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

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Chapter VII The External Features of the Body

The preceding chapters have dealt with the ontogenetic evolution of the various organ systems of the vertebrate body. The present chapter will sketch in outline the development of the external characteristics in so far as these have not already been referred to.

(1) DEvEI.oPMEN'r or GENERAL FORM.

The groups of Ve1‘Lcl)1‘nt('s in which the egg is typically holoblastic will be considered first.

CROSSO1”l‘EltY(:II.———Of the two surviving genera 1’olg/ptcrus alone has been studied (Graham Kerr, 1907) and the main features in the development of its body-form may be gathered from an inspection of Fig. 197.

It will be seen that the head—end of the embryo is the first to project freely above the general surface of the body (Fig. 197, The tail projection soon however makes its appearance (Fig. 197, B) and during subsequent stages grows much more actively in length, the embryo soon assuming a somewhat tadpole-like shape, with a laterally compressed hinder region a11d a rounded swollen anterior region formed by the main part of the yolk-laden egg. Two organs, the cement-organ (0.0) and the external gill (e.g), inake their appearance as slight bulgings of the surface at a very early stage. During subsequent stages the binder, laterally compressed region grows rapidly at the expense of the mass of yolk which becomes consequently reduced in volume and at the same time loses its spherical shape s» that it projects less prominently. It will be noticed that during the later stages the post-anal region grows particularly actively, the anus thus coming to lie at a relatively greater and greater distance from the hinder end of the body and giving rise to a rapidly growing true “ tail” region. During the later stages (Fig. 197, D, E, F) the head undergoes much increase in length, its active forward growth beginning about stage 31. The mouth is at first widely gaping (Fig. 197, E) but by stage 34 the mouth-hinge becomes functional and it can be closed. By stage 36 the anterior swelling due to the yolk has practically disappeared.

ACTINOPTERYGII.—A1nongst the Actinopterygian fishes the Ganoids which still retain the holoblastic segmentation show very

FIG. 197.-——St:1;.:o.s in the «IL-.vclop1'm-.nt of l‘u/_;_/I;/o:'ru.._<»'. (All except A :lft(.!l‘ drawings by lillclgett.)

A, stage 12; B, 23; C, 27; D, 31; E, 33; I", 36; (I, 1:u'\':L 30 mm. in len;.;'t11. (I.,ill|1l. ; mu, cument organ ; E, eye; ¢.-..g, external gill; op, ope:-culum; p.f, pectoral Iin ; y, yulk. (A-E x 11; F x 8.)

much the same arrangement in early stages as will be seen in the Lung-ﬁshes (l<i0'. 200, A), the dorsal part of the embryonic body being curved round the periphery of the egg. As theembryo increases in length the growth of the posterior end is specially active and the general proportions become very much as in Polypterus. The somewhat tadpole-like appearance of the larva, caused by the persistent spherical shape of the main mass of yolk, is again apparent-especially in Amie and Lepidosteus (Fig. 198, A). As in Poly/pterus

Fm. 12.18. —-Stamges in the development of 1.:-,u'¢1u.s-(ms.

(I, anus; I...-_, widely gaping buccal cavity : «nu, (-elln-11l‘nrg':1n ; .»,». npereulum; p.f, pectoral ﬂu; pl.f, pelvic lin.

the intestinal portion of the alimentary canal rudiment is relatively slender in form, arising by a process of actual backgrowth of the posterior trunk region rather than by gradual modelling of the yolk as is the thick intestinal rudiment in the Lung-ﬁsh. Conspicuous characteristics of the actinopterygian Ganoid larvae are the presence of well—deve1oped cement-organs and the absence of external gills.

In the Teleostean ﬁshes there has come about with the high development of telnlecitliality a great reduction in the angular extent of the e1nlu‘_yuni«-_. rudiment during its early stages. Consequently there is very slight ventral curvature round the. yolk. In the FIG. 199.-—-(U//IIIII!/'11/HIS nljlu/I'4'-II.s'. ilftttl‘ Asshetmx.)

A, seventh day; 13, t;o':nt..h «lay ; (J, l‘uurt;ccnt,h «l:1_y ; I), ago unknown; E, I'o1'Ly-tlnirtl day.

Granoids Azrmlco and Lepidosteus the main mass of yolk retains its form for a considerable period, causing a great bulging of the ventral body-wall anteriorly. In the Teleost this is still further accentuated, the bulging forming the yolk-sac which remains prominent even in larvae sufficiently developed to be able to swim actively. An extreme case of the prominence of the yolk-sac is afforded by G’;/mncrclz/us (Fig. 199) where it shows a peculiarly elongated form for a certain period. Cement organs are as a rule absent in Teleostei : so also are external gills though in rare cases the latter have physiological representatives in ﬁlamentous prolongations of the gill lamellae (Fig. 199, B).

Great variety of form exists amongst the larvae of Teleostean ﬁshes, more especially amongst those of pelagic habit. Familiar examples are seen in the pelagic larvae of the Eels—-much compressed from side to side, transparent and colour-less—even the blood being free from liaemoglobin———and much greater in bulk than the innnediately succeeding phase in the life-history. The larvae of the Flat-ﬁshes (Pleuronectidae—Flounder, l’laice, Sole, etc.) are again of special interest owing to the extraordinary asymmetry which they develop. They are at first quite symmetrical and in no way abnormal. The larva swims at this time with its laterally compressed body vertical after the manner of a Bream but later develops the habit of swimming on its side. The side of the head-region which is below now grows more actively than the other so that the head becomes strongly asymmetrical and the eye. of the lower side becomes gradually transferred to the upper, the right and left eyes being now both on the same side of the head. Correlated with this asymmetry in form there comes about a corresponding asymmetry in colour, the chromatophores being collected together on the upper side and giving it its characteristic obliterative colouring, In some genera it is the right side of the body which is above, in others the left——while in a few species it appears to be indifferently the one or the other.

DIPNOI.—-—Both of the dipneumonic L11ng-ﬁsheS——Lq)idos’i7°(m and 1)’I'0t0])t67"’lt8——-ll:tVB been investigated (Graham Kerr, 1900 and 1909; Budgett, 1901). They closely resemble one another and Lepi«lo.yia~en Will be chosen here for description (Fig. 200).

During the early stages of the modelling of the embryonic body (Fig. 200, A) the latter is curved round the egg, occupying about 290° in angular extent. The head-region becomes demarcated as a slight, somewhat lance-shaped protuberance above the general surface of the egg due to the neural rudiment. The branchial region becomes marked at an early stage by a slight elevation of the surface which soon becomes divided by shallow oblique grooves into. the series of branchial arch rudiments. About stage 25 (Fig. 200, B) the tip of the head and the tip of the tail project sharply above the general surface: the external gills (c._q) are now in the form of four distinct little knobs on each side, and the cement organ (6.0) has made its appearance as a crescentic structure on the ventral side curving round the tip of the

FIG. 200.-—Stages in the development of Lepidosiren pa.mdo;ca.

