Modifications Occurring During the Early Development of the Amphibia

The Amphibians form a group of Vertebrates which have taken less or more completely to a. terrestrial existence in their adult condition. They have not been able to emancipate themselves entirely from the ancestral aquatic habitat, possibly on account of the feeble development of the horny outer layer of the epidermis. They are still as a rule entirely aquatic during the early stages of their development,the eggs being laid in water and the young animal passing its larval existence in the water.

In a number of cases, particularly in Anura inhabiting tropical regions with a well-marked dry season, very interesting adaptations are found whereby the young animal is enabled to pass a more or less prolonged period out of the water. In the ﬁrst type of these adaptations we ﬁnd special modiﬁcations of the tertiary envelope which is normally a simple mass of jelly deposited round the egg.

The ﬁrst type of such adaptation is exempliﬁed by various species of If;/locles and by Rana opistltorlon in which the eggs are simply deposited in free air in damp spots, each surrounded by a transparent spherical protective shell. In R. opisthoclon (Boulenger, 1890) the young Frog before hatching develops on the tip of its snout a small conical protuberance apparently used like the egg-tooth of Reptiles and the similar organ in Birds to tear open the egg-envelope. A further interesting adaptive feature. is that the young unhatched Frog possesses on each side of its body a series of vascular ﬂaps of skin somewhat resembling the gill-flaps of an Elasmobranch ﬁsh and apparently functioning as respiratory organs.

In a considerable number of tropical Anura the ovidueal secretion which surrounds the eggs is, at the time of laying, beaten up by rapid movements of the hind feet of the parents into a ﬁne foam or froth with numerous entangled air-bubbles. This may be deposited on the surface of a pool where it floats about like a ﬂeck of ordinary foam with the developing eggs scattered through it (Paludiwla

fuscomacula/u.). At a particular stage in development a digestive

ferment apparently is secreted, probably by ectodermal gland cells, which liqueﬁes the jelly and allows the larvae to drop through into the underlying water.‘ In other cases the mass of foam is deposited in an excavation in the ground, so situated that rain-water readily trickles into it (Engystrmza orale), or merely in a damp spot. In the case of the Japanese 1t’lz.ucoplo.orus (.Polg/pedates) so/Llegelé (Ikeda, 1897) the b11rrow is made in a bank by the margin of standing water and after the mass of egg-foam has been deposited the pair of Frogs make their way out by excavating a tunnel which slopes downwards and opens near the water’s surface. Here again at the appropriate stage. of development the jelly liqueﬁes and the. young larvae are carried down by it into the water.

In the case of Phy/lloznedwsct 11.3/pot-/aonu’rial'£s the process of oviposition was observed by Budgett (1899) in the Gran Chaco. The eggs are deposited during the night, the female clambering up amongst the leaves of a suitable plant by the margin of a pool, with the male on her back (Fig. 208). With their hind legs the. two Frogs bend the margins of a leaf together so as to form a funnel into which the eggs are poured together with the fertilizing sperm. The eggs are enclosed in a mass of ﬁrm adhesive jelly which causes the leaf to retain its funnel shape. The eggs develop within the jelly up till

1 It is probable that. such ferments play an important part in softening the eggcnvclopes preparatory to hatching in various animals. Thus in Lcpidosircn the

process of hatching is rendered possible by the softening of the egg-shell brought about apparently by digestive ferment secreted by the ectoderm covering the body (Graham Kerr, 1900). The same appears to he the case in Telcosts (Wintrebert, 1912). In Xrmbpus amongst Amphibians :1. similar process apparently takes place and in this case Bles (1905) attributes the formation of the ferment not simply to the diffuse activity of the cctodcrm cells but to the action of a special “frontal gland.” It seems not improbable that the formation of such hatching ferments will be found to occur very generally in aquatic Vertebrates.

Flu. ‘Z08. _I’/1,:/llunuv/ustt l1._c/pm:/u_;m.lr£u.l-is, l'e1u.ale carrying male on her back during oviposition. (After Builgttt, 1899.)

contain no egg in their interior? The eggs are thus protected both above and below by a thick mass of eggless spheres. During the later stages of development the layer of envelope next the surface of each egg becomes greatly distended by the accumulation of ﬂuid within it, the jelly between the eggs meanwhile diminishing in volume. with their huge external gills have thus considerable room in which freely. Eventually the envelope ruptures and the larva hatches. comes to be occupied by a seething mass of tadpoles, ﬂoored and roofed in by a thick mass of jelly formed by the empty Eventually——in from 12-24

spheres.

the stage of a tadpole of 9-10 mm. in length. During this process the jelly apparently liqueﬁes, until only a thin membranous bag containin g watery ﬂuid surrounds each embryo. Eventually the remains of the jelly with its contained tadpoles trickles downwards into the water. of the water has retreated from immediately below the leaf the tadpoles may still make their way for a distance of several inches to the pool by active jumping movements, helped it may be by a shower of rain.

In the allied I’hg/llomedusa sauvagii, from the same neighbourhood, a similar mode of oviposition occurs, though here the nest is composed of several leaves (Fig. 209). Agar (1.909) ﬁnds in this case that both at the commencement and end of oviposition there are laid a large number of spheres of jelly which

'l‘he larvae to move

The nest thus

hours after the bulk of the larvae have

hatched——the jelly begins to deliquesee and the larvae drop down with it into

the water.

FM. 209. - -— I‘/lg/ll4ruu;du.w so I’ ('14;/ii, mass of spawn. (After Agar, l909J

Similar nesting habits occur in other tropical Hylids, e.g. Phyll0 1 In the eommon I‘-‘rocr j.’u-nu. /nu.-~m'-rm-in. a narent] em it ca wsnles ma be formed an I l.l y l. y l y

in quantity in the oviduct before eggs begin 10 enter it (Wezel, 1908). with the normal eggs Agar found 2-3 per cent nl'.s1u:l] eggless capsules.

Interspersed 'l‘hese appear

to be deposited round small solid particles such as fragments of shed epithelium

(Lebrun, 1891).

In C'671.t7'opho7'us, where the left ovary is no longer functional, empty tertiary envelopes are frequently still formed in the left oviduct (Braus, 1906).

If, as sometimes happens, the margin

I medusa vllterringvli (von Ihering, 1886), H3/la nebulosa (Goeldi, 1895),

Rltacopltorus 're7Jnwardt'£'13(Siedleeki, 1909). In the last mentioned the eggs are deposited in a mass of foam enclosed in one or several leaves (Fig. 210). At the appropriate time the central portion of the mass liqueﬁes and the colourless tadpoles make their way into this central ﬂuid —«—~ the superﬁcial layer of the mass being hard and dry. Eventually the lower part of the mass softens and the

_1iq_uid containing the tadpoles trickles out on to the ground where

the larvae are able to continue their development in the smallest puddles. s

In the second type of such adaptations the eggs or young are carried about, away from the water, by one of the parents. In the simplest of such cases no structural modiﬁcation of the parent's body is involved. Thus i_n A/,3/tes ribstetrwicans the male draws the strings of eggs out of the cloacal aperture of the female and loops them round his thighs-——the portion of oviducal secretion lying between successive eggs- becoming highly elastic and gripping the thighs tightly. Oviposition takes place on land and the male pays only occasional visits to the water. When one of these happens at the appropriate period the. young hatch in the form of tadpoles while the male parent resumes his terrestrial habits.

In a number of - cases the transport of the young by the parent takes place at a later period, when the tadpole stage has been reached, the larvae adhmhing to the back of the male parent and so being transported from one pool to another (Fig. 211, A). This habit occurs in various species of Iﬂzndrobates and P/b3/U0- p A _ bates (Brandes u. Schoenichen, 1901). 1“‘5,‘,;(,)_:§}g.' "fl£1’"(f)';?’t’f‘;f;El

In the most interesting cases however },,,M,,.,,’ ,p‘.“1‘I;‘f)1t,_\__ ‘(11,;,-W. 5,9,1. the transport of the eggs or young by the lvvki, 1909-) parent is associated with the making use of some particular structural feature of the latter——-either permanent or specially developed for this purpose- In Rhacophorus reticulatus (Uriiiitlxer, 1876) the eggs are carried about by the female, adherent to its ventral surface. In Iig/la goeldivl (Boulenger, 1895) the eggs adhere to the dorsal surface of the female, only in this case the skin of the parent responds to the stimulus afforded by the presence of the eggs and grows up into a slight ledge surrounding them (Fig. 211, B). In Pipe amcricana (Bartlett, 1896) the cloaca of the female is protruded at the time of oviposition as a large spout-like structure which projects forwards between the dorsal surface of the female and the ventral surface of the male. The eggs pass out one by one through this and are distributed at fairly equal intervals over the dorsal surface of the trunk of the female. The skin now proliferates actively, growing up so as to form highly vascular partitions between the eggs, each of the latter coming to be enclosed in a deep pit. The mouth of this becomes closed in by a dark-coloured operculum, possibly formed of hardened epidermal secretion. Each egg is thus enclosed in a little chamber in which it passes through the early stages of its development, including a modiﬁed tadpole stage, and issues forth eventually (after about 82ldays) as a young Toad.

In another set of Anurous Amphibians the eggs undergo their development in a spacious single cavity

  within the parental body. In Rhivzoderma

darwvlml (Jimenez de la Espada, 1872;
Plate, 1897) this cavity is the enlarged

unpaired croaking sac of the male, into

which the eggs, to .the number of from
5 to 15, are swallowed and from which the
 young issue after completing the tadpole

, stage. In the genus Nototrema the brood

cavity is a special large pouch lying
 beneath the skin of the back, lined by
involuted epidermis and opening to the
exterior just in front of the cloacal aperture.

In different species of the genus there is much difference in the length of time

 during which the developing embryo is
retained within the pouch, the length of

this period being apparently correlated with the size of the egg and the amount 1.~IG_ 21]__A, M1,, ,,,- [:/,.‘,/g[,_,_ of food-yolk stored within it. Thus in hates to-'initatz's carrying tad- N. vizarsupiatum there may be as many as P°‘;";',.?. "B! .f""“‘1f_°f ff’Jt"‘ 200 eggs in the pouch, each measuring ?;':',"',,'1',l.',",,_,.(,'.',i.1_‘ rjV§1;,%_i;"gb' ( er about 5 mm. in diameter (Brandes u. Schoenichen, 1901), and the young make their way out as typical tadpoles which doubtless lead for a time a free aquatic existence before metamorphosis takes place.

In N. omgfemm (Weinland, 1854) the eggs are much larger

(10 mm.) and fewer in number (about 15) and in this case as in the

. allied N. testudinemn and N. ﬂs.s"ipes, which also possess large eggs,

the young go on developing within the pouch until after the period of metamorphosis.

In Noto/mama. an interesting adaptive feature characterizes the external gills. These organs are present upon branchial arches I and II, each consisting of a long slender stalk, which passes at its outer end into a thin highly vascular membrane formed by the fused and expanded outer ends of the two external gills. The two membranes so formed, one on each side of the body, are closely applied to the inner surface of the thin egg-envelope. The outer surface of the envelope is in turn in intimate contact with the highly vascular lining of the pouch which sends projecting folds in between the eggs. We have here clearly an adaptive arrangement to minister to the respiratory needs of the developing young, analogous with that provided by the allantois of a Reptile or Bird.

It appears somewhat puzzling that the eggs of Nototrema should come to be contained in a pouch the opening of which is much smaller than the cross-section of the egg. The probability appears to be (Boulenger, 1895) that the pouch is formed in response to the presence of the eggs upon the animal’s back, a ridge growing up round the eggs as in the case of fig/la. goelrlvli but in this case continuing its growth towards the mesial plane until the corresponding upgrowths from the two sides meet and completely roof in the pouchlike cavity. Support is given to this explanation by the condition in N. pg/gznacmn where the opening of the pouch is in the form of a median longitudinal slit, prolonged forwards as a kind of seamvor raphe along which the roof of the pouch readily tears and which presents all the appearance of having been formed by the coming together of two originally separate lips.

It must never be forgotten that such peculiarities of development as have been alluded to in the above--mentioned Anura involve adaptive modiﬁcations on the part of the young individual itself. The most frequent of such modiﬁcations is physiological adaptation, as shown for example by the fact that the transference of the young individual to water before the normal time is commonly fatal. In other cases structural adaptations of a more conspicuous kind are apparent. Thus in 1-’1Ipu. the late tadpole stage, although enclosed within its cell, develops a broad and highly vascular ta.il which doubtless serves for 1'espirato1'y and possibly nutritive interchange with the maternal tissues: again in ]Vutotrema, the external gills show the peculiar modiﬁcation already alluded to. The true external gills are in several cases absent, their function being taken over by the vascular surface of the yolk, while in such a case as Rana opz'.s-thodcm. special new respiratory organs have been developed.

In the various modiﬁcations of development dealt with in the

‘preceding section we have to do with attempts, so to speak, on the

part of isolated members of a particular group of Vertebrates (Anura) to lessen the degree of their dependence upon the ancestral aquatic habitat. Such attempts amongst the existing Amphibia are not altogether successful: the group as a whole remains chained to a watery, or at least humid, environment.

The lower Vertebrates which made a real success of terrestrial existence, emancipating themselves entirely from the aquatic environment, are represented to-day by the Amniota, and it remains now to study their special modiﬁcations of development. 464 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

III. ADAPTIVE MODIFICATIONS IN THE DEVELOPMENT or THE AMNIOTA.-—It is characteristic of many Vertebrates that, associated with the provision of special arrangements for nourishing the young individual, the tiI11e of commencing an independent life on its own account is greatly delayed. In such cases where a considerable proportion of the whole development takes place within the shelter of the egg-shell (or of the parental body) we have to do with what is known as embryonic in eontradistinetion to larval development. During embryonic development the young individual is free from the necessity of ﬁghting and lending for itself; it is to a great extent sheltered from the struggle for existence, and in correlation with this we ﬁnd remarkable hypertrophies and modiﬁcations of various parts of the body taking place which in a free state would render life impossible.

The ﬁrst of these modiﬁcations makes its appearance in the lower, aquatic, Vertebrates in the form of a pronounced bulging of the ventral side of the body. In the more primitive holoblastic Vertebrates this is caused by the great thickening of the ventral endoderm (Fig. 80, E, p. 146), its cells being much enlarged and packed with granules of yolk. Where this distension of the endoderm cells is most marked anteriorly there is brought about the tadpole shape of body as seen in the Ganoids and Lept'do.s7I7vm: or, on the other hand, the distended region may be situated towards the hinder end as in _l-’et7'0r/nyzon, Uemtodas or the Grymnophiona. In such cases as development proceeds the large yolk-cells go on segmenting, the yolk within them is gradually used up, and the Inass of endoderm, becoming Inore and more attenuated, ceases to project beyond the general outline of the body.

In the meroblastic egg, as has already been shown, the proportion of living protoplasm amongst the yolk has been reduced to vanishing point so that except superﬁcially the yolk never segments. Typically it becomes gradually enclosed in the endoderm which spreads over its surface. There is thus formed what is known as the yolk-sac, a structure ‘usually of enormous size as compared with the rest of the embryo. lt will readily be understood how impossible a free active existence would be while there is a large yolk-sac present. The assimilation of yolk and its transport to the actively growing parts of the embryo are brought about mainly by the rich development of superﬁcial blood-vessels forming the vitelline network. In typical Teleosts, ag. Salmonids, the yolk-sac becomes at an early period completely separated from the dorsal part of the endoderm which becomes the functional gut, the yolk absorption taking place entirely by the vitelline vessels.

An important point to be remembered is that the vitelline network though primarily nutritive in function is necessarily also respiratory, gaseous interchange taking place between the blood circulating in its vessels and the medium which bathes its surface. The vitelline network is the primary breathing organ in the great VIII DEVELOPMENTAL AD APTATION S 465

majority of Vertebrates during early stages of development. In cases where the embryo lies in contact with maternal tissues the respiratory exchange takes place ultimately, through the thin intervening layers of ﬂuid or envelope, between the blood circulating in the vitelline network and that circulating in the oviducal lining of the mother. In this way all the necessary preliminary conditions are provided for the evolution of a placenta, and as will be shown later these conditions are actually taken advantage of in some cases and a simple yolk-sac placenta is formed.

In the more highly developed types of yolk-sac the splanchnic mesoderm which surrounds the vitelline vessels sprouts inwards, forming irregular vascular septa which project into the yolk-sac. This modiﬁcation, which brings about a great increase in the assimilatory surface, reaches such a development in Birds that towards the end of incubation these ingrowths form an irregular meshwork of vascular trabeculae traversing the whole of the yolk right to its centre.

Eventually the yolk, whether in the form of a yolk-sac or a mass of heavily yolked cells, is enclosed within the ventral wall of the body. In the holoblastie Vertebrates this comes about as already indicated by the simple spreading of the blastoderm over the surface of the yolk so as completely to enclose it. In the Fowl the spreading of the blastode)rm, and its derivatives the endoderm and mesoderm, round the yolk is never quite completed, there remaining a small circular patch at which the yolk is separated from the albumen only by the remains of the vitelline membrane (of. Fig. 215, am).

Further in the Amniota the region of somatopleure bounding the coelomic space in which the yolk-sac lies becomes converted into amnion and serous membrane (of. Fig. 215, A), and is eventually cast off‘, playing no part iii the formation of the definitive body-wall. The yolk thus lies outside the limits of the deﬁnitive body-wall, projecting through the umbilical funnel which is bounded all round by the stalk of the amnion. Eventually, shortly before hatching, the edges of the umbilical opening are drawn over the yolk-sac in a manner which will be described later (see p. 475). In llacerta mlmlpztm in which the yolk-sac is reduced the remains of it are simply cast off according to Strahl.

The most remarkable of the excrescences adaptive to an embryonic existence are the organs known as Amnion and Allantois ——portions of the embryonic body which become greatly hypertrophied and perform important functions during embryonic life but which are eventually, for the most part, shed about the time of birth or hatching and play no part in the formation of the body of the adult.

AMNION.—-The most nearly primitive subdivision of the Amniota is the group Reptilia and we accordingly turn to it and more especially to the Ohelonia, which have been worked out by Mitsukuri (1891), to provide a foundation for our description.

VOL. II 2 II B

Fro. ‘.212.—-Chelonian blastodenns illustrating the development of the amnion. (A and C after Mitsukuri, 1891.)

A, ('Iemm.ys; 13, tfhelzudm; C, Ulemmys. a, amnion with neural rudiment seen indistinct.1_v through it; a.u., edge of amniotic ﬂap; a.r, amniotic tunnel; c.g, cephalic groove; f, inconstant fold which is sometimes present; 31.1‘, gm-‘:trul8I' rim ; m._f, medullary fold ; gm, proamnion with head of embryo showing through it. *

466 CH. VIII DEVELOPMENT OF AMN ION 467

In Chelonia the iirst indication of amnion formation appears at a stage like that represented in Fig. 212, A. The future body of the embryo, indicated by the medullary folds, lies ﬂat on the surface of the egg, extending out all round into the blastoderm. The ﬁrst sign of the amnion is produced by thefront end of the medullary plate coming to dip downwards so as to form a deep slit or groove (Figs. 212 and 213, c._q) curving tailwards on each side as seen from above. '1‘he posterior wall of this slit forms the anterior limit of the head of the embryo while its anterior wall forms the rudiment of the amnion (Fig. 213, me). The portion of blastoderm in front of and to the side of the head of the embryo is as yet two-layered, the Inesoderm not yet having spread into it, and it follows that the amniotic ru(:1in1ont is also two-layered. This region of the blastoderm,

FIG. 213.——-Sagittal section through the head end of a Chelonian embryo. (After lVIit'sul<m'i, 1891.)

t.l..(:, anmiot;-iv ml;_-,-u : mgr, cephalic groove; earl, 4'-I.-t.m1r-1'-n1 of medullary plate ; end, oudoderm.

which is still without mesoderm and which in this case forms the amniotic rudiment, is termed the proamnion. As development proceeds the head end of the embryo increases in size and as it does so it dips more and more downwards so as to deepen the cephalic groove or slit in front of it. While this is going on there takes place active growth of the ectoderm along the sharp edge of the amniotic rudiment (Fig. 213, a.e) i.n such a way that this edge becomes prolonged backwards as a solid ﬂap, covering over the body of the embryo from before backwards. This amniotic ﬂap continues to grow tailwards, its growing edge concave and prolonged backwards on each side (Fig. 212, B, a.e), until it reaches the tail end of the embryo, so that the whole of the latter is covered in by an amniotic roof. Nor does the process stop now: it goes on with the result that there is formed a long tunnel (Fig. 212, C, a.t) continuous in front with the amniotic cavity, ~23.e. the cavity between 468 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

the body of tlie embryo and the amnion, a11d terminating behind in an opening bounded above by a concave free edge (a.e)._

An important point to realize is the relation of the amnion to the cell layers. The ﬁrst rudiment, as has been indicated, is composed of the two primary layers ectoderm and endoderm, and this applies also to the lateral prolongations baclnvards of the free edge. The whole of the amniotic roof however except these marginal parts is formed at first of solid ectoderm and of ectoderm alone (Fig.

FIG. 214. —-—Diagrammatic transverse sections through Clielonian en1ln‘_\'ns (f-.'!v-m-nz.a/.s-. A, stage with 2-3 mesoderin segments; B, 6-7 segments) i1ln.s-1.r::t_i'n«,-; tlw rela1..ion.~e of tinamnion. (Based on ﬁgures by Mitsnkuri, 1891.)

a.f, amniotic ﬂap; am, amnion: H", I'(:l.u¢lterm; rm/, vndoderrn; _/Zn, fnI.~u-_ amnion: 'nu-.<-, 1m-sods-.rm segment; N, notoehord; srI., so-ru-amniotzie junction; mm, somatoplenre: spl, sphmuhnupleme; splc, splanchnocoele.

214, A, a.f). As development goes on the mesoderm extends between ectoderm and endoderm and then splits into somatic and splanchnic layers. The result of this is that the endoderm, with its covering of splanchnie mesoderm, sinks down and no longer projects upwards on each side into the base of the amnion (Fig. 214, B). The somatic mesoderm on the other hand does continue to project into the base of the amnion just as did the endoderm previously (Fig. 214, B). The originally simple ectodermal roof of the amniotic cavity undergoes a process of splitting from its lateral margin inwards and as this split extends towards the mesial plane. the amniotic fold of VIII DEVELOPMENT OF AMNION 469

somatic mesoderm spreads with it. Except along the middle line the amniotic roof thus becomes double——-the inner roof being formed of ectoderm internally and somatic mesoderm externally, the outer roof of somatic mesoderm internally and ectoderm externally. Of these. two roofs the inner is the amnion (Fig. 214, B, am), the outer is the false amnion or serous membrane (f.a). The portion which retains its original condition of being formed of unsplit ectoderm (sa) may be. called the amniotic isthmus or the sero-amniotic connexion (Mitsukuri). During later stages of development this becomes reduced to a thin vertical partition in which form it persists throughout, except in the region of the head where it disappears entirely so that there is here a continuous coelomie space stretching from side to side between amnion and serous membrane.

’J‘he posterior tubular prolongation of the amniotic cavity becomes obliterated through part of its extent and in this way the amniotic cavity becomes completely closed.

The first-formed part of the amnion, lying in front of the head of the embryo, remains for a time proamniotie in character, '£.e. composed of ectoderm and endoderm, but eventually the mes'oderm and eoelomie. space spread in between the two primary layers and the portion ot' the amnion in question comes to resemble the rest.

As the body of the embryo becomes constricted oil’ from the yolksac the basal edge of the amnion continuous with that of the embryonic somatopleure becomes tucked inwards so that the amnion, which formed in earlier stages a mere roof, comes to form a complete envelope. The amniotic cavity is ﬁlled with secreted ﬂuid in which the body of the embryo ﬂoats.

BIRDS.-——-The process of amnion formation i11 the Birds shows conspicuous dil‘f'erenees from that which has been described for the more primitive Reptiles. Two of the chief of these dili'ere.nces seem to be associated with the fact that the amnion develops relatively later in the Bird, at a period when the head and anterior body region of the embryo project prominently above the general level of the blastederm and when the mesoderm has already split into splanchnic and somatic layers. Correlated with this fact we ﬁnd (1) that in the Bird the amniotic rudiment has to grow upwards so as to surround the projecting head and trunk, and (2) that the upgrowth is composed of somatopleure only.

The amnion may be said to originate as a kind of wall, formed of a11 upwardly projecting fold of somatopleure, which comes to surround the actual body of the developing embryo. This wall is not absolutely vertical: it is tilted, or inclined inwards, towards the middle of the embryonic body. With increasing growth it projects more and more over the body of the embryo, its free edge bounding a gradually diminishing opening, through which the body of the embryo is visible when looked down upon from above. Eventually this opening is reduced to vanishing point and the body of the embryo is completely 4'70 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

covered in by a double roof formed by the amnion and the serous membrane.

The amniotic fold does not develop with equal activity throughout its extent. Its growth is much more active anteriorly than elsewhere, with the result that the headward portion of the fold becomes extended rapidly backwards as an amniotic hood over the head and anterior end of the body of the embryo (cf. Figs. 233, 235, 236). '.l‘he last remnant of the amniotic opening is consequently situated quite near the hind end of the body.

Correlated with the later appearance of the amniotic hood——at a time when the coelomic cavities are extensively developed—-it is at no period composed throughout, from side to side, of a simple layer of unsplit ectoderm as was the case with the Chelonian. It is of interest to notice however that the sero-amniotic isthmus has not altogether disappeared, although it never has the breadth that it has in early stages in the Ohelonian.

The details of amnion formation are readily observable in the Fowl and have been fully described by Hirota (1894). The process takes place as follows: The iirst step consists in the appearance of a crescentic upgrowth of blastodcrm just in front of the head of the embryo at about the stage of 14 segments. At this period the mesoderm has spread forwards on each side but has not yet extended i11to the space immediately in front of the embryonic head (proamnion). Where the mesoderm is present it has split to form the coelome and owing to this being ﬁlled with secreted ﬂuid the somatopleure bulges up somewhat so as to be conspicuously marked oil’ from the ﬂat proamniotic area. The amniotic fold makes its appearance just about the anterior boundary of the. proanmion. As it increases in height it overlaps the head of the embryo and grows backwards over it as the amniotic hood (Fig. 233). Into the fold the mesoderm and coelomic cavities have already penetrated. Where the mesoderm from the two sides meet in the mesial plane of the hood the two portions of coelome do not open freely into one another but remain separated by a septum of mesoderm—-the mcsedermal sero-amniotic isthmus. At an early period of the backgrowth of the amniotic hood the ectoderm in the middle of its free posterior edge is seen to project headwards as a small wedge, the base of which is formed by the growing edge. As this wedge is carried backwards by the continued progress of the amniotic edge it leaves behind it a kind of trail in the form of a continuous line, or rather partition, of ectoderm connecting the ectoderm on the outer surface of the amniotic fold with that on its inner surface. This is clearly the ectodermal sero-amniotic isthmus of the Reptile persisting in a much attenuated form; the attenuation being due to the fact that the coelomic spaces have extended much nearer to the mesial plane than in the corresponding stage of amnion-formation in the Reptile.

Up till about the time when the amniotic hood has completed its backgrowth its cavity--—-the amniotic coelome—-—remains divided VIII DEVELOPMENT OF AMN ION 471

into two separate halves by a septum, which in front is purely mesodermal but throughout the rest of its extent is traversed by the ectodermal sero-amniotic isthmus. The anterior, purely mesodermal, part of the septum disappears early in the fourth day so as to make the amniotic coelome continuous from side to side, but the rest of the septum persists throughout the whole period of development although its central ectodermal portion becomes gradually reduced and by the tenth day has completely disappeared.