A, stage 23; 13,25; 0, 26; D, 28; E, 31; F, 33; G, 35; II, 36. (2.0, cement organ; E, eye; ¢a.g/, external gill; M, mnuth; p.f, pectoral ﬁn; pl. f, pelvic ﬁn; sp.z..~, spiral valve of intestine. (A-FXB; Gx2'5; IIX2.) VII EXTERNAL FEATURES OF DIPN OI 435

head. The posterior part of the body now becomes laterally compressed, it grows rapidly in length and the larva assumes a somewhat tadpole-like form——the apparent “ tail” being at ﬁrst bent ventrally (Fig. 200, O). '1‘he anus is situated close to the tip of this portion of the body, therefore it is, strictly speaking, not tail but rather posterior trunk-region. About this period hatching takes place. The tail-like hinder region now straightens out (Fig. 200, D) and grows rapidly in length, the growth being at ﬁrst mainly pre-anal and the true tail-region developing later. As in Crossopterygians the tail is throughout protocercal. As in I’ol3/pterus again the headregion for a considerable period shows no active growth in length: it is not until about stage 31 (Fig. 200, E) that its growth becomes active and the head-region begins to develop the modelling of its deﬁnitive features. The external gills grow actively in length after hatching: each develops a double row of pinnae along its external margin and eventually all four become fused togetlier at their bases. They reach their maximum about stage 35 and thereafter undergo a process of atrophy resulting in their complete disappearance. The limbs make their appearance about stage 31, each as a little knob bearing a striking resemblance to the ﬁrst stage of an external gill. The cement organ increases in size forming a large cushion-like and very conspicuous organ in the larva of stages 32-34 (Fig. 200, F). Eventually it shrivels up and disappears without leaving a trace behind.

In 1’r0topte7°zLs as already mentioned the general features of development agree very closely with those of Lep'iclos'£7'en.

Of Cerutoclus developmental material was obtained by Caldwell in 1884 a11d by Semen in 1891. Semon’s material has formed the basis of a long series of investigations by himself and others which together constitute an important contribution to Vertebrate morphology (Semen, 1893-1913; 1901*).

While the general modelling of the body shows a general resemblance to that of Lepido.9-iren and P7'otopterus there are certain well-marked differences in detail. Perhaps the most striking of these is that the head-region shoots ahead in its development and grows actively in length so as to project freely in front of the yolk at a much earlier period than in the other genera (Fig. 201, A, B). Again the main mass of yolk undergoes a more uniform process of lengthening so that it assumes a somewhat spindle-like form and allows the body as a whole to become slender and “ﬁsh ”-like,. the “ tadpole” shape due to the persisting spherical mass of yolk in Polypterus or Lepiclosiren being here absent. During the later larval stages the divergence of Oemtodus from the other two Lungﬁshes towards the more typical ﬁsh condition becomes marked by the paddle-like form of the limbs and the much greater development of the median ﬁn round the hinder end of the body. It will be noticed also that two conspicuous features of the young Lep'id0s'i7'en or P'rotopte'rus—the Cement organ and the external gills-are completely absent in (Ieratodus.

In the Urodela the least specialized subdivision of the Amphihia the evolution of external form closely resembles that of the Lung Fm. 20].——Development of C'emt4)dus_/0'rste'ri. (From Sen1ou——1'n. the Australian Bush.) A, stage 32; I3, 34; C, 38; D, 41; E, 45; F, 48. (Magnillcation about 6,} diameters.)

ﬁshes. An early ‘stage of such a relatively primitive member as Nectums might readily be mistaken for the corresponding stage of I vn

EXTERNAL FEATURES OF AMPHIBIA

Oeratodus and an almost equally striking resemblance is shown by

an Axolotl or Newt about the time of hatching, except that in this case there are the well-developed external gills which were as we have seen absent in Ueratodus though present in the other two Lung-ﬁ.shes.

In the case of the Anura it is perhaps premature to make general statements regarding the diflerences in form which distinguish them from the more primitive Urodela, for different species

differ greatly in the size of the

egg and its richness in yolk and the great majority of them have not as yet had their development worked out.

The head-region projects less prominently, sometimes beingin its early stages quite ﬂattened out on the yolk (Alytes, Phyllomedusa) while in other cases the embryo elongates as a whole there being for a time no marked break in contour between head, trunk and tail. In such cases growth in length may for a time be most active ventrally, so as to cause a curvature of the embryo with its concavity on the dorsal side (Rama). In the later stages the tail-region is highly developed, the splanchnocoele being greatly shortened and widened and the head also very broad giving the

characteristic tadpole type of

larva.

Particular interest attaches to the development of such types of Amphibia as possess heavily yolked eggs. A good example is afforded by the Gymnophiona such as Hypogeophxis (Fig. 202). A conspicuous difference from the condition seen in the Telec SCOIIIBS (1),

FIG. 202.—Embryos of 11;:/pogeopluis rostratus. (After Brauer, 1899.)

A, 15, ()x4_; I) xll. (For 41¢‘-tails of B cf. Fig. 87, In‘, eye; «.3/, (‘Kl-I‘-l'lHll gill ; ul_/ ‘l':u-tory orgzm. 438 EMBRYOLOGY OF THE LOWER VERTEBRATES OH.

in the fact that here as in the Dipnoi the embryonic body during the early stages of its differentiation has a much greater angular extent, curving round the mass of yolk cells instead of being restricted to a small extent near the apical pole. Another important point to notice is the well-marked downward flexure of the head during early stages—-—-a feature which has already been correlated (p. 93) with the presence of a large supply of yolk. The active forward growth of the head-region leads to the rounded main mass of yolk being situated well back, just in front of the anal region (Fig. 202, 0), instead of anteriorly as in the tadpole,shaped larvae of Lepidosiren. or Protopterus or the Ganoid ﬁshes.

ELASMOBRANCHII.—-Of the isolated groups of Vertebrates characterized by having meroblastic eggs the most nearly primitive is that of the Elasmobranch ﬁshes. Unfortunately for purposes of comparison we are not, up to the present, acquainted with any member of the group possessing small eggs poor in yolk.

Here as in other groups with typically meroblastic eggs the early rudiment of the body of the embryo——or more correctly of the dorsal portion of the body——extends through a relatively small angular extent, in striking contrast with the 200” or more of a Lung-ﬁsh or of one of the Gymnophiona. As the embryo proceeds with its development it grows actively in length, headwards and tailwards, so as to project freely in a tangential direction, remaining in connexion with the main mass of the egg (yolk-sac) by a narrow yolk-stalk. During the forward growth of the head growth-activity is less pronounced on the ventral side so that the gill-clefts are forced into an oblique position and the head undergoes pronounced cerebral ﬂexure.

AMNIOTA.——In the non-mainmalian Amniotal the ﬁrst point to notice is that although the size of the egg and the absolute amount of food-yolk contained within it are relatively enormous yet the degree of telolecithality is less extreme than it is in the case of the meroblastic eggs of ﬁshes. Consequently the segmentation process resulting in blastoderm formation spreads in an abapical direction past the level at which the posterior end of the embryonic rudiment will be developed: as a result of this the entire embryonic rudiment lies at its first appearance well within the boundary of the blastoderm, instead of its hinder end being coincident with that boundary as is the case in Elasmobranchs.

Here again the embryonic body grows forwards and backwards free from the surface of the egg, the backward growth being much less pronounced than in the case of the ﬁshes in anticipation of the ultimate lesser degree of development of the tail-region correlated with its diminished locomotor importance in the adult.

The most striking feature however is one which may perhaps be correctly expressed by saying that the clogging inﬂuence of the

1 The external features in their development are well illustrated by the developing Bird (see the figures in Chap. X.).

yolk upon the growth in length of the ventral side of the body is much more marked than in other Vertebrates. The result is a strong ventral curvature of the body. The ventral flexure of the head. in the mid-brain region already seen in the Elasmobranchs and Grymnophiona is here still more marked, but in addition the whole body is strongly curved ventrally to such an extent as to form more than one complete t11rn of a spiral. This curvature is in its incipient stages of great morphological interest as providing a possible explanation of the downward indentation of the blastoderm by the head and tail regions, and their consequent ensheathment in blastedermal pockets, which led eventually to the evolution of the amnion.