Towards the end of the second or early in the third day the tail of the embryo begins to project, bending ventrally and dipping downwards as it does so. As it does this the tail comes to be hidden under a projecting amniotic fold precisely as happened at the head end except that here the coelomic cavity is already completely continuous across the mesial_ plane there being no trace of a septum or sero-amniotic isthmus. The free edge of this “tail fold” of the amnion is, as was that of the “head fold,” concave only here the concavity is directed headwards. Early in the fourth day the concave edges of the head and tail folds become continued into one another at about the level of the hind limb rudiment, so that the body of the embryo is now surrounded by a continuous amniotic fold———most highly developed anteriorly where it forms the amniotic hood, less so in the caudal portion and least of all laterally. The more or less elliptical opening bounded by this fold, through which the dorsal surface of the embryo is exposed, gradually shrinks as the fold grows and eventually, during the ﬁrst half of the fourth day as a rule, it becomes obliterated and the amniotic cavity closed.

The true amnion at first closely enshcaths the head and trunk of the embryo but from about the ﬁfth day onwards watery amniotic ﬂuid is secreted into its interior so as to form an extensive water jacket in which the embryo is suspended (Fig. 215). For a considerable period the embryo is gently rocked to and fro in the ﬂuid by the slow rhythmic contractions of muscle ﬁbres which develop in the somatic mesoderm covering the amnion on its outer surface.

The development of the amnion in the Sauropsida in general is adequately illustrated by the two types which have been described. There occur variations in detail. Thus the inequality in the activity of growth between the anterior and posterior portion_s of the amniotic fold so marked as a rule may be practically absent (Chameleons), or it may reach an extreme limit, the posterior

portion of the fold being obsolete and the anterior portion continuing

its backgrowth past the tail end of the embryonic body to form an amniotic tunnel, as in the Chelonians above described (Sphenodon, Gannet———S'ula, Puﬂin—Frate'rcula).‘

ALLAN'1‘oIs.———The allantois may also be conveniently studied in the Bird. In the Fowl it makes its ﬁrst appearance as a little clear

‘ Schauinsland , 1906. 472 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

vesicle, projecting from the ventral side of the trunk near its hind

Fm. 215.-—~—Diug1-ams illustrating the arrangement of amnion, allantois, etc., in the Fowl. (After Lillie, 1908.)

A, fourth da '; B, ninth day. (1.0, amniotic cavity; alb, albumen; all, allantoic cavity; u.ll.st, allantoic stalk; am, amnion; coal, eoelome ; f.a, false amnion, or serous membrane; sa, seroamniotic isthmus; spl,splanchnop1eure; v.m, vit.elline membrane; 3/, yolk; 1, outer wall of allantois fused with serous membrane; 2, inner_wa1lofa1lantois. VIII ALLANTOIS 473

end (Figs. -239, 240), and serving for the reception of the renal secretion. 'l‘he study of sections shows that the allantois is simply a pocket of the ventral wall of the gut towards its hind end--correr sponding exactly with the bladder of an Amphibian. It is thus lined with endoderm and covered externally with splanchnic mesoderm. The allantois like the bladder of the Amphibian bulges into the splanchnocoele. As development goes on the allantois, distended with ﬂuid, increases in size, projecting on the right or upper side of the embryo till it comes in contact with the inner surface of the soniatopleure (Fig. 215, A, all), and with still further growth ﬂattens

out against the somatopleure taking a somewhat 1r_1_ushljopin-likeU

shape. In the case of an independently living airiiiiial such as an

- illlilc. 2l5A.~—-Diagram illustrating the arrangement of amnion, allantois, etc., in the Fowl. (After Lillie, 1908.)

C, twelfth day. ulb, albumen ; all, allantoie cavity; 3;, yolk.

Amphibian the allantoie outgrowth of the gut can only increase in size within the restricted space of the splanchnocoele which is already occupied by the viscera. In the Bird embryo on the other hand there are available for the growth of the allantois the wide—spreading extensions of the coelome, on the one hand between amnion and serous membrane and on the other over the surface of the yolk. The allantois accordingly spreads out all round towards the limits of this space (Fig. 215, B). As it does so it loses its rounded vesicular form, its proximal (Fig. 215, B, 2) and distal walls (Fig. 215, B, 1) approaching one another. The mesoderm covering its outer surface tends to undergo secondary fusion with that of neighbouring structures. Thus about the end of- the sixth day it fuses with the adjacent surface of the amnion. Again towards the time of hatching a similar fusion takes place with part of the yolk-sac. The most important of these fusions 474 EMBRYOLOGY OF THE LOWER VERTEBRATES 011.

however is that, which commences early in the ﬁfth day, with the inner surface of the serous membrane. ' At a comparatively early period (during the ﬁfth day) the mesoderm covering the allantois becomes vascular and as the organ Recoines flattened its proximal or inner and its distal or miter walls ecome strikingly different as regards their vascular-ity, the outer wall developing an extremely rich network of capillary blood_-ves§_<_:_s with very small meshes, while the inner wall possesses merely a gparse network together--.witl1 the large vessels of supply. This difference between the two walls of the allantois becomes conspicuous about the end of the sixth day of incubation in the common Fowl. The difference is associated with the fact that the distal wall of the allantois is destined to become the great respiratory organ, taking over this function from the vascular area of the yolk-sac by which it is performed during the early stages of development. In correlation with the more efﬁcient performance of this function the albumen, or white, as it gradually shrinks in volume and acquires greater density gizavitates down to the lower side of the egg thus bringing the mushroom-shaped allantois close up to the shell membrane on the upper side. The process is still further facilitated by the ectoderm of the serous membrane becoming reduced to a very thin—-hardly distinguishable-—-layer in the region where it is underlain by, and fused with, the allantois. The capillary network thus comes into very close relation with the shell membrane and the overlying porous

' shell, and gaseous exchange can readily take place between the blood

circulating in the network and the external atmosphere.

As development goes on the respiratory needs of the embryo become greater and greater and these are met by the allantois spreading outwards all round its periphery, so as to provide a greater and greater respiratory area. During this spreading outwards of the allantois the three main alla11t(_;ic__ves_sel§ are somewhat retarded in their growth with the result that each one causes an indentation of the growing edge of the allantois beyond which the allantois bulges on each side.

When the growing edge of allantois comes, after about nine days’ incubation, into the neighbourhood of the remaining mass of albumen, a new phenomenon appears inasmuch as the allantoic margin with its covering of serous membrane proceeds to grow onwards close under the shell membrane as a circular fold recalling the amniotic

[old and enclosing the mass of albumen (Figs. 215, B, 215A, 0). l The"

ectodermal lining of the cavity so formed sprouts out into the albumen in the form of irregular projections which become vascularized from the allantoic mesoderm and no doubt play a part in absorbing the last remains of the albumen. By about the end of the second week of incubation the shell membrane is lined throughout the whole of its extent by the highly vascular outer wall of the allantois. This remains the breathing organ until-—a day or two before hatching—the y_gu_ng_chick_’s__l)eak vm DEVELOPMENTAL ADAi>rxrioy_s 475

/‘=r":“T _ , _ _ penetrates the air_-space and'\ ulmonary breathmg\ begins. The

-«up-w

all_ant9_i_c circiilation then gradua ffiecoines sluggish and stops, and eventually by a process of autotomy the allantois is separated from the body of the embryo and is left behind as the vascular membrane seen lining the fragments of ‘shell from which a young bird has hatched. '

ENCLOSURE OF YOLK—SAC WITHIN THE EMBRYONIO BODY.--—As already indicated thF3ﬁ)1K—:sac~heco'mes eventually (about a couple of days before hatching in the case of the common Fowl) ,e_nclosed within the body-wall. The process by which this is brought about appears to be as follows (H. Virchow). With the growth of the embryo a great increase takes place in the area over which the amnion is fused with the proximal wall of the allantois (cf. Fig. 215A, C), the compound and highly muscular membrane so formed extending eventually almost completely round the yolk-sac. At its edge it is continued onwards by the somatopleure, this latter terminating round the circular area where the yolk remains exposed. The yolk-sac is thus contained in a space the wall of which is formed of the following components in sequence starting from the body of the embryo : (1) amnion, (2) amnion fused with proximal wall of allantois, (3) proximal wall of allantois and (4) somatopleure in the region of the distal pole of the yolk-sac. The proximal portion of this wall, being formed of amnion, is necessarily continuous with the body-wall of the embryo at the umbilical opening and further those parts of it formed from amnion and allantois are highly muscular and contractile. l)uring the later stages of development this wall slowly contracts and as it does so the yo1k—sac is pushed into the umbilical opening which closes after it.

_._EV QRIGIN.- QE.S|l11E.A.Ml>IION .——-As regards this question,

which has excited much controversy, the following appears to the

present writer to be the working hypothesis which ﬁts most easily the facts so far as they are known.

(1) The amnion originated as a fold of l)l€t.'s't0d6’7'?Il« round the body of the embryo (Fig. 216, A, B).

As has already been shown the amnion arises in this way in ontogeny in the Reptilia which are generally recognized as being the most primitive Amniotes. The same holds for the Birds and for some of the Mammals.

The Mammalia as a group are admittedly descended from ancestors in which the egg was large and meroblastic as it is in the Reptilia. This is indicated, apart from other convincing evidence, by the fact that they still exhibit in ontogeny a well-d_eve_loped though yolkless

_Jt follows then that it iswiiiadniissilile to regard facts

derived from the study of certain mammals in which the mode of amnion formation during ontogeny is of a‘ different, even though apparently simpler, type as constituting important evidence in regard to the phylogenetic origin of the amnion, as has been done in particular by Hubrecht (1895). vm DEVELOPMENTAL ADAPTATIONS 475

’‘v’?.‘’‘__'_‘ .5 .-.-.4-..»—.~-..~. u-...—oc-no-‘Q

_ _»_M ,_ A _~_ V__ . penetrates the air-s ace and(g11lgngn,ary ,b(r_e,a_t_hi(ng) her ms. The

allantoic c1rculatioii”t en gradua y ec6i:11ss"lsmggisii*a;’iiH”st'bps, and

eventually._by“a process of autotomy the allantois is separated from the body of the embryo and is left behind as the vascular‘ membrane seen lining the fragments of ‘shell from which a young bird has hatched. ‘

ENCLOSURE or YOLK-SAC WITHIN THE EMBRYONIC BoDY.—~—As already indi.cated t1i?yo1k?sae"b“eeo‘nies eventually (about a couple of days before hatching in the case of the common Fowl) _e,ncl_gserl within__thye_”_(_bo‘dy;wal.l. The process by which this is brought about appears to be as follows (H. Virchow). With the growth of the embryo a great increase takes place in the area over which the amnion is fused with the proximal wall of the allantois (cf. Fig. 215A, 0), the compound and highly muscular membrane so formed extending eventually almost completely round the yolk-sac. At its edge it is continued onwards by the somatopleure, this latter terminating round the circular area where the yolk remains exposed. The yolk-sac is thus contained in a space the wall of which is formed of the following components in sequence starting from the body of the embryo : (1) amnion, (2) amnion fused with proximal wall of allantois, (3) proximal wall of allantois and (4) somatopleure in the region of the distal pole of the yolk-sac. The proximal portion of this wall, being formed of amnion, is necessarily continuous with the body-wall of the embryo at the umbilical opening and further those parts of it formed from amnion and allantois are highly muscular and contractile. During the later stages of development this wall slowly contracts and as it does so the yolk-sac is pushed into the umbilical opening which closes after it.

.,_E mQm:mJmAMmQ§mAs regards this question, which has excited much controversy, the following appears to the present writer to be the working hypothesis which ﬁts most easily the facts so far as they are known. .

('1) The amnion originated as a fold (pf blastoderm round the body of the embryo (Fig. 216, A, B).

As has already been shown the amnion arises in this way in gnatggeynypiri the Beptilia which are generally recognized as being the most primitive Amniotes. The same holds for the Birds and for some of the Mammals.

The Mammalia as a group are admittedly descended from ancestors in which the egg was large and meroblastic as it is ‘in the Reptilia. This is indicated, apart from other convincing evidence, by the fact that they still exhibit in ontogeny a well-dey_e_lgpe,,d‘_,thgugh yolkless

t follows then that it is inadmissible to regard facts

derived from the study of certain mammals in which the mode of amnion formation during ontogeny is of a‘ different, even though apparently simpler, type as constituting important evidence in regard to the phylogenetic origin of the amnion, as has been done in particular by (Hubrecht (1895). on. V11‘ ‘EV/OLUTION” OF AMNLION 477

(2) The amniotic fold consisted at ﬁrst of yolk-sac wall, the body of the embryo being forced down into the yolk-sac as it increased in size, possibly by the resistance of the rigid protective shell associated with the assumption of a terrestrial habit.

The tendency towards predominant development of the anterior portion of the amniotic fold may probably be correlated with the predominant growth and ventral llexure of the head end of the body which would cause it to dip down into the yolk-sac particularly markedly.

The delay in the appearance of mesoderm in the region of the proamnion may similarly have been originally due to the pressure of the downwardly ﬂexed head,

(3) The yolk-sac with its richly developed superﬁcial network of blood-vessels was the respiratory organ of the embryo at this early phase in the evolution of the Amniota. It follows that the portion of it nearest the shell, and therefore in the most favourable position for carrying on the breathing function, would tend to increasein area and would therefore bulge more and more over the body of the embryo (amniotic fold, Fig. 216, A, B, gt. f) so as eventually to utilize the whole of the inner surface of the shell.

(4) The egg being new terrestrial the excretory poisons produced by the activity of the already functional renal organs could no longer pass away by diffusion into the surrounding water. It would obviously be disastrous were they to accumulate in the space round the embryo and they therefore had to be retained within the body. This led to the great and precocious enlargement of the receptacle for these excretory poisons, already present in the pre-anmiote ancestor, the allantoic bladder.

(5) This precocious enlargement of the allantois in turn necessitated the early increase in size of the coelomic cavity to accommodate it.

(6) The allantoic wall-—-a part of the gut-wa1l——was naturally vascular, like the rest of the gut-wall, and with its great increase in size it would come in contact with the inner surface of the somatopleure. But as soon as it did this respiratory exchange would take place between its b1ood—-—through the substance of the somatopleure ——and the medium outside. The allantois would thus constitute a new, though at ﬁrst small, breathing organ.