The formation of the amnion and the separation of true amnion from false amnion involve as will be gathered from Chapter VIII. a solution of continuity of the somatopleure or original body-wall and probably this has initiated what is perhaps the most striking feature of amniote development—the loss, at the time of batching, of a relatively large proportion of somatopleure together with the allantois.

As a matter of minor detail it should be mentioned that in the case of Birds as compared with the lower Amniota the embryo is distinguished during a long period by the relatively enormous size of the head. It seems reasonable to regard this as in the main an anticipation of the great development of the eyes and optic lobes in the adult.

In the foregoing short sketch the author has confined himself to the main branches of the Vertebrate stem. He has omitted all reference to three different types near the base of that stem, namely Amphz'oams, the Lamprey, and the Myxinoid, which are of great interest in themselves but which are of less importance for enforcing general principles of Vertebrate development. Of the three types the ﬁrst will be found fully described by MacBride in Vol. I. and it will easily be seen how in the general form of body, as in various other characteristics, the young Amphioxus has diverged widely from the more typical Vertebrates. The Myxinoids, so far as they are known from Bashford Dean’s researches on Bdellostoma (1899), appear also to be highly specialized. The Lampreys on the other hand have diverged to a much less extent from the normal. The most striking features during the early development of the body are (1) that the head-region, as Was the ease in C'e7"at0du.~: and Hypogeoplz/is and as is the case also with Bdellostoma, shows a marked activity in its growth in length, the mass of yolk persisting longest posteriorly and (2) that the outgrowth of the tail is delayed until a comparatively late period. A marked negative feature in all three of the types mentioned is the absence of all trace of paired limbs.

(2) THE MEDIAN FINs.—- The primitive Vertebrate, with its segmented musculature arranged along the two sides of the body and its skeletal axis and central nervous system lying at the mesial plane, is clearly a creature constructed for swimming by lateral ﬂexure after the manner of an Eel. To secure greater eﬂiciency the body, more particularly its purely motor post-anal portion, becomes compressed from side to side, the compression being most marked near the margin of the body where the thin almost membranous median ﬁn is produced.

In development the median ﬁn arises as a projecting fold of slightly thickened ectoderm into which later on mesenchyme penetrates. 111 what the evidence points to as being the primitive condition this ﬁn rudiment is continuous and extends round the hind end of the body. In such relatively primitive Vertebrates as Orossopterygians, Lungﬁshes, and some Elasmobranchs, it extends forwards on the dorsal side practically to the head-region, while on the ventral side it reaches the anus and may even be continued onwards as a pre-anal median ﬁn, though possibly this has originated in phylogeny independently of the main ﬁn-fold.

In the Lung-ﬁshes the median ﬁn-fold during the course of development never loses its continuous and practically symmetrical arrangement round the tip of the tail. lt retains throughout life the ptimitive symmetrical (protocercal) form. In the Crossopterygians (apart from the anterior portion ofthe dorsal ﬁn which becomes divided up into a series of ﬁnlets) the same holds until a very late stage in development, the tail of the adult becoming very slightly asymmetrical though the term protocercal is usually and justiﬁably still applied to it. A similar protocercal tail occurs in the Amphibian larva while the tail of the adult Newt or Crocodile is simply a protocercal tail in which there is no longer a membranous ﬁn-fold present.

It is however characteristic of the ﬁshes in general that, in accordance with their high specialization as expert swimmers, the median ﬁn during ontogeny loses its homogeneous character——eertain portions of it, probably those portions which are in mechanically the most favourable positions, becoming enlarged while the intervening portions become reduced to the point of complete disappearance. The result is that the place of the originally continuous ﬁn-fold is taken by a series of separate ﬁns—--one or two dorsal, a caudal or tail ﬁn, and on the ventral side, an anal ﬁn. 01' these the caudal fin--most favourably situated of all the series to serve as a propelling organ——becomes specially enlarged. It is also characteristic of the more efficient swimmers that the part of the caudal ﬁn lying on the ventral side of the axis becomes particularly developed. We may probably associate this with the function of rotating the body about its long axis as may be seen in a shark when it seizes its prey. The unsymmetrical condition of the tail so produced is termed heterocercal. When carried to its extreme the tip of the vertebral axis becomes tilted upwards and, so far as external appearance goes, a (secondarily) symmetrical condition is arrived at, as is seen in the homocercal tail of the Teleostean ﬁshes. It will be understood that the protocercal, heterocercal and homocercal conditions merge into one another and cannot be distinguished by any rigid deﬁnition.

They clearly represent successive grades in the evolution of the tail as a more and more perfect organ of propulsion, a process of evolution which has come about independently in the various groups of ﬁshes. Thus even the Lung-ﬁshes—the surviving members of which group possess the primitive protocercal type of tail——during the geological periods when they most ﬂourished showed numerous forms in which there was a highly developed heterocercal tail.

Again the assumption of a sluggish mode of life, or the simpliﬁcation of the swimming movements, is frequently correlated with reversion of the tail towards the. protocercal condition. This is clearly seen in many teleostean ﬁshes, such as the Eels and many deep—sea bottom-frequenting ﬁshes. In such cases all trace of the unsymmetrical condition may have disappeared from ontogeny but there is no room for doubt regarding an ancestral heteroeercal or homocercal condition——-for in their general structure these ﬁshes are highly evolved Teleosts and the group as a whole is characterized by the tail being homocercal.

In the case of’ the surviving Lung-ﬁshes the general archaicism in structure, and more especially the extremely archaic character bf the paired ﬁns, are in favour of the protocercal character of the tail being persistent rather than revertive-—apart from the evidence of embryology which fails to disclose any trace of a pre—existing heteroeercal phase.

(3) THE LI.\ms.—~()nc of the characteristic structural features 01 the Vertebrata is the presence of the two pairs of limbs, pectoral and pelvic. Two main types of such limbs can be recognized—the ﬁn type for swimming and the. pentadactyle or leg type for moving on a solid substratum. As the former is on the whole characteristic of ﬁshes, and as ﬁshes are on the whole more nearly primitive than are terrestrial \'e1‘tcbrates, the idea has naturally arisen and has now attained perilously near to the position of a dogma that the leg type of limb has been evolved out of the fin; and elaborate attempts have been made to deﬁne the manner i11 which this has come about. It is necessary at the outset to emphasize the importance of keeping an open mind upon this question: there exists the possibi1ity———which as will be seen later is not lightly to be. brushed aside—that pentadactyle limb and ﬁn are not in the relation of lineal descent at all but that they have been derived from a common ancestral type of limb differiiig from either.

No limbs exist in Amp/uJo.vus or in the Cyelostomata. There is however a general tendency in Vertebrates which have assumed an eel-like form of body for the limbs to degenerate and disappear, and it is well to bear in mind the possibility that this has happened in the case of both of the types mentioned.

The limb at its ﬁrst appearance in embryonic development forms a little projection from the body surface—a core of mesenchyme enclosed in an ectodermal sheath. In Lapidosirevt or Protopterus or a Urodele it is in the form of a rounded knob identical in appearance 442 EMBRYOLOGY OF THE LOWER VERTEBRATES CII.

with the rudiment of an external gill, but in a large proportion of the Vertebrates it is narrower in a dorsi-ventral than in an anteroposterior direction so as to have the form of a short longitudinallyrunning ridge.

As is usual where active increase of surface is about to take place the projecting limb rudiment is foreshadowed by a thickening of the ectoderm and by a condensation of the underlying mesenchyme.

In Torpedo, one of the Rays--fishes characterized by the great antero-posterior extension of the large pectoral ﬁn——the two limb, rudiments which are at ﬁrst distinct (Rabl, 1893) become for a time joined together by a transitory ectodermal thickening. This phase, in which the two ﬁn rudiments are as it were parts of a continuous ridge, was the earliest stage observed by Balfour (1878) and it afforded him an embryological basis for the lateral-fold view of the phylogenetic origin of the Vertebrate limbs (see p. 445).

As the limb rudiment develops it shows in many cases characteristic changes in its position. First it shows a movement of rotation. This is well illustrated by the ease of C'e7'at0dus as described by Semen (1898). Here the pectoral limb rudiment becomes rotated in such a way that its originally pre-axial or headward edge becomes dorsal and its originally lower or ventral surface comes to face in a headward direction. In other words, if one could observe the developing left pectoral limb from a point away to the animal's left side the limb would be seen to undergo a clockwise rotation. It results from this that when the fully developed limb is folded back alongside the body its outer surface is that which was originally ventral. A rotation similar in direction though varying in angular extent in different forms occurs also during the development of the pectoral tin in Crossopterygians and Actinopterygians. In Tetrapoda, on the other hand, a rotation of the limb rudiment in the opposite direction takes place—the pre-axial edge becoming ventral. N ot improbably this may be regarded as a secondary modiﬁcation foreshadowing the pronate position of the fore-limb characteristic of terrestrial progression.

The pelvic ﬁn in Ceratodus undergoes a similar rotation but in the opposite direction to that of the pectoral: the left pelvic ﬁn regarded from a point away on the animal's left would be seen to undergo a counter-clockwise rotation. The result is that the originally dorsal surface comes to face headwards or, when the ﬁn is folded back alongside the body, outwards.

The corresponding rotation of the pelvic limb in other ﬁshes and in the lower Tetrapods appears to stand in need of further investigation,

It is clear from the facts of Comparative Anatomy that the paired limbs have undergone extensive shiftings along the surface of the vertebrate body in adaptation to its general form and its method of movement (see below, p. 448). It is of interest-——though not necessary for establishing the fact of such phylogenetic shifting-—to enquire whether any record of it occurs in ontogeny. Obvious evidence which at once suggests itself‘ in this connexion is the presence of abortive muscle-buds in front of or behind those which become incorporated in the definitive limb. These seem clearly to indicate that the part of the body surface superﬁcial to these buds was at one time part of the actual limb. But unfortunately such abortive buds occur both anterior and posterior to the definitive. limb and there is no means of ﬁxing deﬁnitely the time in phylogenetic evolution from which the two sets of abortive buds date. They may date from the same period, in which case they might merely aﬁbrd evidence of the process of narrowing of the limb base which has undoubtedly taken place during the later evolution of ﬁns; or they may date from dill'ere11t periods, in which case the anterior set might be taken as evidence of a backward movement of the limb, and the hinder set as evidence of a forward movement occurring at a dilli-rent period—— movements which again have undoubtedly taken place. In View of the impossibility of determining to what extent the evidence in any particular case is to be interpreted in these two different directions it seems on the whole advisable to leave this muscle-bud evidence on one side.

Other evidence has been adduced from cases where the actual limb rudiment as a whole (’i.6. the projection from the surface of the body) seems to be displaced during development. For example in the ﬁgures illustrating the development of the pelvic limb in Spvlnaa; (p. 207) it will be seen that the anterior limit of the ﬁn is in successive stages of development opposite myotomes 21, 26, 28 and 3]; the hinder limit at the same stages opposite myotomes 30, 38, 38 and 39, and the middle of the ﬁn base opposite myotomes 25, 32/33, 33/34 and 35/36. It seems quite allowable in such a case to speak of the limb as having undergone a backward displacement. In other cases, as that of Sq?//ldzmz. according to Goodrich (1906), ontogenetic development discloses no evidence of such backward migration.

The limb rudiment gradually increases in size and assumes its deﬁnitive form and as it does so it becomes equipped with its characteristic skeletal and neuromuscular arrangements in the manner already described.

Phylogenetic Origin of the Limbs

The limbs are organs highly characteristic of the V ertebrata. While they exist typically as two pairs, pectoral and pelvic, one or both pairs readily disappear in groups where they are no longer needed. They are particularly prone to disappear in those Vertebrates which assume an elongated form of body and revert to the archaic method of moving by lateral ﬁexure. Thus in Eels the pelvic limb has disappeared, in S3/mbrancltus both pairs. In Lepidosiren, the most elongated Lung-ﬁsh, we see both pairs in process of reduction. We see the same in elongated Urodeles such as A1n.ph'im22a., while in the Gymnophiona both pairs have vanished. In Reptiles we see beautifully how the limbs undergo reduction (O/mlcvldes) and complete disappearance (Amphisbaenidae, Alngwis) in those various groups of Lizards which have developed an elongated snake-like form. So also in Snakes.

In cases where the limbs are completely gone in the adult it may be possible to observe them during early stages of development. The young Symbranchus (Fig. 203) has for a time huge pectoral ﬁns which it uses as organs of respiration (Taylor, 1914). In Gymnaphiona and Blind Worms (Angu'£s)‘ minute limb rudiments have also been observed in the embryo. In other cases no trace of the missing limbs has been found during early development. In view of this general tendency of the limbs to disappear in Vertebrates which have assumed an eel-like or snake-like form of body it is well, as already indicated, not to assume a dogmatic attitude in regard to such Vertebrates as Lampreys or Hag-ﬁshes. The possibility is not excluded that even these Cyclostomes are descended from ancestors in which limbs were present.

FIG. 203-""SU7n.bm-m:/rus -ﬁ‘e..m'm.m'u/am. Larvae showing I-lectoml ﬁ"S' (After Taylor, 1914.)

o.u, opercular opening; s.i.'v, subintestinal vein ; y, yolk.

The interesting question now emerges—-1-Iow did the limbs of the Vertebrate originate in evolution 2 Few morphological speculations have excited more interest and more controversy than this. Two main hypotheses have been propounded and each has found supporters amongst the most eminent morphologists. Although in the opinion of the present writer it is no longer necessary to fall back upon either of these views, a simpler possibility having presented itself, a

The elementary student may be warned not to mistake the rudiments of the paired penes in Snake embryos for limbs

short sketch of each and of the arguments for and against it may now be given. The two hypotheses indicated are the “ Lateral Fold ” hypothesis of Balfour, Mivart, Thacher and others and the “ Gillseptum ” hypothesis of Gegenbaur and his school. Each hypothesis concerns itself with the origin of the paired limbs of ﬁshes -—the ﬁn being regarded as the primitive type of limb from which the pentadactyle limb has been evolved later on.

The Lateral-Fold Hypothesis

It will be remembered that the mode of development of the median unpaired ﬁns indicates clearly that these ﬁns are simply persisting and exaggerated portions of a once continuous median ﬁn-fold. According to the lateral-fold hypothesis of the origin of the limbs the paired ﬁns of ﬁshes are similarly to be looked on as persisting and enlarged portions of a continuous ﬁn-fold which once extended along each side of the body. The hypothesis rests upon a tripod basis of Embryological, Anatomical and Palaeontological fact.

Balfour in his Development of Elasmobranch ﬁshes (1878) wrote: “Along each side of the body there appears during this stage (G-I) a thickened line of epiblast, which from the ﬁrst exhibits two special developments: one of these just in front of the anus, and a second and better marked one opposite the front end of the segmental 1 duct. These two special thickenings are the rudiments of the paired ﬁns, which thus arise as special developments of a continuous ridge on each side, precisely like the ridges of epiblast which form the rudiments of the unpaired ﬁns.” “If the account just given of the development of the limbs is an accurate record of what really takes place, it is not possible to deny that some light is thrown by it on the ﬁrst origin of the vertebrate limbs. The facts can only bear one interpretation, viz. that the limbs are the remnants of continuous lateral ﬁns.”