(7) As the embryo grew its respiratory needs would grow also. Meanwhile of its two respiratory organs the one—~-the yolk-sac-— would be shrinking in size and therefore diminishing in efficiency while the other—the allantois———would be increasing in size as it became more and more distended. This would lead to the supplanting of the yolk-sac by the allantois as the main respiratory organ. As the allantois increased in size it would tend to extend in the position of greatest respiratory efliciency, 13.6. close under the somatopleure.

(8) With the development of the allantois and coelome the splanchnopleure would be freed from the somatopleure and the 4'78 llll\lliI'i-1r().I40(iiY OF THE LOWER VERTEBRATES OH.

upgrowth round the body of the embryo-—the amniotic fold- —would now become purely somatopleural (Fig. 216, C).

(9) As soon as the amniotic fold extended so far over the body of the embryo as to roof it in completely it would at once assume a new importance in protecting the delicate body of the embryo, enclosed wi.thin it as in a Water jacket, from the dangerous jars and shocks incidental to a terrestrial existence. In correlation with the importance of this function of the closed amnion we might expect to ﬁnd a tendency for its closure to be accelerated. As a matter of fact i.t will be found that in various mammals, including man, the amniotic cavity is closed from the beginning. ,

——-In many different groups of animals the embryonic phase of development is passed within the oviduct (uterus) of the mother. The advantages of this are obvious, for not only is the young individual sheltered to a great extent from the struggle for existence, as it is even Within an egg-shell, but it forms for the time being as it were part of the body of a complete adult individual with its full equipment for holding its own in the struggle. It is in the group Mammalia amongst Vertebrates that viviparity reaches its highest development, as the ﬁnal touch in their adaptation to a terrestrial existence, but it is of interest to notice that the phenomenon occurs, in a less highly elaborated form, here and ,.~,(,_ 21;_.---,.,-.H..._,__,.m.,“ Ur there amongst the lower Vertebrates-——Fishes, A(?(I../If/H'II..s‘Hi5llClOSl1lg‘ Amphibians, and Reptiles. t‘V"°«‘=’%"- (The ‘mi’ Thus amoncr the Elasmobranch ﬁshcsl there sious of the scale rc- _ ° . .

I_n.emt millimetres.) are numerous genera in which the early stages 1Il development are passed through in the uterus.

In such cases we ﬁnd in the ﬁrst place a well-marked tendency towards the reduction of the protective egg-envelopes which are no longer necessary. Thus there is found, as a rule, during early stages a typical set of egg-envelopes, but the horny shell is very thin and weak as compared with that of oviparous Elasmobranchs and as development goes on (embryo of 7-8 cm. in Acantluias) it becomes still

thinner, breaks up, and disappears.

A curious feature in such cases is the tendency for a group of eggs to be enclosed in a common set of envelopes instead of each egg having its own set. Thus in Acanthvlas (Fig. 217) there are commonly from two to six eggs enclosed in a common shell; in Trygonomvine two or three, in It/uinoliatus seven or eight.

The embryo within the uterus is still nourished primarily by the yolk in its yo1k_-sac. This primitive mode of nourishment has not

1 See Gudger, 1912.

IV. Vrvrmnrrr IN THE LOWER VERTEBRATES.Vin VIVIPARITY IN FISHES 479

yet been replaced by a process of Etbsorpiiloll from the uterine wall as is the ease in the Mammalia. But the uterine wall already plays a part though a minor one in providing food material for the young individual by its glandular activity. The beginnings of this are seen in the albuminous ﬂuid enclosed within the egg-shell, and it is possible that the elongated gill-ﬁlaments of the embryo play a part in absorbing nourishment from this. A further development consists in the secretion of an abundant “uterine milk ” which is drawn into the pharynx through the spiracles by precocionsly occurring movements like those of respiration and passed on into the digestive tract.

In accordance With its glandular activity the lining of the uterus frequently undergoes an increase of area by growing out into villi or trophonemata (Wood -Mason and Alcock, 1891). In the StingRays specially enlarged trophonemata may be drawn into the pharyngeal cavity of the embryo through its greatly dilated spiracles so that their secretion reaches the alimentary canal of the young ﬁsh directly (Fig. 218).

During the later stages of intrauterine development there usually comes about an intimate relationship between the surface of the yolk-sac and that of the uterine lining and in associ.ation with this there is found 3' Varying degree of Fro. 218. -—-Portion of uterus of Pterospecialization Of the uterine llI1- plataca. 7aiz:ru:ra slit open to show an ing (Ercolani, 1879; Widakowich, f"":?"3'r°.‘l":t')“. 1907). This latter may be smooth ,:,,l,p1(Ai1';,.,;|’{, 1g._;9i:)

(Squatina angelus, Notitlomus cine mas), or project into longitudinal folds so as to give increase of surface (Acantlvias oulgamls, .«S'c3/mnus lz'c}m'a), or grow out into papillae or trophonemata (Torjoeolo, Pteroplataea). ﬁnally it may develop folds which interlock with grooves on the surface of the yolk-sac, the uterine and yolk-sac surfaces being iii the most intimate contact so as to constitute physiologically a deﬁnite yolksac placenta (0'cm'chcm3as glcmcus, Mustelus laemls, etc.). _ p

Amongst the Teleostean ﬁshes viviparity occurs occasionally, in at least half-a-dozen different families; the Cyprinodontidae, Seorpaenidae and Embiotocidae furnishing the greatest number of cases. They are particularly numerous amongst the Embiotocidae and Scorpaenidae of the western coast of North America (Eigenmann, 1894). i 480 EMBRYOLOGY OF THE LOWER VERTEBRATES OH.

The eggs are retained in the ovary, either in the follicle, or in the cavity of the ovary; more rarely in the dilated oviduct or uterus. The developing embryo may depend for its nourishment upon the yolk (Scorpaenidae); it may absorb nourislnnent by the surface of the yolk—sae which grows out into villi (Anableps); or the nutritive secretion of the ovarian wall may be taken into the alimentary canal and there digested (Embiotocidae).

Among the Amphibia true viviparity is rare. A well-marked case occurs in Salmnanrlm atm (Wiedersheim, 1890). Here a large number (40-430) of eggs pass into the oviduct when breeding is about to take place but of these all except the one (in rare cases as many as four) next the eloaeal opening Simply break down forming a kind of broth which fills the oviducal cavity. The embryo nourishes itself, after it has used up its own yolk supply, by gulping down and digesting this ﬂuid, which contains not merely the yolky debris of disintegrated eggs, but also large, quantities of red blood corpuseles derived from extensive haemorrhages of the uterine wall.

Perhaps the most striking feature of the Mammalia is the ex't1‘e1ne degree of adaptation which they typically show to an intra-uterine mode of development in which the embryo leads a parasitic existence attached to the uterine lining of the mother. In accordance with this the external ectoderm of the blastocyst becomes modiﬁed to form organs of attachment which eventually, in the region of the yolk-sac and more especially in the region of the allantois, become vascularized and elaborated i11to the complex nutritive and respiratory organs named placentae. This being so, it becomes of much interest to enquire whether amongst those Amniota which are lowest in the scale of evolution——the Reptiles—— there are any foreshadowings of the type of adaptation to intra-ute.rine development found in the Mammalia. Probably numerous such cases exist but at the present time, with our extremely imperfect knowledge of Reptilian development, we are acquainted with only a-few. The most interesting of these is that of the Italian Lizard Ohalcides ttrlidactylus (Seps clmlcides). Giacominfs description of this (1891) may be said to form the foundation of what will one day probably form an important chapter in Vertebrate embryology.

The eggs, which measure about 3 mm. in diameter, are ﬁrst found in the oviducts early in May, while the first young are born towards the end of July, the period of gestation thus being between one and two months.1 The eggs become spaced out along the oviduct or uterus, so as to give it a moniliform appearance, each egg being arranged with its apical pole towards the mesometrium. At about the Iniddle'of gestation the “egg” presents the appearance shown in Fig. 219, A, the whole forming a kind of blastocyst about 7 mm. in diameter. The outer surface is formed by the ectoderm of the serous membrane. Within the serous membrane there can be seen the allantois with transparent, richly vascular, wall and the yolk 1 About sixty-ﬁve days according to Mingazzini. vm EMBRYONIC ADAPTATIONS IN REPTILES 481

szw, more opaque than the allantois and already much smaller than the latter as seen in surface view. The edges of the allantois and the mushroom-shaped yolk-sac ﬁt closely together and between them is the body of the embryo contained in the amnion. As in other Sauropsidans or Prototherian Mammals the yolk-sac lies on the embryo’s left, the allantois upon its right—-upon the side, in this case, next the mesometrium. As development proceeds the exposed area of yolk-sac becomes gradually reduced by the encroachment of the allantois. The latter however remains merely in contact with the edge of the yolk-sac and never comes to "surround it. Over the yolk-sac area there remain visible, for a long time the remains of the vitelline membrane (cf. Bird). Both allantoic and yolk-sac regions of the surface develop placental arrangements, the former being physiologically the more important of the two:

The allantoic placenta is already becoming apparent at the stage shown in Fig. 219, A, in the form of an elliptical area at the mesometrial pole which adheres to the uterine lining by means of numerous little projections which interlock with similar projections on a corresponding uterine area. As de- L up velopment goes on the egg assumes an elongated shape (Fig 219, The whole of FIG. 219.--“ Egg": of ()'[urlcides trzdactylus. the uterine lining in contact (After (‘”“’°"i“"" 1891')

with the outer surface of the A, 7 mm. in diaineter, showing yolk-sac (3/.3), allan “ n - - - . _ - tois (all), and foetal portion of allantoic placenta (pl); ego ls Provlded “nth 3' nch B, 15-16 mm. in longest.-diameter, seen from apical

O

capillary network C1033 pole,slm\\'in;.:I'«n-1:11portionufnllauitoic pla.centa(pI). beneath the uterine epithe lium and here and there insinuating itself between the epithelial cells. Over the allantoic placental area the maternal projections now form undulating ribbons attached along one edge and free along the other. On the surface of these ribbons the uterine epithelium instead of being ﬂattened as it is elsewhere is columnar and has a glandular appearance. With the r.il)ho11-like projections just mentioned there interlock the somewhat similar projections of the foetus. These are also covered with columnar epithelium close under which lies a rich capillary network. The latter is not conﬁned 482 EMBRYOLOGY OF THE LOWER VERTEBRATES OH.

to the actual placental projections for even the smooth parts of the surface over the allantoic area are provided with an extraordinarily rich network of capillaries which show an even more marked tendency than those of the uterus to penetrate into the epithelium. Over the smooth area the foetal and maternal surfaces are in intimate contact, so that the two capillary networks lie parallel and close to one another, separated only by two very thin epithelial membranes. In the region where foetal and maternal projections interlock chinks are apparent between the two in which there appear to be traces of a ﬂuid 1naterial—-—probably nutritive and secreted by the maternal epithelium which as already mentioned has in this region a glandular appearance.

The. yolk-sac placenta is less highly developed. In the region of the centre of the yolk-sac ﬂattened ridge-like projections also appear which interlock with corresponding uterine projections and become vascularized as the mesoderm spreads beneath them. Between the two surfaces is the remnant of vitelline membrane but this gradually disappears so that foetal and maternal surfaces come into intimate contact.

(7/utlcides ((}(m.gg/lus) ocellatus, another Italian lizard, is also

viviparous and in it occur similar though less marked adaptations to viviparity (Griacomini, 1906). Here in the later stages of gestation the general arrangement of the foetal envelopes resembles that in 0’. t9~'o'dwctg/lus. The allantoic region of the foetal surface is smooth and possesses a rich capillary network. It lies in immediate contact with the uterine lining, which in this region is covered with very thin ﬂattened epithelium overlying an extremely rich network of maternal capillaries.

.The portion of uterine lining in relation with the vitelline region of the foetal surface is less richly vascular, is covered with thicker epithelium of vacuolated cells with large nuclei, and is thrown into low folds which interlock with corresponding folds of the foetal surface so as to form an incipient yolk-sac placenta. The foetal epithelium of this region is thickened and in places columnar and appears to have an absorbent function. As in 0. tmldactg/lus remains of membrane are to be seen for a time between the foetal and maternal surfaces in this region.

To sum up, we ﬁnd in Chalcicles ocellatus a less advanced stage of adaptation to intra-uterine development than in C’. tmidactylus. Probably similar conditions will be found in various other viviparous Lizards as e._q. in the Australian Tmcltysaurus and T'il'iz1ua scincoides (0'ycloclus botidccerti) (Haacke, 1885).

In the Blind-worm (Angwis fm_q'il'is) and in the Viper (Vipem) and Smooth snake (C'oronella austrriaqa) viviparity also occurs but here in a still more deﬁnitely incipient form—a thin shell persisting throughout development and the foetal envelopes and uterine lining remaining practically unmodiﬁed.

Thus in the three sets of Reptiles above mentioned we see three steps in the evolution of viviparity: VIII EMBRYONIC ADAPTATIONS IN REPTILES 483

(1) the mere retention of the egg within the uterus, the shell still remaining and no intimate relations being developed between foetal and maternal tissues (Angwis, Vipera, Uoronella),

(2) the rupture at an early stage and eventual disappearance of the shell, and the coming into intimate relations of foetal and maternal tissues, both becoming highly vascular and there being an attempt at the formation of a yolk-sac placenta (C'halc7Ides ocellatus),

and (3) the development of an allantoic placenta (0. tridactylus).

LITERATURE

Agar. Proc. Zool. Soc. Lond., 1909.

Bartlett. Proc. Zool. Soc. Lond., 1896.

Bles. Trans. Roy. Soc. Edin., xli, 1905. ‘

Boulenger. Trans. Zool. Soc. Lond., xii, 1890.

Boulenger. Proc. Zool. Soc. Lond., 1895.

Brandes und Schoenichen. Abhandlungen Naturforscli. Gesell. Hallo, xxii, 1901. Brauer. Zool. Jahrb. (Anat.), xii, 1899.