Further embryological support to this hypothesis has been provided (1) by the fact that the muscles of the limb are of segmental origin, derived from a number, often a considerable number, of myotomes (see p. 207) and that apparently vestigial muscle-buds have been found both headward and tailward of the series which take part in the muscularization of the deﬁnitive ﬁn, a11d (2) by the fact that the ﬁn type of limb commonly shows a marked narrowing of its base. of attachment during the process of development, the rudiment having during early stages the form of a longitudinal ridge attached throughout its length to the body.

Regarding the evidence upon which the ﬁn-fold hypothesis rests the following criticisms may be expressed. (1) The ectodermal ridge described as connecting the two limb rudiments in Elasmobranchs turns out to be a characteristic not of Elasmobranchs in general but only of Rays (Torpedo) 7I.e. of forms in which there is an enormous, admittedly secondary, extension of the pectoral ﬁn along the side of the body. The Elasmobranchs less specialized in this respect—the

1 = Archinephric.

Sharks and Dog-lisl1es——-do not, so far as is known, develop this ridge.

(2) The fact that the myotomes-—-from which the limb rudiment, like other portions of the body, has to derive its equipment of voluntary muscles———arc themselves metameric and that the skeletal elements necessarily correspond in position with the muscles seems to render it unnecessary to seek any further evolutionary explanation of the tendency on the part of the musculature and skeleton of the limb to exhibit a markedly metameric appearance during early stages in its development. The occurrence of abortive muscle-buds 111 front of the deﬁnitive limb is taken-——-quite reasonably-——as evidence pointing to a tailward shifting of the anteiior margin of the limb having taken place, and similarly the presence of abortive buds behind the deﬁnitive limb is taken as evidence of a headward shifting of the hinder margin of the limb. but this shifting of the anterior and posterior margins of the limb may have in evolution taken place either synchronously (13.6. together with a narrowing of the base of attachment of the ﬁn) or at dhferent periods as the limb shifted backwards and forwards as a whole in accordance with variations in adaptational requirements. The present writer sees no convincing reason for rejecting either of these possibilities and if either be possible then the evidence loses its value as support of one view rather than the other.

(3) The narrowing of the limb proximally and its expansion distally is a process which would naturally take place as the ﬁn became more eﬂieient as a propelling organ --—just as in the evolution of a racing oar or paddle with its broad blade and slender shaft-and, accordingly, too great weight should not be attached to the occurrence of such a process during ontogeny in arguing as to the evolutionary 07"£g'i'a of the limbs.

As regards anatomical evidence stress is laid on the exceedingly close structural resemblance in skeleton and musculature between the paired and the unpaired ﬁns. On the other hand it is suggested that, seeing that lateral and paired fins are organs similar in function and built up out of similar muscular elements, a close similarity in their anatomical arrangements may quite probably be merely a case of that secondary convergence of which so many striking examples are known in the animal kingdom.

An ancient fossil ﬁsh, Cladoselache, is brought in to corroborate the view, its paired ﬁns having each a broad longitudinally-running base of attachment and being apparently supported by separate rays without any continuous basal skeleton. But it is pointed out (1) that what signs there are of basal skeleton maybe readily interpreted as representing the axis of a ﬁn of the Ceratodns type laid back against the side of the body (see Fig. 169, E, p. 353), and (2) that the structure of the tail is of a very highly developed and powerful type and that it is most unlikely that a powerful swimmer, such as the highly evolved tail demonstrates Oladoselache to have been, should VII EVOLUTIONARY ORIGIN OF LIMBS 447

have retained its paired ﬁns in a relatively primitive a11d ineﬁicient condition.

Finally there are great physiological dillieulties in the way of accepting the lateral-fold hypothesis. There are no more fundamental characteristics of the Vertebrate body than the arrangement of its longitudinal muscles in segmental masses along each side of the body, a'nd the position of its skeletal axis, its central nervous system and its main arterial trunk in the region of the mesial plane. It is quite clear that such a creature is built for swimming by waves of lateral ﬂexure after the manner of an Amphioxus, a Lamprey or a Lung-fish. Any new swimming organ that became evolved 111 primitive Vertebrates must have had some advantage over, or at least not interfered with, this primitive method of swimming. it is difficult to see how the supposedly ancestral lateral fold could possibly have complied with these conditions. 'l‘l1e suggestion that the lateral fold may have functioned at first as a balancing organ or as a “bilge keel” will not bear examination from the point of view of elementary physics. Rabl suggests that the two lateral folds may have acted primitively as a kind of parachute and that they became muscularized at their anterior and posterior ends, the intermediate portion undergoing atrophy (thus originating the two pairs of limbs). The‘skeletal elements on this view would also develop at the ends of the ridge ﬁrst, and spread backwards (pectoral ﬁn) or forwards (pelvic ﬁn). Thus would be explained the reversal of the position of the anterior and posterior edges of the two ﬁns in 0.9. C'e'mtodu.s-. Such an explanation however fails entirely to meet the diiliculty that there exists not merely an antero-posterior reversal in the structure of the two ﬁns but also a dorsi-ventral one.

THE GILL-sEr'rUM llYI’O’l‘HESIS.-—Tl1iS hypothesis was based by Gegenbaur (1872) on facts of adult anatomy. In some of the Elasmobranclis (1’r1Istt'.s) the central gill ray attached to the branchial arch is enlarged and the rays next to it have come to have their bases of attachment shifted secondarily from the arch 011 to this enlarged ray, so as to produce an arrangement recalling the biserial archipterygium of Oemtodus with its central axis and lateral rays; Gegenbaur suggests that the archipterygium with its limb girdle has in fact been evolved o11t of such an arrangement of rays attached to a branchial arch and.that the limb itself is serially homologous with the gill septum.

In support of this view it is pointed out that branchial arch and limb girdle are each in early stages of development in the form of a continuous curved rod of cartilage; that this becomes usually segmented in the case of the branchial arch but that even ill the girdle it also shows traces of segmentation in some ancient fossil forms (Pleuracanthids, Acanthodians); that in some cases the perichondrium of the pectoral girdle is known to be innervated by that typical branchial nerve the Vagus; that in the lower forms the t7'apez'ius,o11e of the muscles associated with the fore-limb, is innervated 448 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

by the same nerve; and that connected with the ordinary branchial arches there are myotomic muscles as well as splanchnic, so that the basis already exists for a muscularization purely myotomic.

On.the other hand the objection is urged against the (legenbaur hypothesis that it involves a very great shifting of the pelvic ﬁn backwards from its assumedly original position at the hinder end of the branchial region. This objection need not be taken seriously in view of the extensive shiftings of the limbs which are deﬁnitely known to have taken place. Thus in Rays we commonly ﬁnd that the pectoral girdle has moved back to a position in relation to the segmentation of the body far posterior to the position which it occupies in Sharks: in Urodele Amphibians the hind-limb has taken up positions, as indicated by the position of the sacrum, varying between the 14th (ﬂriton palmatus) and 63rd vertebra (Amphvluma means) while in the Anura—where in accordance with the leaping habits it is advantageous to have the attachment of the hind-limb far forward——the sacrum has come to be as far forward as the 9th or even (II;/menoclmlrus) the 6th vertebra 1 : in l’l'esiosaurs and Birds a still more striking backward migration of the pectoral girdle with its attached limb has taken place (any. in the Swan as compared with A7'cltaeopte'rg/at through 14 or 15 segments): and ﬁnally in many Teleostean ﬁshes the pelvic ﬁns have become so shifted forwards along the sides of the body as to attain to an actually jugular position.

The fact that the limb girdles are embedded in the somatopleure while the branchial arches lie in the splanchnopleure has again been raised as a diﬂiculty in the way of accepting the Gegenbaur theory. The diﬁiculty is not so serious as it seems at ﬁrst sight. The chief obstacle in the way of a splanchnopleural organ becoming shifted outwards into the somatopleure is clearly the coelomic cavity—but in the branchial region this tends to be in great part obliterated. As regards blood-vessels, nerves, etc.——-these form by no means insuperable barriers to the change in position of skeletal elements. Such skeletal tissue may; as has already been indicated in Chapter V., spread past a blood-vessel or nerve and if it then becomes absorbed behind the obstacle there is brought about a complete transposition of the two structures. The criticism that the musculature of the limbs is myotomic in origin while that of the branchial arches is splanchnic is provided against by the mixed character of the muscularization of the branchial arches, taken in conjunction with the demonstration that in such a case replacement ofsplanchnic muscle by myotomic may take place (p. 217).

Rabl considers the metameric origin of the muscles etc. of the limb to be enough by itself to undermine the Gegenbaur hypothesis, but it is diﬁicult to see how the musculature could be otherwise than metameric in origin seeing that it has to be derived from the segmentally arranged myotomes.

1 Gadow, in Cambridge Natural Ilistory. VII EVOLUTIONARY ORIGIN OF LIMBS 449

The muscularization of the jugular pelvic ﬁn of Teleostean fishes is admittedly secondary: the limb rudiment becomes muscularizerl by the myotomes to which it happens to be opposite- at the time muscularization begins: but if this fact be admitted it is not open to us to deny the possibility of a similar process having taken place in the successive positions taken up by the pelvic limb in the course of the movements which it has undergone during phylogenetic evolution.

A further objection urged against the Gegenbaur hypothesis is that there have not been discovered, up to the present, any examples of the intermediate stages between gill-septum and limb which must have existed if this hypothesis be a true theory. This objection appears to be a valid one.

Again it is urged that in those Vertebrates which would appear, in this respect, to have retained most nearly the primitive condition (Cyelostomata, Elasmobranchii) the gill-septa are fixed firmly in position and are therefore not likely to become converted into motor organs, which must necessarily project beyond the surface and be freely movable. This objection like the last appears to be a valid one.

It will be apparent from the short sketch which has been given of the two rival views of the evolutionary origin of the limbs of Vertebrates that neither can be regarded as wholly satisfactory. However these hypotheses are old, as the science of Embryology goes. They were designed to ﬁt the data available at the time they were formulated and the great bulk of subsequent work upon this particular problem has consisted in the adducing of new facts which appear conveniently to ﬁt on to those already accumulated by the supporters of one view or the other. In a rapidly advancing science like Embryology however it is advisable to have from time to time a stocktaking of the facts of contemporary knowledge with the object of seeing whether the more extensive body of available facts suggests the same. working hypotheses as were suggested by the facts known at earlier periods or, as is always possible, something quite different. The putting this principle into practice is more conducive to progress and more stimulating to research than the mere accumulation of further facts to support or to confute the working hypotheses of earlier times.

THE EXTERNAL GILL HY1>o'rIn3s1s.——App1ying this principle to the problem of the evolutionary origin of the limbs one ﬁnds an important set of data which were not available to Gegenbaur or Balfour. In their day there was no proper appreciation of the importance of the fact that there existed in three of the less specialized groups of Vertebrates——Urodele Amphibians, Lung-ﬁshes and Crossopterygians——-those organs which have been described in Chapter III. under the name External Gills. The mode of development of these organs is now known in all three of the groups mentioned and the

VOL. 11 2 G 450 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

evidence appears to be conclusive that they are truly homologous throughout.

It has been shown that there is a tendency for the External Gills to become eliminated-—as e.g. in various Anurous Amphibians: it has been shown further that in some of the main groups of Vertebrates in which they do not occur. their disappearance may be accounted for by the evolution of a new physiological substitute-— the vascular surface of the yolk-sac.

Having regard to these facts and to the relatively archaic character of the groups in which they actually occur the conclusion is considered justiﬁable that such external gills are organs of high antiquity in the Vertebrate stem. Further, from their distribution upon the various arches it is inferred that in all probability an external gill was once present upon each visceral arch. But it has also been shown to be probable that the series of visceral cleft_s —-and therefore of visceral arches—was formerly more extensive, extending farther back along the body than it does in existing Vertebrates. It is therefore concluded that in an earlier phase of its evolution

A the phylum whose modern representatives we call Vertebrates was characterized by me. 204. -—'Left side of head the possession of a series of external gills fig?“ ‘:lp](:f":‘vh‘i’:h‘Rm? extending tailwards ‘beyond the limit days pl'eviou.x-ly, .1 piece of reached by the branchial region of existskin from the branchial region 'Verteb1~a,t,gs_

3fa;}t1;_f;fh¢;!'A ;?t*(

I}?;j,33m11l‘=j:119"1*;;f'; But such external gills are potential

organs of support—as shown by the __-"-P "' ‘”= ‘,“‘il""_"“' 3*”-" (“_""_°' “balancers” of Urodeles (see Fig. 88, p. 157) sltlc), e.g/.t, external gills (pa1a- . . .ee.,) me. «levvloped ——and also potentlal organs of moVement——— the implanted piece of skin; on, as shown by the well-developed muscula"1’°""“"‘“" ture by which they can be ﬂicked backwards. In other words these organs—— and these alone among the organs of the Vertebrata—posseSs the qualiﬁcations which have to be postulated for the evolutionary forerunner of the Vertebrate limb.

In view of such considerations as those just set forth the present writer believes the most plausible working hypothesis of the evolutionary origin of the limbs—having regard to our present-day knowledge-—to be that which interprets them as modiﬁed external gills, belonging to visceral arches farther back in the series than those forming the branchial arches of existing Vertebrates. The limb girdle would on this hypothesis, as on that of Gegenbaur, be interpreted as representing a branchial arch skeleton, the dllfeI‘('.‘.I1("(' from the Gegenbaur view having to do rather with the nature of the projecting limb itself. VII EVOLUTIONARY ORIGIN OF LIMBS 451

Fig. 200 illustrates how close may be the general resemblance between the earliest stages of development of limb and external gill. The same is brought out also by Fig. 204, representing part of a frog larva on which had been grafted a piece of skin from the gill-producing region of another larva. The external gills of the graft have gone on developing and are remarkably limb-like in appearance.‘

The External Gill Hypothesis as to the evolutionary origin of the limbs ﬁts in well with other facts which are n.ow known. In the breeding male Lepidosiren the hind limb regularly and the pectoral limb occasionally (Agar, 1908) take on temporarily the characters of an external gill both in structure and in function (Fig. 205). This remarkable fact——-otherwise a morphological 1nystery—becomes at once understandable on the hypothesis outlined above, as a simple “reversion” towards an ancestral condition. Fig. 205 brings out clearly a further peculiarity of these gill-like limbs-of the male Lepidosiren, namely that the respiratory outgrowths of the limb are

Flo. 205.--Lq2i4lo.w79-en., breeding male showing apparent rever.si«:m of hoth pectoral and pelvic liinhs to the branchial condition. (From a specimen in the Zoological Museum of the University of Glasgow.)

in the case of the pectoral limb attached to its ventral side, in the case of the pelvic to its dorsal side. But it has already been shown that the deﬁnitively ventral side of the pectoral limb is homologous with the deﬁnitively dorsal side of the pelvic limb——the difference in position lming due to the rotation ,in different directions undergone by the llllll.) rudiments in the course of their development. This reversed position of the respiratory ﬁlaments in the two sets of limbs clearly then ﬁts in exactly with the View that they are ancient morphological characteristics of the li.mb which have reappeared in the male Lepidosiren.