Braus. SB. kgl. preuss. Akad. Wiss., 1906.

Budgett. Quart. Journ. Micr. Sci., xlii, 1899.

Dandy. Quart. Journ. Micr. Sci., xlii, 1899.

Eigenmann. Bull. U.S. Fish Commission, xii (1892), 1894.

Ercolani. Mem. Ac-cad. Bologna (Sez. Sci. Nat.), x 1879.

Espada, Jimenez de la.. An. Soc. Espafiola do Historia Natural, i, 1872. Giacomini. Monitore zoologico italiano, ii ; and Arch. ital. Biologic, xvi, 1891. Giacomini. Mem. Accad. Bologna (Scz. Sci. Nat.), Ser. 6, iii, 1906. Goeldi. Prov. Zool. Soc. Lond., 1895.

Gudger. Proc. Biol. Soc. Washington, xxv, 1912.

Giinther. Ann. Mag. Nat. Hist. (4), xvii, 1876.

Haacke. Zoo1.Anz. viii,1885.

Hirota. Journ. Coll: Sci. Tokyo, vi, 1894.

Hubrecht. Verh. Akad. Amsterdam, 2de Sect., 1895.

von Ihering. Ann. Mag. Nat. Hist. (5), xvii 1886.

Ikeda. Annot. Zool. Japonenses, i, 1897. ,

Kerr, Graham. Phil. Trans. Roy. Soc., B, cxcii, 1900.

Lebrun. La Cellule, vii, 1891.

Lillie. The Development of the Chick. New York, 1908.

Mitsukuri. Journ. Coll. Sci. Tokyo, iv 1891.

Plate. Vcrh. Deutsch. Zool. Ges., Kiel: 1897.

Schauinsland. Hertwig1sbHa.n(lbuch der Entwicklungslehre, I. Jena, 1906. Siedlecki. Biol, Centra latt, xxix, 1909.

Virchow, H. Inteiinat. Beitragti zur wiss. Medizin, I, 1891.

Weinland. Arch. . Anat. u. ’ iys. 185-1.

Wetzel. Arch. Entw. Mcch., xxvi,,1908.

Widakowich. Zeitschr. wiss. Zool., lxxxviii, 1907.

Wiedersheim. Arch. mikr. Anat., xxxvi, 1890.

Wintrebert. C. R. Soc. Biol. Paris, lxxii, lxxiii, 1912.

Wood-Mason and Alcock. Proc. Roy. Soc. Lond., xlix, 1891. CHAPTER IX

SOME OF THE GENERAL CONSIDERATIONS RELATING TO THE EMBRYOLOGY OF THE VERTEBRATA

IN the course of the preceding chapters many of the general principles of vertebrate embryology will have made themselves apparent: the

present chapter will deal shortly with some others of these principles which seem to require special notice.

(1) THE ONTOGENETIC EVOLUTION or THE ZYGOTE INTO THE COMPLETELY FORMED INDIVIDUAL.—Tl1e Vertebrate commences its individual existence as a zygote— a single ce1l——in which the speciﬁc characteristics, derived from the paternal and maternal ancestors, are already present though not recognizable. That this latter statement is accurate is demonstrated by such a fact as the following. The pelagic fertilized eggs of different species of Teleostean ﬁshes show no trace of the speciﬁc features which characterize the adults. Such distinguishing features as are present and enable a specialist to identify them are mere differences in size, amount of yolk, colour of oil globule and so on, and have nothing to do with adult characteristics. Yet if a selection of such eggs are allowed to develop together under a homogeneous set of environmental conditions each is found gradually to unfold the complete array of characteristics which distinguish its own kind. As the various zygotes have developed under the same identical set of environmental conditions it follows that the differences which gradually become apparent cannot be due to the moulding inﬂuence of external conditions: they must have been already present though in invisible form in the zygote.

It follows further that the evolution of the zygote into the adult is in the main not a process of acquiring greater and greater complexity, in the sense of acquiring new properties, but rather of the loca1iza_tion—the segregation—of special peculiarities in particular portions of the individual, so that these portions assume a, speciﬁc character and become recognizable as deﬁnite tissues or organs. The peculiarities were there to begin with, but they were diffuse and therefore unrecognizable—somewhat in the same way as the various

484 CH. Ix ONTOGENETIC EVOLUTION 485

colours of the spectrum are present in ordinary “ white” light but are invisible until they are sifted out from one another by the action of a prism.

The lesson learned from the developing pelagic zygote——that in its case the full equipment of the complete individual is provided from internal sources——-is one which should ever be borne in mind. It makes it- easier to realize that in other cases, where the developing organism exists in a less homogeneous environment and where it has to fend for itself, characters impressed upon it directly by the environment, however conspicuous, are still superﬁcial as compared with the really fundamental characters already present in the zygote.

The course of ontogenetic development from the zygote stage involves two main processes, (1) increase in bulk accompanied by the assumption of a multicellular condition, and (2) differentiation of parts 73.6. the segregation, into localized portions of the living substance, of peculiarities which were in the zygote distributed without deﬁnite arrangement. The topographical differentiation of the developing embryo does not necessarily keep exact pace with the subdivision into cells. Thus in Amplviomus the egg appears to be still homogeneous throughout up to the time when it has segmented into 8 or even 16 blastomeres for even at this stage a blastomere isolated from its neighbours experimentally may go on for a time pursuing the same course of development as it would have done were it a complete zygote. In other cases, as appears to be the rule in the Frog, the ﬁrst step in segregation—-the segregation of characters belonging to the right and left halves of the body into corresponding hemispheres of the egg—-would appear to take place in the zygote stage 7I.e. before the appearance of the ﬁrst cleavage furrow.

The progressive segregation of speciﬁc characters in the various parts of the developing individual is beautifully brought out in the case of various invertebrates by the elaborate studies on “ Cell lineage,” some of which have been fully described in Vol. I.

The animal individual lives its life under a particular set of environmental conditions, constituted by the external medium—— water or air—with its other living inhabitants: the latter play an important part, it may be by such comparatively simple and direct methods as by affecting the composition of the external medium, it may be by far more complex and obscure inﬂuences due to biological inter-relationships. The individual is able to go on living because of its organization and its living activities being ﬁtted, in the most intimate manner, into the particular set of conditions which constitute its environment.

So also with the various parts of the body—organs, tissues, individual cells —of the young developing individual. Each lives amidst an environment of extreme complexity and of perfectly deﬁnite type of complexity, conditioned by the nature of the body of which it forms a. portion and by the character of the parts of the 486 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

body which are in proximity to it. Its living substance is everywhere bathed by——and no doubt intimately adapted to life in--an internal medium, watery ﬂuid laden with the products of metabolism of the living substance as a whole. The differences in function of the various organs and tissues necessarily involve diﬁ“erences in their metabolic activity and therefore differences in the chemical nature of the contributions which they make to the complexity of the internal medium as Well as differences in the substances which they

. withdraw from the internal medium for their own needs.

Physiologists recognize that changes in the constitution of the internal medium play an important part in exciting and controlling vital activity.‘ In the ordinary life of the animal important examples of such inﬂuence are aiibrded by changes in the activity of the normal function of an organ, as for instance when the pancreas secretes actively in response to the presence in the internal medium of a special substance secreted by the intestinal wall when stimulated by food material. Other examples are afibrded by changes in growthaetivity-—as of the skin in response to a change in the amount of substance secreted by the thyroid, or of the mammary gland in response to the presence of substances produced by the metabolic activity of the foetus.

There is no reason to doubt that the living cells and tissues and organs of the embryo are similarly adapted to and inﬂuenced by the constitution of the internal medium, and if this be so the inﬂuence in question must play an important part i11 development. A possible example is aﬂbrded by the experimental result that ‘the grafting of the developing optic cup of an Amphibian embryo into near proximity to ectodermal tissue (such as the pigment-layer of the retina, the wall of the brain, the olfactory epithelium, the external ectoderm of the head or trunk) is apt to induce that ectoderm to develop into a lens (Bell, 1907). Such inﬂuence upon one portion of embryonic substance by another portion in its neighbourhood may well be exercised through chemical or other changes produced by the specific metabolism of the latter in the internal Inedium in its neighbourhood.

A corollary to the consideration outlined above, which has an important bearing upon much work in experimental embryology, is that it is unwise to place reliance upon the mode of development of an organ-rudiment being normal, unless its environment is normal.

(2) CELLULARIZATION or THE ZYGOTE: CELLULAR CONTINUITY AND DIsCoNTINU1'1‘Y.—-Protoplasm being a soft semi-ﬂuid substance a particle of it, as it increases in volume during the process of growth which is associated with normal metabolism, would soon reach a mechanically unstable condition, in which retention of its characteristic form, or even cohesion, would be impossible. In nature a corrective to this is provided by the protoplasm undergoing ﬁssion. In the Protozoa the products of this ﬁssion normally break apart and

‘ For their bearing upon evolutionary change see Parker (1909). IX ONTOGENETIC EVOLUTION: CELL-DIVISION 487

lead an independent existence, while in the Metazoa the subdivision is less complete and the growing mass of living substance continues to exist as a coherent individual. The physiological advantages of subdivision of the individual body into cellular units is apparent. It renders possible the intercellular deposit of rigid skeletal materials which act as a support to the organism as a whole: it facilitates localization of function and enables blocks of units specialized for particular functions to be transferred d11ring ontogeny to the positions in which they will be most useful: it enables other units to move hither and thither, either by their own activity or by being swept along in a circulating stream of ﬂuid, to wherever they are specially needed in the course of the ordinary vital processes: and it is of enormous importance in relation to attacks upon the organism from without, whether by limiting the area of injury to comparatively small tracts of living substance or by enabling portions of the living substance specialized for defence to be mobilized and ready to concentrate at the point of attack.

Modern science impresses upon us the. importance of regarding the individual not merely as an aggregation of cells and organs, but rather as a mass of living substance imperfectly subdivided up into cells and organs: imperfectly because each cell and each organ is inextricably linked up in the living activity of the whole individual. It brings to our notice numerous tissues in which the actual living substance of the constituent cells is linked up by intercellular bridges of protoplasm: it tells us of particular cases of developing embryos where similar intercellular continuity is apparent. The question is thus raised: are we correct in our belief that actual complete separation of cells takes place as a general rule when they undergo ﬁssion during ontogeny? More especially is it really the case that the individual blastomeres of the segmenting egg become completely separated from one another: is it not rather the case that the apparently complete separation is only apparent, that the individual blastomeres remain continuous through ﬁne protoplasmic bridges: and that cases of intercellular continuity observed in the adult are merely expressions of the fact that such bridges persist throughout the whole period of development ?

That the latter is really the case has been held by various workers and supported particularly strongly by Sedgwick (1895, 1896). It will however have been gathered by the reader from Chapter I. that such a view is in the opinion of the present writer not tenable. The fact that the blastomeres of a segmenting egg tend to take a spherical form, or at least to be bounded by convex surfaces, seems by the ordinary laws of surface tension to indicate that these blastomeres are not continuous with one another. Continuity of substance between the cells of the embryo or adult is therefore when it occurs a secondary and not a primary phenomenon. At the same time the present writer’s observations lead him to agree with Sedgwick that such intercellular 488 EMBRYOLOGY OF THE LOWER VERTEBRATES 011.

continuity ‘of protoplasm is much more widely spread than is generally recognized.

(3) YOLK. —- Theoretically the most primitive type of zygote should from the beginning be able to absorb food for itself. As an actual fact however the zygote is provisioned for a shorter or longer period by the highly nutritious fat and proteid, in the form of yolk which is stored up in its cytoplasm.‘ With increasing specialization the amount of this store becomes greater and greater so as to lengthen the period during which the young individual is provisioned and freed from the necessity of working for its own living. A good example of a high degree of such specialization amongst Vertebrates is afforded by the relatively huge egg of the Ostrich.

It has of course to be borne in mind that the degree of specialization in this direction is to be estimated not merely by the absolute amount of yolk present but still more by the relative amount of yolk in proportion to protoplasm. Thus two eggs may be described as equally richly yolked although very different in size provided that the proportion of yolk to protoplasm is similar in the two cases. In correlation with this we find that a group characterized by heavily yolked eggs may evolve in the direction of producing more and more numerous, and therefore necessarily smaller, eggs. Good examples of this are seen in the Teleostean ﬁshes where the eggs may be produced in enormous numbers and of very minute size although still retaining a proportionately large supply of yolk.

In C. Rabl’s discussions of his “ Theory of the Mesoderm ” (1889) an important place is taken by repeated losses and re-acquisitions of yolk during the phylogeny of the Vertebrata. Rabl arranges Cyclostomes, Elasmobranchs, Ganoids, Amphibians, meroblastic “ Prota1nniota” and Mammals, in a linear series, and concludes that Ganoids and Amphibians have undergone a diminution of yolk and have therefore reverted to the holoblastic condition; that meroblastic Protamniota have re-acquired a large amount of yolk and have therefore reverted to the meroblastic condition; and that ﬁnally Mammals have lost their yolk and again become holoblastic. In the opinion of the writer there is no suﬁicient justification for any one of these assumptions except the last. There is, as is well known, definite evidence to show that Mammals are descended from ancestors with large and heavily yolked eggs and that the small size and practically yolkless character of their holoblastic eggs are secondary acquirements. In this case the loss of yolk has brought in its train profound changes in the early processes of development but of such there are no signs in those other cases in which llabl supposes loss of yolk to have taken place. It must also be remembered that in the Mammal there is an obvious physiological reason for the loss of yolk——namely that the food material needed during the development of the embryo is provided from the tissues of the mother.

1 For a detailed account of the development of the yolk in the egg of one of the lower Vertebrates (Proteus) see J orgensen (1910). Ix YOLK 489

On the recapitulation hypothesis the segmentation and other early stages of ontogeny represent ancestral evolutionary stages common to all Vertebrates. The differences to be observed between such stages in different members of the group are consequently not to be looked on as ancestral but rather as due to the inﬂuence of disturbing secondary factors. Of these by far the most important is the presence of the particles of yolk, this dead substance clogging and retarding the living activity of the egg protoplasm. 'l‘he extent to which it does this in any particular region of the egg is roughly proportional to its relative amount as compared with the living protoplasm in that portion of the egg. The yolk is as a rule of higher speciﬁc gravity than the protoplasm. Correlated with this it

tends to be in proportionally greater amount in the lower parts of’

the egg than in the apical part, with the result that the processes of cell division and of development generally are relatively more slowed down in these lower portions———in extreme cases brought to a full stop——-by its retarding inﬂuence. Typical examples of this are seen in the holoblastic but unequally segmenting eggs of the ordinary Amphibia. In this case it is possible by replacing experimenta‘lly the action of gravity by a more potent force (by centrifugalizing the eggs) to concentrate the yolk still more than is natural iii the lower hemi_sphere with the result that the egg is now converted into a meroblastic one (0. Hertwig) the lower hemisphere being unable to segment. On the other hand by inverting the egg and so allowing the yolk granules to settle down towards the apical pole under the inﬂuence of gravity it is possible to cause the segmentation furrows to start from the abapical pole and spread towards the apical.

The influence of yolk upon the gastrulation process will have been realized from the perusal of Chapter II.: it is well illustrated by the series Amplmlowus (Fig. 18), Petromg/zon (Fig. 23), Rama (Fig. 25), Lepirlosiren (Fig. 21), II;/pogeoplzxis (Fig. 27) and Torpedo (Fig. 28). Put in a single sentence it may be said to consist above all in the gradual subordination of the process of invagination to those of overgrowth and delamination. In the succeeding stage it makes itself apparent more particularly in the modiﬁcation of the mode of origin of the mesoderm, the outgrowth of hollow enterocoelie pouches being replaced by the delamination of a solid mass or sheet.

The storage of yolk carries with it not merely the modiﬁcations just indicated in the processes of segmentation and_ gastrulation. Its inﬂuence becomes retrospective and affects even preceding stages during the growth of the intra-ovarian egg. This is shown more especially by the precocious concentration of yolk in that portion of the egg which will later become endodermal. Thus is the telolecithal condition brought about and telolecithality itself is seen to be really a foreshadowing of a particular adaptive feature of later stages of development (p. 183).

In examining sections of later stages of Vertebrate embryos in 490 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

which the eggs are rich in yolk it is readily seen that there are conspicuous differences between different parts of the e1nbryo’s tissues in regard to the yolk contained in their cells, for example endodermal structures are frequently marked out by larger yolk granules which cause them to stain more deeply with yolk-staining dyes. The condition of the yolk in a tissue may indeed give a useful hint as to the cell layer to which it belongs and as a matter of fact evidence of this kind has played a conspicuous part in many embryological discussions. '

It is important to bear in mind however the physiological signiﬁcance of the character in question. It appears to be closely related to the metabolic processes in the tissue concerned. As a given tissue in a yolky embryo goes on with its growth and development its yolk is gradually used up, a necessary preliminary being its breaking down into ﬁne particles easily assimilable. Tissues or cells undergoing active growth and multiplication have their yolk in this ﬁne-grained condition: those which are for the time being comparatively inert retain their yolk in a coarse-grained for“m. Thus a disturbing factor is introduced which has to be carefully borne in mind when using the character of the yolk as a criterion of the morphological nature of a given cell or tissue. '

A still further disturbing factor lies in the fact that while yolk is being used up and disappearing from view in one part of the body it may be deposited in cells elsewhere-—as for example takes place in eggs during their period of growth within the ovary. Such increase in the amount of yolk however, accompanied commonly by increase in the size of the individual granules, is naturally relatively rare in comparison with the breaking down of yolk which is occurring through the general tissues of the embryo. It follows that on the whole coarsely granular yolk in a cell or tissue affords more reliable evidence as to its nature than does ﬁne-grained yolk———which may be and usually is merely a symptom of active metabolism.

(4) RECAPITULATION.——'l‘he fascination as well as the philosophical interest of the study of Vertebrate embryology rests in great part upon the recapitulation of phylogenetic evolution during the development of the individual. In the early days of evolutionary embryology this idea was accepted in an unquestioning and uncritical spirit and it was supposed that all that had to be done to obtain a11 accurate‘ and fairly complete picture of the phylogenetic history of any particular animal was simply to work out its ontogenetic development. The more extensive knowledge which we have regarding embryological phenomena to-day serves on the one hand to conﬁrm fully the truth of the general principle and on the other hand to indicate how its working is interfered with by various disturbing factors.

The main controlling factor in ontogeny is the character of the adult. This is the motive power throughout the developmental period. Just as according to N ewton’s First Law a moving body tends to continue in Ia state of uniform motion in a straight line, so in Ix YOLK : RECAPITULATION 491

ontogeny the developing individual tends to progress constantly towards the goal of adult structure. Not in this case however necessarily by the straightest and shortest path. The structure of the adult is the expression of the action of Heredity. The earlier stages are not exempt from the same inﬂuence. Each step in the development of the ancestor tends to be repeated in the development of the descendant. The descendant then during its ontogeny tends to pursue the same, it may be devious, path as the ancestor. If in the course of generations the adult structure becomes shifted onwards in a process of evolution, this merely means the adding on of a new portion at the latter end of the ontogenetic path. The earlier portions of this path, built up of similar increments representing previous steps in evolutionary progress, are repeated as before, and so the complete process of individual development forms a record or recapitulation of phylogenetic history.

It cannot be too constantly borne in mind that the factor just indicated is the supreme factor in ontogenetic development. Other factors may be superﬁcially conspicuous, may have far-reaching inﬂuence upon details, but this factor—-the tendency to repeat ancestral steps in development up to and including the final characters "of the adult—is and must always be paramount.

Modern advances in knowledge of the facts of embryology, together with the assumption of a properly critical frame of mind, have shown, however, that the picture of past evolution afforded by the phenomena of individual development is at the best but a blurred and imperfect one, and that this must necessarily be so is readily realized when we remember that a large proportion of the characters of any organism are adaptive to its special mode of life. The circumstances under which a developing organism exists are, as a rule, widely different from those under which its ancestors proceeded along the evolutionary path, and in correlation with this its adaptive features are equally distinct. As we study the development of any species of animal we do not then see before us a complete and perfect picture of its evolutionary history, but merely gain ﬂeeting, and it may be misleading, glimpses through the obscuring_ clouds of adaptive features.

A further disturbing factor is indicated by the consideration that in past evolutionary history each stage in evolution was represented by a complete functional organism, all the parts of which were necessarily at correlated stages of development so as to form a functional whole. Many modern animals however develop under conditions in which the different systems of organs are no longer forced to keep accurate step with one another, and the result is that some lag behind while others, particularly organs of great histological complexity in the adu1t——-such as the brain or the eye——are accelerated in their early development, so as to give time for the complicated histogenetic processes that have to be completed before the organ can become functional. It will be realized that this latter type of 492 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

disturbance affects the development of the individual as a whole much more than it does its component organs, the result being that embryology frequently affords a much more perfect picture of the evolution of single organs than it does of the organism as a whole.

In reference to the ontogenetic record of phylogeny an interesting question presents itself regarding the reliability or otherwise of the information derived from the study of larval forms. To what extent may a particular type of larva be taken as probably representing a corresponding phase in the evolutionary history of the group: to what extent are its features to be regarded as ancestral, to what extent as mere modern adaptations to the environmental conditions among which the particular creature now pursues its individual development? In connexion with various groups among the Invertebrata larval forms have played a conspicuous part in phylogenetic speculation-—in some cases without due discrimination in interpreting their features as ancestral—the climax perhaps being reached by the view which regards such pelagic larvae as trochospheres or naup1ii——precocious1y developed and free-swimming heads without any trunk-—as representing ancestral forms (of. Graham Kerr, 1911).

In considering whether a particular stage of development is to be taken as probably repeating an ancestral stage of the adult special attention should be directed towards its mode of life, with the object of estimating the degree to which it diverges from the probable mode of life of the ancestral stage. If its mode of life is strikingly aberrant, ag. parasitic where the normal habit of the group is free-living, or pelagic where the normal habit is not pelagic, then we must always keep in mind the possibility or probability that its most conspicuous features are mere modern adaptations and are therefore worthless as evidence of ancestral conditions.

Again it should be considered whether in the main features of its organization it agrees with animals which are admittedly allied to it.

Larvae occur in the following Vertel;rates———Amp7z/ioasus, Petromg/zon, Crossopterygians, Ganoids, many Tcleosts, Lung-ﬁshes and the majority of Amphibians. Applying such criteria as are indicated above we should rule out as probably devoid of phylogenetic signiﬁcance the larva of A7nph'i0;L'u.s’ on account of its quite aberrant “pleuronectid” asymmetry (see Vol. I. Chap. XVII.). We should again rule out the Teleostean larvae on account of their extreme diversity. In Urodele Amphibians and Dipneumonic Lung-ﬁshes on the other hand we see larvae which appear to be distinctly of a common type. And in Crossopterygian and Actinopterygian Ganoids we again ﬁnd larvae which differ from these in detail rather than in fundamental characteristics. Consequently we should incline towards the view that the type of larva in question does not depart very

widely from the common ancestral type out of which existing Vertebrates have evolved. ' IX RECAPIT ULATION 493

Again in considering whether a particular feature of structure is to be regarded as ancestral or as a modern adaptation the following questions should be asked: (1) Is the feature peculiar to one group of Vertebrates or does it occur in several groups, and (2) if it occurs in several groups do the various animals possessing the peculiarity in question undergo their larval stages in similar sets of environmental conditions?

If the particular feature occurs in several groups derived from a common ancestral form this obviously increases the probability of the feature itself being ancestral. If however the several groups show similar sets of environmental conditions during their larval stages this introduces the element of doubt whether the similar features may not after all be merely adaptations to these similar sets of conditions.

Again it is important to make out whether the particular similarity has to do merely with parts of structure in direct functional relationship to external conditions. If there be deep-seated correspondences in structure with no such direct functional relationship to external factors then this gives greatly increased probability to these correspondences being truly ancestral in their nature.

The morphologist in trying to decipher the record of evolutionary history from the data of comparative anatomy or embryology is constantly impressed by the potency of nature’s economy of living substance. An organ no longer required may be eliminated within a very short period of evolutionary time. Thus in some species of Mackerel (Scombe7') so important an organ as the air-bladder has been eliminated: in various Frogs and Toads the external gills have been eliminated from development. Thus negative embryological evidence is of peculiarly little weight in relation to phylogenetic problems.

(5) THE PROTOSTOMA HYPOTHESIS.——Tl1iS is a working hypothesis which links together and in a sense explains a number of features in the early development of Vertebrates which are otherwise extremely puzzling. The more important of these features may be summarized as follows:

In Amplmloruus as has already been shown the dorsal side is at ﬁrst occupied by the widely open gastrular mouth. Later this becomes roofed in by a backgrowth of the gastrular rim anteriorly. A similar process of backgrowth appears to take place in the gastrulation of lower Vertebrates in general. The roof of the gastrular cavity formed by this process gives rise later not merely to the dorsal wall of the alimentary canal but also to notochord and central nervous system.

I. N ow occasionally there are appearances which suggest that this archenteric roof consists really of two lateral halves which have become fused together along the sagittal plane. Thus in Protopterus the down-growing dorsal lip of the blastopore is frequently indented by a median incision. Again in Urodeles the medullary plate is 494 , EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

frequently traversed by a ﬁne superﬁcial groove wh.ich passes forwards along the median line.

II. Then there occur curious cases of abnormality in which the dorsal region of the body is actually divided into two halves by a longitudinal split in the mesial plane. Thus Oscar Hertwig found

FIG. 220. -—Ahnorxnal embryos illustrating the Protostoma theory.

A, abnormal Frog embryo seen from the dorsal side; B, transverse section through hinder third of ditto (after 0. Hertwig, 1892); C, abnorma.1'I‘ront embryo (S. famio) in dorsal view (after Kopsch, 1899); D, ahnorxnal embryo of Pike (Esox lucius) (after Lereboullet, 1863). m. f, medullary fold ; m.s, mesoderm segment; mes, mesoderm; N, notochord; 0, opening leading down into enteron; ot, otocyst; 3/,'_1nass of yolk-cells.

(1892) that by fertilizing frog’s eggs which had become over-ripe, either by retention within the oviduct or by being kept for from one to four days in a moist chamber, he obtained a certain number of abnormal embryos of the type shown in Fig. 220, A, where a large expanse of yo1k—cells is visible in dorsal View instead of being completely covered in as would be the case normally. In transverse section (Fig. 220, B) such an embryo was found to have two half IX PROTOSTOMA THEORY 495

neural rudiments and two notochords of half the usual size, widely separated by the mass of yolk or endoderm.

Similar abnormalities have been observed in Teleostean ﬁshes. E.g. Fig. 220, D shows a Pike-embryo which is normal towards its anterior and posterior ends but interrupted for some distance in the mid-dorsal line by a Wide cleft in which the yolk is visible. Again in Fig. 220, C a similar cleft" is seen to traverse the whole length of a Trout-embryo from the hind-brain region tailwards.

An important feature of such abnormal embryos of ﬁsh and amphibians is that they frequently proceed with their development, the lips of the ﬁssure closing up and the two sets of half-organs being brought together in the mesial plane, undergoing complete fusion and the individual becoming in fact entirely normal. The importance of this return to the normal on the part of such split embryos is that it indicates that the departure from the normal during the split condition is far less fundamental than would appear at ﬁrst sight.

Here then we have to do with two very remarkable phenomena. Firstly there is the abnormality itself—-—the fact that the dorsal region of the body is for a time in the form of two distinct halves. Abnormalities of such a definite type as this usually have a deﬁnite evolutionary or other meaning and it is necessary to search for such a meaning in this particular case. Secondly, there is the fact that an embryo almost completely bisected in this way is frequently able to right itself and become perfectly normal. This again suggests the question whether this power of righting itself has not some special

- evolutionary meaning.