The striking resemblance between the pectoral girdle and the branchial arches in some of the more ancient Fishes again ﬁnds its explanation in the morphological identity of the two structures. It is now established that the swim-bladder of Fishes is morphologically a lung, and that the lung is to be regarded as at the least an extremely ancient organ in the Vertebrate phylum. This points to the probability that the early Vertebrates were creatures which clambered

-‘ Ii('.ll:l'(-‘.1l(_i4.‘. slmllltl also be made to Fig. 88 (p. 157) which brings out clearly the rcn1:.n'kahly limb-like eh:n'acter of the Urodele “ balancers.”

Budgctt (]9()‘l) mentions the case of an abnormal Protopterus larva which had failed to develop the pinnae upon one of its external gills. “This bare shaft so much resembled the pm-_-.toi-al limb that the larva appeared to have two pectoral limbs on one side.” 452 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

about amongst the vegetation of shallow water and we may suppose that in this early stage the limb is as of a crude styliform shape such as we see exempliﬁed in the metamorphosed external gill of the Urodele balancers, or in the actual limb of the larva of Lepidosiren.

On this hypothesis the ancestral styliform limb has pursued two divergent lines of evolution. The one of these is found in those Vertebrates which have developed along the lines of becoming specialized for eﬂicient swimming. Here it has become a ﬁn, an early stage of this evolution being represented by the crude paddle of Ueratodus. That this biserial archipterygial type does actually represent an extremely early type in the evolution of ﬁns seems to be demonstrated by two facts taken in conjunction with one another——

1. That this thick and clumsy organ represents functionally a relatively ineﬂicient type of swimming organ as compared with the thin ﬂat ﬁn of most existing Fishes, and 2. That palaeontology shows it to have been a widely distributed type of ﬁn in the early days of the evolution of the main groups of Fishes. It was in fact the predominant type of limb amongst ancient Elasmobranchs, Ganoids and Lung-ﬁshes.

Evidence is not entirely wanting to show how the Crossopterygian type of ﬁn on the one hand (as seen in the existing Polypterus) and the Actinopterygian type on the other (as seen in Amie and other Ganoids and Teleosts) may have been evolved out of the biserial archipterygial type. This evidence cannot be gone into here but so far as Crossopterygians are concerned the student should note the close resemblance of the pectoral ﬁn of the young Polypterus (Fig. 197, E) and of its supporting skeleton (Fig. 169, F) to the modiﬁed archipterygial ﬁn of the ancient Shark Plcumcanthus (Fig. 169, B).

Along the other line of evolution the styliform limb has given rise to the pentadactylc leg with its expanded foot and its characteristic jointing. It is of great interest in this connexion to watch the clumsy movements of a Lepidosiren larva and to note that the hind limb by which the creature pusllvs itself along becomes bent twice upon itself precisely in the way which would give rise to the ankle and knee-joints of one of the lower Tetrapoda. Occasionally the appearance is rendered still more suggestive by the tip ﬂattening out slightly into a foot-like expansion. The observer watching a Lepidosircn larva. performing such movements ﬁnds it difficult to avoid the suspicion that he is witnessing something very like What took place in the early stages of the evolution of the pentadactyle limb. Should this be the true history of the origin of that type of limb it would explain the unsatisfactory and wholly unconvincing results of the efforts of comparative anatomists to derive the skeletal elements of the pentadactylc limb from those of one or other type of ﬁn.

P VII ORIGIN OF LIMBS AND TAIL 453

Embryology offers no explanation of the number of digits being so generally ﬁve. The physiological advantage of the expanded foot being divided up into separate radiating digits is obvious, as is that of the double nature of the adjoining portion of the limb skeleton to facilitate rotation round the axis of the limb. There are also mechanical advantages in there being a central digit with one on each side of it. Possibly the presence of an additional digit outside of these is to be looked on as of the nature of simple reinforcement.

The modiﬁcation of the pectoral limb in the case of Birds for purposes of ﬂight is of great interest, but nothing is known as to the phylogenetic transition from Reptile to Bird in this connexion. To the present writer it seems most probable that the Birds were evolved out of aquatic Reptiles in which the fore-limb was specialized for use in swimming under water, after the manner of existing Penguins, and that the function of aerial ﬂight was evolved directly from such movement under water. On this hypothesis the more or less terrestrial habits of modern Birds would be regarded as a secondary acquirement. _

(4) EVOLUTIONARY ORIGIN or THE TAIL REe1oN.—It is characteristic of Vertebrates that the anus loses its practically terminal position and comes to be situated some distance forwards on the ventral side, the overhanging hinder end of the body forming the tail. This opens up a question of much morphological interestthough one to which we are not yet in a position to give any certain answer—as to the phylogenetic origin of the tail.

It seems clear that the tail arose in ancient aquatic Vertebrates as an adaptation to swimming and on the whole it seems most probable that it came into existence through the gradual migration forwards of the anus upon the ventral side. Such a shifting forwards of the anal opening from the binder end of the body is a familiar feature in many groups of invertebrates where it is associated as a rule with a tubicolous habit and has doubtless for its object the getting rid of excretory products which would otherwise be discharged into the depths of the tube, or burrow, or shell. In the Vertebrate the forward shifting of the anal opening has probably its physiological signiﬁcance in the increasing eﬂicieney of the tail as the main motive organ—the disappearance from it of the alimentary canal, and its surrounding splanchnocoele, being correlated with the conversion of the tissues on each side of the skeletal axis into a solid mass of muscle. Probability is added to this conjecture by the fact that we see what appears to be a continuation of the same process in the most efficient group of modern swimming Vertebrates (Teleostei) where in the most highly developed forms the alimentary canal and splanchnocovle come to be restricted to a relatively small region immediately behind the head, the remaining and main part of the body being entirely “ tail.”

In actual ontogeny the tail region is developed not by the withdrawal from it of gut and splanchnocoele but as an actual outgrowth, 454 EMBRYOLOGY OF THE LOWER VERTEBRATES CH. VII

the hind end of the body continuing to sprout out past and dorsal to the anal opening. It is of course conceivable that in phylogeny the tail arose similarly as an outgrowth of the body dorsal to the anus but this seems in every way less probable than the method of

evolution sketched above.

LITERATURE

Agar. Anat. Anzciger, xxxiii, 1908.

Balfour. Monograph on the Development of Elasmobranc-h Fishes. London, 1878. Budgett. Trans. Z001. Soc. Lond., xvi, 1901.

Caldwell. Jouru. Proc. Roy. Soc. New South Wales, xviii, 1884.

Dean, Bashford. Kupfl'crs Festscl1rif't. Jena, 1899.

Ekman. Morph. .lahrb., xlvii, 1913.

Gegenbaur. Untersuchungen zur vergl. Anat. dcr Wirlielfllierc, iii. Leipzig. 1872. Goodrich. Quart. Journ. Micr. Sci., l, 1906.

Kerr, Graham. Phil. 'l‘ran.s. Roy, Soc. London, B, oxcii, 1900.

Kerr, Graham. The Work of J. S. Blulgett. Ua.1nl)ridgv, 1907.

Kerr, Graham. Kcihcls Normentafcln, iii. Jena, 1909.

Rabl. Morph. Jaln‘l)., xix, 1893.

Semon. Zoologische Fo1'soln111gsreison, i. Jcna, 1893-1913.

Semon. Koibcls Normentafcln, iii. Jena, 1901*.