III. In the higher meroblastic Vertebrates we have seen that there exists along the middle line of what corresponds with the archcnteric roof of Avnplzxioccus (’i.8. the region which becomes converted into the dorsal part of the body, including notochord and medullary plate) the structure known as the primitive streak. We have also seen that in the lowest Vertebrates possessing it, this primitive streak represents the line of fusion of the gastrular lips, and that we are therefore justified in attaching the same signiﬁcance to the primitive streak in those higher forms in which the actual process of fusion can no longer be observed. That this interpretation is correct is indicated by the occasional occurrence of openings in the line of the primitive streak communicating ventrally with the enteron and dorsally with the outer surface of the medullary plate, or its derivative the ﬂoor of the neural tube (pp. 51, 53). Such neurenteric communications are readily explicable by the view that they represent simply parts of the line of fusion of the gastrular lips where the actual fusion has not been completed. Here again we have a phenomenon which demands explanation-——the occurrence of what seems to be the vestige of a slit-like gastrular mouth along the middorsal line.

IV. We have another remarkable body of facts associated with the fate of the blastopore or remnant of the gastrular mouth in 496 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

various groups of the animal kingdom; Thus within the limits of the groups Annelida or Mollusca the blastopore in some forms becomes the mouth, in others the anus. N 0 one would doubt for a moment that the mouth opening is homologous throughout these groups yet in one member of the group it can be traced back to the blastopore while in another member it is the anus which can be so traced. In other forms the gastrular mouth simply vanishes away during development and in some of these cases it assumes a curious elongated slit-like form along the mid-neural line before it disappears.

It is the merit of the Protostoma theory that it—and it alone—— affords an explanation of these four very different but equally puzzling bodies of facts. It falls therefore to be accepted by the Vertebrate embryologist as one of his working hypotheses.

The Protostoma theory is simply a special development of the theory of the evolution of the coelomate Metazoa which is generally accepted by morphologists, namely that the animals in question have passed, during the remoter parts of their evolutionary history, through a Protozoan and later a Coelenterate stage. The peculiarity of the Protostoma theoryis that it includes

"FIG. 221.-—~View of neural rudiment in embryo of within the coelenterate period

{;6’i'lZ}1(ltllu$’  Sedgwiclp,  ; '8.Il(l.  a Stage correspondillg in

Cpl, 081/F871;. I1 1e Case 0 epz. osrren le - - embryo is shown as it appears when straight- maln Structural matures Wlth

ened out. the Actinians of the present

time, characterized by the

presence of an elongated slit-like mouth, dilated somewhat at each

end and surrounded by a specially concentrated portion of the ecto dermal nerve plexus. The portion of the surface on which the slit-like mouth was situated was thus the neural surface.

Sedgwick (1884) was led to the idea by his studies on the development of Peripatus. He found in the species investigated by him a stage (see Fig. 221, A) in which the gastrula-mouth formed a long slit traversing the neural surface and surrounded by the ectodermal neural rudiment. As development went on the gastrular mouth or protostoma became obliterated, except in its dilated terminal portions, by fusion of its lips. The terminal parts remained open as mouth and anus respectively. The portions of nerve rudiment between the two openings became the ventral nerve cords while the portions in front of the mouth and behind the anus gave rise respectively to the IX _ PROTOSTOMA THEORY 497

supra-oesophageal ganglia and the suprareetal commissure. According to Sedgwick this stage in the development of Pervlpatus repeats the features of an Actinozoon-like Coelenterate ancestor, not merely of Pemlpatus, and therefore of Arthropods in general, but of such other groups as Annelids, Molluscs and Vertebrates.

It will be noted that on this protostoma hypothesis an important physiological distinction has at an early period of evolution marked off the Vertebrates from the other groups mentioned. This distinction came about with the acquisition of different habits of movement. In the stem which gave rise to Annelids, Arthropods, Molluscs, movement took place with the neural surface next the substratum (as in those modern Medusae which are able to creep on a solid surface-—e.g. Cladonerna), while in the Vertebrate stem on the other hand the neural surface was directed away from the solid substratum (as in the modern Actinian when it creeps). This difference in the position of the body in relation to the substratum would naturally lead in time to the different types of dorsiventrality so apparent in the fundamental organization of the two diverging stems. It is frequently stated by critics of the protostoma hypothesis that it involves a reversal of dorsal and ventral sides during the evolution of Vertebrates from their invertebrate ancestors but it will be gathered from what has been said that this criticism rests on a misunderstanding.

It will be readily seen that the protostoma hypothesis successfully explains the four categories of puzzling facts already enumerated. The paired appearance of the gastrular roof would be a reminiscence of the fact that originally it was actually paired: the split along the back of the abnormal embryos would mean the temporary re-appearance of the ancestral split or mouth: the primitive streak would be the scar along which the lips of this ancestral mouth or protostoma underwent fusion: and the converting of blastopore now into mouth now into anus would he an imperfect reminiscence of the fact that in phylogeny it gave rise to both.

On this hypothesis the various signs of a split along the neural surface of the vertebrate embryo, whether in the form of a dorsal furrow or a primitive streak or an actual opening, areinterpretable as reminiscences of the protostoma slit which traversed the neural surface of the Actinozoon-like ancestor.‘ It is of interest to notice that in two Vertebrates at least there exist what seem to be obvious traces of neural rudiment extending round behind the anal part of the protostoma precisely as in Peripatus. In Fig. 221, B, is shown an embryo of Lepidosiren spread out in one plane, with the neural rudiment in the form of a ridge which is continuous behind the blastopore or anus. If it be reﬂected that this opening may be

1 That the primitive streak and primitive groove are closely related to the gastrula mouth was perceived by Rauber (1877) but a. clear evolutionar explanation of this relationship was ﬁrst given by the protostoma theory of Sedgu 1c (1884) and Hertwig (1892)

VOL. 11 2 K 498 EMBRYOLOGY OF THE LOWER VERTEBRATES en.

regarded as being continued forwards by a potential slit, represented eg. by the primitive streak of other forms, it will be realized how close is the resemblance to the conditions in Peripwtus. The pre-anal portions of the neural rudiment in Lepidosiren come together in the mesial plane to form the spinal cord, while the postanal portion ﬂattens out and disappears so that theanal opening comes to lie entirely behind the posterior limit of the central nervous system. It is clear that if the development of the anal opening were delayed until the neural folds had already come together it would make its appearance completely behind the central nervous rudiment and with no obvious connexion with it. This is very possibly the case in Vertebrates other than those mentioned. '

Although the anal opening of Vertebrates is thus brought into the relations with the nervous system that we should expect on the protostoma hypothesis there is no such deﬁnite evidence in the case of the mouth. It is true that in some cases the dorsal furrow has been traced to the neighbourhood of the mouth and that the mouth opening has in some cases at first the form of a sagittally placed slit, but in no ease, up to the present, has the neural rudiment been traced round in front of the mouth. This difficulty however is greatly lessened when We correlate the facts just mentioned in regard to the anal opening in Lepidcisiren with the relatively late appearance of the mouth opening of Vertebrates as discussed on p. 193. It may well be that the non-inclusion of the mouth opening within the obvious neural rudiment is due simply to the pre-oral parts of the medullary folds having already ﬂattened out and disappeared before the oral opening makes its appearance. If this is the case it carries with it the interesting consequence that the supra-oesophageal or pre-oral ganglia of I’emIpatus have disappeared in the Vertebrate and it is therefore waste of energy to discuss what parts of the brain of a Vertebrate are homologous with the supraoesophageal ganglia of Invertebrates.

This Protostoma idea, dealing as it does with extremely remote phases of the Vertebrate phylogeny, must not be looked on as a deﬁnitely proved theory, nor can it be expected ever to reach that dignity, but it is a fascinating working hypothesis which serves, and which alone serves, to link together and in a sense explain a considerable body of otherwise mysterious and apparently inexplicable facts of Vertebrate embryology.‘

(6) THE VERTEBRATE HEAD.-—-The two phyla of the animal kingdom which have reached the highest stage of evolutionary deve1opment—the Arthropoda and the Vertebrata——are alike characterized by the possession of a well-developed head. In the

1 In considering the diﬂiculties in the way of the theory afforded by cases where the gastrula becomes roofed in by a process of simple backgrowth without any trace

of protostoma. (e.g. Amphiomus), it is well to bear in mind the parallel case of the

amnion-——of which a large portion may be formed by simple backgrowtb, although the sero-amniotic isthmus and the ingrowth of mesoderm from the two sides seem to point clearly to a former formation by the meeting of two lateral folds. IX THE VERTEBRATE HEAD 499

evolution of a head we may take it that the principal factors involved are probably the following:

(1) The habit of active movement in a direction corresponding with the prolongation of the axis of the body,

(2) The concentration of organs of special sense towards the end of the body which is in front during movement,

(3) The concentration of nerve centres to form a brain in proximity to these organs of sense.

In the case of the Vertebrate the brain has reached a comparatively large size and in correlation with this the protecting skeleton has become highly developed and has lost the ﬂexibility which is characteristic of it in the trunk. Further in the Vertebrate the walls of the buccal cavity and pharynx have become highly

specialized, particularly in the matter of their skeleton, in relation‘

to the functions of ingestion and mastication of the food on the one hand, and of respiration on the other.

Each of these various factors involves structural change, not affecting merely one organ but causing modiﬁcation of the whole complex arrangements of the head-region. Thus associated with the loss of ﬂexibility we ﬁnd (1) loss of segmentation of the skeleton, (2) disappearance or great modiﬁcation of the myotomes, (3) corresponding changes in the nerves supplying these myotomes and (4) disappearance of the coelomic cavities.

The full appreciation of the importance of this feature of the Vertebrata makes it, in the present writer's opinion, impossible to doubt that the possession of a deﬁnite head is a feature that has come down from the unknown ancestral form from which the Vertebrate stock has evolved. If this be correct it follows that the relatively feeble differentiation of the head end of the body seen in Amplmioams is to be regarded as a secondary condition, correlated with the peculiar mode of life of this animal, and devoid of phylogenetic signiﬁcance.

It has already been pointed out that organs of great complexity in the adult tend to be laid down at an early stage of individual development, time being thus obtained for the development of their complex detail. It is perhaps in direct relation to this principle that the highly complex head - region of the Vertebrate, which comes to assume control over most of the activities of the individual, develops particularly early in ontogeny ——the Various developmental processes making themselves as a rule ﬁrst apparent in the head region and spreading thence tailwards along the trunk. This fact is of practical importance to the embryologist for in the case of segmentally repeated organs it enables him to ﬁnd a series of developmental stages within the body of a single embryo.

Though this precocious cephalization is a marked feature of

Vertebrate ontogeny it never goes within this phylum to the length it does amongst certain Invertebrates where the larval stage 500 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

(N auplius, Trochosphere) is practically a precociously developed and free-living head which has not yet developed a trunk.

As will have been gathered, one of the most conspicuous features of the head-region is the loss of segmentation in organs in which it was once present.

Metamerie segmentation, which ﬁrst makes its appearance in typical form in the Annelida, is probably to be associated primarily with the coelome and its lining the mesoderm. The coelome is distended with coelomic ﬂuid and the turgidity so caused gives ﬁrmness to the body. The physiological advantage of the coelomic cavity being subdivided into successive compartments is obvious. The segmentation of other organs is to be looked on as secondary to that of the mesoderm, and more especially to that of the muscles. Thus the segmented character of the nervous system of an Annelid or Arthropod is due to the ganglion-cells tending to become concentrated at the level of the masses of muscle which work the parapodia or limbs. So also the segmentation of the skeleton which permits flexure of the body is correlated directly with the segmentation of the musculature which causes that ﬁexure.

So, conversely, with the disappearance of segmentation in the head of the Vertebrate. Correlated with the loss of ﬂexibility in the brain region the myotomes which produce the flexure have disappeared, and correlated with this in turn the ensheathing skeleton has lost its segmentation and the segmentally arranged motor nerves have also gone. The process has taken place from before backwards. It has been carried to the greatest extent in front, to the least at the hinder limit of the head.

It is deﬁnitely established that the head of the Vertebrate has at least in part come into being by the modiﬁcation of what was once the anterior portion of the trunk. With the gradual evolution and increase in size of the brain—-so characteristic of the phylum Vertebrata—this organ has gradually encroached upon the spinal cord, and its protective skeleton the chondrocranium has pare} passu encroached upon the vertebral column. This is clearly indicated by the fact that included within the limits of the skull are nerves which are serially homologous with those of the trunk. Putting on one side the probability-as many would regard it— that cranial nerves III, IV, V, VI, VII, IX and X are really homologous with the spinal nerves, we ﬁnd behind the Vagus a series of spino-occipital nerves (Fiirbringer, 1897), which although included within the limits of the skull are yet undoubtedly members of the same series as the spinal nerves. The number of those is very different in the different subdivisions of the Vertebrata as may be gathered from aninspection of Fig. 222. In all probability they will be found also to show considerable variation in different individuals of the same species.

During the evolution of the head there is some reason to believe adult stage of modern Cyclostomes: it is also seen in the young Lepidosiren of stage 34 (see Fig. 154, B, p. 309).

The next phase is seen in the adults of such relatively primitive groups as the Elasmobranchs, the dipneumonic Lungﬁshes and the Amphibians, in which an occipital region has been added on to the palaeocranium.

ii jjj =...‘!....'I.2_IL_A_Il_'«’..1L._$_1L_1.JL_§_iL_9._JL_7_|i_!3_i

L_V_l|_w_lIJ.JLL1L_zJI_A_JLB_JL_Q_1L_D_JL_E_JL_F.JL_LJL_8_J

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O jjjj |v3 |Z||A| |Bg|g||4| .5. 113.17. [8]

FIG. 222.-—-Diagram illustrating the relations of the binder limit of the cranium in an Elasmobranch (A), Lepidosiren (B), Polypterus (C), Acipenser (D), an Amphibian (E), and a Reptile (F), as seen from the left side.