Taylor. Quart. Journ. Micr. Sr-i., lix, 1914. CHAPTER Vlll

Al)A‘PTA'l‘ION TO ENVIRONMENTAL CONDITIONS DURING EARLY STAGES OF DEVELOPMENT

I. PROTECTIVE ENVELOPES on THE ZY("}O'I‘E.——Tl1e Zygote or fertilized egg is in the Vertebrata as in other groups provided with protective envelopes. Of such we may recognize three fundamentally distinct types which are conveniently designated as primary, secondary and tertiary envelopes respectively. A primary envelope is a cuticular covering of the surface of the zygote: it is therefore produced by the living activity of the protoplasm of the macrogamete or zygote itself. A typical example of a primary envelope is the vitelline membrane which is formed on the surface of the Echinoderm egg in response to the act of fertilization. The “ vitelline membrane ” which covers the surface of the egg of a Bird is commonly looked on as a primary envelope.

A secondary envelope is one which is formed by the activity of the surrounding cells while the egg is still contained in its ovarian follicle. It may be cuticle-like in its nature or it may be composed of cells.

Finally tertiary envelopes are formed by the excretory activity of the oviducal lining, being deposited upon the surface of the egg as it travels down the oviduct. Of such a nature are the complicated protective envelopes which surround the egg of a Bird or Reptile, or the simpler jelly - like investment found in the case of most Amphibians.

Apart from tertiary envelopes the. most conspicuous envelope of the Vertebrate egg is usually what is known as the zona radiata or zona pellucida—-—the former name being given to it from the fact that it is pierced by numerous very ﬁne canals which give it a characteristic radiate appearance when seen in section. These ﬁne canals apparently contain protoplasmic bridges connecting the protoplasm of the egg with that of the follicle-cells which surround it while still in the ovary, and doubtless having for their function the passing in of food-material from the follicle-cells into the egg-cell.

The zona radiata is, as a rule, most conspicuous during early intra-ovarian stages while the egg is undergoing active growth during the storing up of yolk. Later it thins out and becomes less con 455 456 EMBRYOLOGY OF THE LOWER VERTEBRATES on.

spicuous. The zone radiata is usually looked upon as primary in

its nature but this is by no means settled and some competent authorities regard it as secondary. ‘ 4 Outside the zona radiata there may often be found a second envelope which does not show the perforations characteristic of the zona radiate: this also in the case of the large heavily yolked eggs becomes thinned out during the process of growth. Envelopes of this type are specially conspicuous in those Vertebrates 111 which there is no great development of tertiary envelopes secreted by the oviducal wall, ag. Teleostcan ﬁshes. In such cases the

Flu. 206.-—A, cluster of eggs of Btlc/lo.stom.a, attached together by the interlocking of their anchoring ‘filaments ; B, apical portion of the egg-shell. showing the anchoring ﬁlaments projecting from the middle of the separable “lid.” (Figure by Bashford Dean, from The (;’r.rni..lmTcig¢: .Vrttu-ru..l lI'[stm;z/.)

outer layer of the envelope, lying immediately external to the typical radiate layer, frequently shows characteristic modiﬁcations, consisting of closely packed villi or columns composed of cells which swell up and become strongly adhesive, serving to attach the eggs to one another or to a solid object (Roach-———I,euc7Jscus 9'-utvllus, Bleak-——Albu7~mzs, Herring—,—-C'lupea harengus). In the Actinopterygian Ganoids a similar condition is found. In Uemtodus this special outer layer is not found, there being here a tertiary envelope of jelly. ~ In I.cpz'nlosz”re7a._ and Protoptev-us the tertiary envelope is as a rule no longer formed, the eggs lying loose in the bottom of the burrow, though it is of interest to notice that in Lepidosiren the secretion of a jelly-like tertiary envelope round the eggs is still occasionally found as an individual variation. In Petromyzon, as in the \Teleosts alluded to above, a radiate envelope is found inside a villous one which becomes swollen up and sticky on the absorption VI ll EGG-EN V ELOPES 457

of Water. In the Myxinoids the egg is contained in a cl1aracteristic elongated shell provided at each pole with a group of stiff anchoring ﬁlaments ending each in a lobed umbrella-shaped expansion (Fig. 206). The piece of shell covering the germinal pole is marked off by a deep incision from the rest so as to form a lid which is forced ell’ at the time of hatching.

Whatever the true nature of the enve.lopes under discussion, whether primary or secondary, they already exist round the egg before fertilization takes place, and as the substance of the envelope is, as a rule, impenetrable by spermatozoa there necessarily exist one or more openings or micropyles through which the fertilizing sperniatozoon makes its way into the egg. In the Myxinoids one such micropyle is found in the middle of the lid, surrounded by the concentric circles of anchoring ﬁlaments. The presence of a micropyle in Lampreys and in Lung-ﬁshes is not delinitely established. In Lepiclomlren it has been observed that the envelope enclosing the coelomic, and therefore unfertilized. egg is thick and gelatinous while after fertilization it becomes dense and horny. Possibly therefore during the. ﬁrst-mentioned condition it is penetrable by the spermatozoa. In Te.leostean ﬁshes a mieropyle occurs at the apical pole, and so also with Actinoptcrygian Ganoids except that in the Sturgeons there exist a group of openings (5-13 in the Sterlet, according to Salensky) instead of a single. one.

Of the more complicated arrangements of tertiary envelopes found in Vertebrates no better example could be taken than those found in the case of the Fowl’s egg. These will be found described in Chap. X. In Birds in general the envelopes resemble those of the Fowl, differences occurring in details of relative size, shape, and colour of the shell. The “ egg ” (73.0. the zygote with its envelopes) appears to be largest relatively in Apiary/a; where it reaches about a quarter ot' the weight of the parent.

The shape of the shell is impressed upon it by the pressure of the oviducal wall and differences in shape are no doubt due to differences in the peristaltic contraction. Thus the strong contraction of the oviducal muscles which, acting on the headward side of the egg, propels it onward, if combined with comparatively slight contraction on the tailward side of the egg will naturally cause the egg to assume a more or less markedly conical shape-—the end of the egg directed towards the eloaca being broader than the other end. In some cases, as that of eggs laid on bare ledges of rock, this conical shape has probably had a deﬁnite natural selection value, in causing any rolling niovement of the egg to follow a strongly curved path. In other cases where there ' is less marked inequality of pressure on the two poles of the egg the shape is more regularly ellipsoidal.

The eggs of Birds being commonly exposed to light and to view they very often show a characteristic colouring, either throughout the thickness or merely in the outer layer of the shell. In very numerous cases the natural selection value of the colouring as a means of making the egg less conspicuous is obvious.

In Reptiles the tertiary envelopes resemble those of Birds though in many cases, as in various Lizards and Turtles, there is no deﬁnite rigid shell. On the other hand there may be a certain amount of lime deposited in the outer layers of the shell-membrane. The albumen varies in amount : in Sp}z,e7z0(lo72, it forms only a very thin layer (Dendy, 1899)

In Elasmobranch ﬁshes the egg is again enclosed in a layer of albumen and this in turn surrounded by a shell. The shell is of a horny consistency and is frequently rectangular and pillow-shaped. Characteristic dilfereiiees are found in different genera and species.

Thus in the Skates (Ram) each angle is prolonged so that the egg has an outline like that of a hand-barrow. In Sag/llz'mn (Fig. 207) the prolongations become long spirally coiled anchoring ﬁlaments: in Pmlstiurus two short’ prolongations occur at one end while the other end is simply rounded.

Fig. ‘207.——Egg of .\f'cyl/(um, held in position by its four l‘l.‘l.'~‘llI'. lilunu-uts being wound round a plant. (Fi_<_r1|re l»_\' Kopscli, from The (Jam.i;r£¢[_r/+3:.;\'u/um! //-1'.<:lo-ry.)

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Reference

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

Cite this page: Hill, M.A. (2024, April 16) Embryology Text-Book of Embryology 2-7 (1919). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Text-Book_of_Embryology_2-7_(1919)

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