The cranial floor is indicated by the broad horizontal black band : it is demarcated from the vertebral column by the vertical band which represents the occipital limit of the cranium. Dorsal and ventral nerve roots are shown as black dots, when transitory as rings, when occurring only occasionally as dotted rings. The myotomes are indicated by rectangular outlines. The Spinooccipital myotomes are lettered according to Furbringer's system—the anterior batch (occipital) with the concluding letters_of the alphabet, the posterior batch (occipito-spinal) with the commencing letters (A, B, C’). Trunk myotomes not yet incorporated in the head are designated by numbers.

Ix THE VERTEBRATE HEAD 501 that its extension backwards has taken place by successive steps. In the most ancient recognizable stage the cranium (Palaeocranium ——Fiirbringer) extended no farther back than the vagus nerve. This phase is represented--either persistent or revertive——in the 502 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

Finally the hinder limit in the other Vertebrates has been shifted still farther back—one segment (Poly/ptems), three segments (Amniota) or as many as ﬁve segments (Acipenser).

As far forwards as the hinder limit of the palaeocranium there is, as already indicated (p. 317), clear evidence that the cranial wall represents a series of neural arches which have undergone fusion. As indicated on the same page it is difficult to avoid extending this homology to the mesotic portion of cranial wall lying still farther forwards. As regards the prechordal portion of the cranium there is no deﬁnite evidence, but if we regard the trabeculae as primitively in continuity with the parachordals we have to grant the possibility of even this part of the cranium being in series with

' the portions farther back and therefore also originally vertebral in

constitution.

In conclusion it must be remembered that the series of myotomes is also continued into the head-region, and the occurrence of typical myotomes as far forwards as the premandibular or oculomotor segment (p. 210) may be taken as strong evidence that the segmentation of the mesoderm originally extended throughout the head-region including its pre-chordal portion.

(7) EMBRYOLOGY AND THE EVOLUTION or THE VERTEBRATE.—— The special charm and the chief importance of the study of embryology reside in the fact that it is one of the main branches of evolutionary science. The greater part of what is ordinarily called evolutionary research deals with the possible methods and causes of evolutionary change. '.l‘he data of Embryology on the other hand form a branch of synthetic evolutionary science which deals not with possible causes or methods but with the actual facts of evolutionary change, striving to map out the course along which this has proceeded. ln compiling the record of evolutionary progress we are dependent upon Comparative Anatomy and Palaeontology as well as Embryology, and in formulating conclusions care has to be taken that whenever possible they are based on the data of all three sciences. In cases where these data are not in agreement care must be taken to bear in mind the main disturbing factors which are liable to invalidate the conclusions in each case. In reasoning from Embryology and Comparative Anatomy the possibility that particular features are modern adaptations to existence say within a uterus or egg-shell or under any other set of conditions different from those of the ancestor has to be borne in mind. In the case of Palaeontology and Comparative Anatomy there exists the same danger of error as besets the protozoologist when he endeavours to construct a continuous life-history out of a number of isolated observations on the dead animal—the error of arranging observations in a series which is not natural, or on the other hand, if the seriation be done correctly, of reversing its direction. In Palaeontology errors of this type are peculiarly apt to arise on account of the extraordinary imperfection of our knowledge. If a- series of organisms a, b, c, d, IX EMBRYOLOGY AND EVOLUTION 503

become known from a series of geological deposits A, B, 0, D, this affords convincing evidence in most cases that the particular organisms lived at the time the particular deposits were laid down: the conclusion may also be fairly justifiable that not only did they exist but that they were abundant at the period in question. The conclusion however which is so apt to be drawn that w, b, c, d, actually made their ﬁrst appearance in the same order as the deposits A, B, 0, 1), is quite unreliable. They may have existed in smaller numbers for immense periods of time before the periods corresponding to A, B, 0’, 1), when they were really abundant, and the order of their ﬁrst appearance may have been d, c, b, a, or any other. Such a geological series is in fact in itself of little value as an index to the order of evolution. In Embryology on the other hand where the evolutionary stages occur as part of a continuous process, each dependent upon its predecessor, we appear to be safe in assuming that the record, however incomplete, is at least arranged in proper sequence.

Another principle to be borne in mind, when the attempt is being made to work out the evolutionary history of a particular group‘ is that conclusions must be based upon broad knowledge of structure as a whole. No implicit reliance must be placed upon evidence relating to one system of organs unless it is corroborated by the evidence of other organs. Failing this precaution the investigator is liable to the pitfall afforded by convergent evolution of organs of similar function. Here again the palaeontologist ﬁnds himself much hampered as compared with the embryologist, for as a rule all evidence except that of the skeletal system has passed completely beyond his ken.

EVOLUTIONARY ORIGIN or THE VERTEBRATA.——In the preceding portions of this book it has been shown that Embryology provides us with a record in at least its main outlines——ot' the evolutionary changes which the various organ-systems have undergone within the group Vertebrata. For, amongst others, the reasons stated at the foot of p. 491 the record is less clear regarding the evolutionary history of the complete individual. Even however if we had this record complete for the various types—Fish, Amphibian, Reptile, Bird—we should ﬁnd ourselves still confronted with the interesting problem of the first origin of the primitive Vertebrate type :—from whence came these lowly original Vertebrates out of which the various existing types of Vertebrate have been evolved?

This problem of the ancestry of the Vertebrata is naturally a fascinating one and it has attracted much attention and been the theme of voluminous writing. Enthusiasts have at different times endeavoured to demonstrate that the Vertebrates are descended from this phylum or from that. It is perhaps best not to take such attempts very seriously. They have served a useful purpose in arousing interest and stimulating research but they have little claim to a place in the permanent literature of Zoology. «

We are naturally unable to get any evidence bearing upon the 504 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

problem from Palaeontology. The most ancient Vertebrates of which fossil remains are known had probably already evolved to a far greater distance from the original type of Vertebrate than that which separates them from the existing Vertebrates of to-day. And the probability is that the earliest Vertebrates went on existing and evolving through long ages before they developed those complex skeletal structures which are alone adapted for preservation as fossils in the geological record. Comparative Anatomy fails us too——-for up to the present no existing type of animal has been discovered which can justiﬁably be interpreted as an unmodiﬁed survivor of the original Vertebrates.

It is Embryology alone which yields us examples of Vertebrates in the earliest stages of evolution but the data afforded by that science do not carry us beyond the formulation of a few very broad and general conclusions regarding the prevertebrate phases in the evolutionary history of the phylum.

(1) The fact that Vertebrates, like other Metazoa, commence their existence as a unicellular zygote appears to justify us in postulating a unicellular tie. a Protozoan ancestral stage.

(2) The fact that there occurs in the admittedly more primitive Vertebrates a gastrula stage appears to justify us in postulating a diploblastic or Uoelenterate ancestral stage.

(3) The facts which are united together in the Protostoma hypothesis suggest that the coelenterate ancestor evolved along lines somewhat similar to those of the modern Sea—anemones with their elongated slit-like protostoina dilated at each end and surrounded by a concentration of the ectodermal nerve-plexus.

(4) The facts that the coelome was probably originally segmented (as indicated by Amphtowus), that the excretory organs are in the form of nephridial tubes, that the vascular system consists fundamentally of longitudinal vessels on opposite sides of the alimentary canal connected together by vascular arches, the blood passing tailwards in the vessel on the neural side of the alimentary canal—— suggest that there intervened between the coelenterate phase and the vertebrate phase a stage which possessed many features in common with those animals which are grouped together to-day in the phylum Annelida. We may suppose that this annelid-like creature became evolved from an Anemone in which the body had become drawn out, as in the genus Herrpolitha or one of the brain corals, and which had become actively motile. In the two diverging stems which gave rise to Annelids and to Vertebrates respectively we may take it that a difference existed in the normal position of the body—-—the former progressing with their neural, the latter with their abneural, surface underneath. It is conceivable that this difference may have been associated with the difference between a creeping mode of life in which the chief sensory impressions were related to the solid substratum and a swimming mode of life in which they rather came from above. Ix GERM LAYER THEORY 505

ADDENDUM TO CHAPTER IX.——More than once in the course of this volume reference has been made to the “ Theory of Germinal Layers” or the “Germ Layer Theory.” This theory, which has played a great part in the development of embryological science in the past and still dominates to a great extent embryological research, had its foundations in observations made by these pioneers of embryological science — Wolff, Pander, von Baer and Remak. Wolff (1768) observed that the alimentary canal in the Bird embryo is developed out of a thin membrane or leaf (“ Blatt”) and inferred that the other organs go through a similar stage. Pander (1817) gave the name “ blastoderm ” to the ﬁrst membrane-like stage of the embryo as a whole, saw how this became differentiated into the three layers-——outer, middle and inner——and traced out the development from _these of the main organ-systems. Von Baer (1828) carried on and elaborated l’ander’s work, recognized that the middle layer was double, and that it was secondary to the two primary layers: the outer and the inner. He also extended his observations to forms other than the Fowl and laid the foundations of Comparative Embryology. Remak (1855) ﬁnally worked out the germ-layers in terms of the Cell-theory, traced the origin of the coelome to a split in the middle layer, and worked out more precisely the relations of the layers to the deﬁnitive organ-systems.

One of the most important steps in the development of the Germ Layer Theory was made by Huxley (1859) who as a result of his researches upon the Medusae recognized the two primary cell-layers in these animals (named by Allman “ eetoderm ” and “ endoderm ”) and suggested the comparison of them with the two primary layers of the Vertebrate embryo.

Embryology, like Morphology in general, ﬁrst became a real living science as a result of Darwin’s demonstration of the fact of evolution. In the Omlgivt Qf Species (1859) the principle of recapitulation is already admitted. “Embryology rises greatly in interest, when we thus look at the embryo as a picture, more or less obscured, of the common parent-form of each great class of animals.” The idea was further elaborated by Fritz Muller (1864).

Kowalevsky (1871, etc.) and other embryologists had demonstrated the wide-spread occurrence among the Invertebrates of an early stage of development more or less cup-shaped in form and consisting only of the two primary cell-layers, and the important advance was made synchronously by Lankester and Haeckel of perceiving in this two-layered stage a repetition of a common ancestral form.

Lankester (1873) recognized amongst the Metazoa two distinct grades of complexity of structure so far as their cell-layers were concerned—the diploblastic grade (represented by the Coelenterate) consisting of the two primary layers, and the triploblastic grade with an interposed middle layer. Further he recognized that each Metazoon—whatever its deﬁnitive condition—passes in the course 506 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

of development through a diploblastic stage which he termed the planula. Such a planula. stage he regarded as a repetition of a common ancestral stage of evolution.

Haeckel (1872) about the same time as Lankester also developed the idea that the diploblastic stage of ontogeny was to be interpreted as the repetition of an ancestral form: Haeckel called this ancestral form Gastraea. The main difference between Haeckel’s view and Lankester’s was that the former regarded the endoderm as having arisen by a process of invagination——-as it actually does arise in ontogeny in the great majority of cases—-—while Lankester regarded it as having arisen by a process of delamination from the outer la er.

y As regards the middle germ-layer ideas remained somewhat vague until Agassiz (1864) showed that in the Starﬁsh the mesoderm arose in the form of an outgrowth of the archenteric wall. The same was found to be the case in various other Invertebrates, and in 1877 Kowalevsky showed how in Amp}:/iowus the mesoderm was during an early stage in the form of archenteric pockets. In the same year Lapkester developed the generalization that the coelome is to be regarded as uniformly enterocoelic in origin and comparable with the diverticula of the archenteric lining seen in Coelenterata.

The separation of such mesodernial cells as are in their early stages free and amoeboid under the common name mesenchyme was ﬁrst made by O. and R. Hertwig (1882).

The later developments of the theory of the mesoderm involved in the Protostoma theory have already been alluded to earlier in this volume and the same applies to what the author regards as the chief qualiﬁcation of the germ-layer theory indicated by modern work, namely that the boundary between two layers where they are continued into one another must be regarded not as a sharply marked line but as a more or less broad debatable zone.

LITERATURE

Agassiz. Contributions to the Natural History of the United States of America, v. Boston, 1864. [Vol. v printed as vol. v, pt. 1, of Mem. Mus. Comp. Zoology H8l'Va.1‘d.] _

Baer. Uber die Entwickclungsgeschichte der Thiere. Beobachtung und Reﬂexion, i. Konigsbcrg, 1828.

Bell. Arch. Entwick. Mechanik, xxiii, 1907.

Piirbringer. Gegenbaurs Festschrift. Leipzig, 1897.

Haeckel. Die Kalkschwamme. Berlin, 1872.

Hertwig, 0. Arch. mikr. Anat., xxxix, 1892.

Hertwig, 0. and R. J enaische Zeitschrift, xv, 1882.

Jérgensen. R. Hertwigs Festschrift. Jena, 1910.

Kerr, Graham. Proc. Roy. Phys. Soc. Edin., xviii, 1912.

Kopsch. Internat. Monatsschr. Anat. u. Phys., xvi, 1899.

Kowalevsky. Mém. Acad. Sci. St-Pétersbourg, (7), xvi, 1871.

Kowalevsky. Arch. mikr. Anat., xiii, 1877.

Lankester. Ann. Mag. Nat. Hist., (4), xi, 1873.

Lankoster. Quart. Journ. Micr. Sci., xvii, 1877.

Lereboullet. Ann. Sci. Nat., 4, Zool., xx, 1863. IX GERM LAYER THEORY 507

Mﬁller. Fiir Darwin. Leipzig, 1864. ‘ Pander. Beitrzige zur Entwickelungsgeschichte des Hiihnchens im Eye. Wiirzburg, 1817.

Parker. American Natltralist, xliii, 1909.

Rabl. Morph. Ja.hrb., xv, 1889.

Rauber. Priniitivstreifcn und Neurula. der Wi1'bc1thie1'e. Leipzig, 1877.

Remak. Uxltersuchuugen ulwr die Entwicke-lung der \Virbe1thiere. Berlin, 1855. Sedgwick. Q,11a.rt. Journ. Mic-r. Sui., xxiv, 1884.

Sedgwick. Quzwt. Jmxrn. Micr. Sci., xxxvii and xxxviii, 1895 and 1896.

Wolff. Nov. Conmwnt. Acad. Sci. St-I’éte1'Sl>O1U'g. Xii, 1768.