Embryology - 26 Apr 2024 Expand to Translate
Google Translate - select your language from the list shown below (this will open a new external page)
العربية \| català \| 中文 \| 中國傳統的 \| français \| Deutsche \| עִברִית \| हिंदी \| bahasa Indonesia \| italiano \| 日本語 \| 한국어 \| မြန်မာ \| Pilipino \| Polskie \| português \| ਪੰਜਾਬੀ ਦੇ \| Română \| русский \| Español \| Swahili \| Svensk \| ไทย \| Türkçe \| اردو \| ייִדיש \| Tiếng Việt These external translations are automated and may not be accurate. (More? About Translations)

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

- Currently only early Draft Version of Text -

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

Chapter V The Skeleton

The skeletal tissues of the animal body show a variety which is at first sight quite bewildering. (Jloscr scrutiny however reveals certain general principles which are at Work. In a very restricted set of cases We see that the supporting structure consists of a row or red of cells which is rendered stiff through the individual cells being blown out or distended with ﬂuid. Such turgor of cells is a far less conspicuous feature in the animal kingdom than it is in the vegetable. lt is well seen in the axial row of endoderm cells which supports the tentacles of the Hydrozoa. In the Vertebrate it is seen in the notochord.

Far more usually the support is given by a deﬁnite supporting substance with such physical qualities as rigidity, tensile strength, elasticity, as may be required in the particular case.

These supporting substances of the animal body again show the greatest variety in their morphological nature but they may all be classed between two extremes——in one of which the supporting substance consists clearly of modiﬁed cells or portions of cells and in the other of dead intercellular substance. Examples of the former are seen in the rema.rkable phagocytic organs of nematode worms where an enormous cell becomes developed i11to an immensely complicated branched structure of stiff horny consistency upon the terminal twigs of which are perched innumerable minute blobs of phagocytic protoplasm. A good example of the second type is seen in the skeleton of ordinary coral——a mass of hard calcareous material lying clearly outside the limits of the living cells.

It is necessary to emphasize the fact, which is frequently lost sight of, that the ditl'erenees between these two types are superﬁcial rather than fundamental. They are merely the extremes of a series and are connected up by innumerable intermediate conditions. The skeleton of an Arthropod such as a Lobster is in the early stages of its development simply the stiffened and hardened outer layer of the cytoplasm of the ectoderm cells, while in its latest stage, immediately before it is shed, it has become a thick layer of dense chitinous and calciﬁed non-living substance lying outside the limits of the living protoplasm.

Non-living material “ secreted” by cells consists no less of modiﬁed cytoplasm, although here the cytoplasm so modiﬁed does not form a continuous mass and retain its original position in regard to the rest of the cell body. It arises commonly as isolated droplets or particles which may secondarily run together within the body of the cell or, without this happening to any obvious extent, are extruded from it, passing on to a free cell surface or into the intercellular matrix. The process can be followed by observation, naturally, only in cases where the secretion runs together into discrete droplets or particles sufﬁciently large to be visible under high powers of the microscope, as commonly happens in gland—cells. Far more frequently the extruded particles are so small———possibly molecularas completely to elude observation. Such is the case where the intercellular substance undergoes skeletal modiﬁcation: all that can be observed is simply a gradual transformation in the physical and chemical characters of the matrix, due in some cases to a gradual change in the metabolic activities of the_ cells which inhabit it, in others to the immigration into it of cell-colonists of a new type.

The supporting skeleton of the Vertebrate is an endoskeleton ;1 it is developed not on the outer‘ surface of the body but within its substance. In this it contrasts with the skeleton of the Arthropod or Mollusc which is exoskeletal—-con sisting of thickened and stiffened cuticle. In the case of the most ancient skeletal structure in the Vertebrate body———the notochord—-—the. stiff’ supporting character is due to the individual cells being distended by ﬂuid secreted in their interior but as a rule in other skeletal tissues the stiffriess is given not by the cells but by the intercellular matrix.

The Notochord and its Sheaths

A comparative study of the Vertebrate skeleton shows that it illustrates three phases of evolutionary progress (1) the notochordal phase, (2) the cartilaginous or chondral phase and (3) the bony or osseous phase. Of these the primitive is indisputably the first. It is a phase which is passed through during ontogeny in all Vertebrates and it remains permanent throughout life in Amphiowus.

The notochord is in its origin a rod of cells split oil‘ from the endoderin along its mid—dorsa1 line. This is seen in all the lower Vertebrates. In some of the more primitive members of the group the notochordal rudiment is for a time deeply grooved on its lower side, so as to form an inverted gutter along the middle of the enteric roof, and it may well be that this is to be regarded as the primitive mode of formation of the organ.

The notochord becomes constricted off as a cylindrical rod extending along the dorsal side of the alimentary canal from a point just behind the tip of the infundibulum to the tip of the tail. The individual cells develop in their cytoplasm ﬂuid vacuoles which increase in size and become conﬂuent until at last the cell takes the form of a comparatively thin layer of protoplasm surrounding an enormous vacuole and containing embedded in its substance at one point the nucleus. The turgescent condition of the cells inﬂated With fluid gives them the ﬁrmness which enables the notochord to carry out its function as a supporting structure.

It is regrettable that the term exoskeleton has crept into use by writers on Vertebrate anatomy for structures such as ﬁsh-scales. As will be seen later these are really endoskeletal, even the enamel being-developed on the inner surface of the epidermis.

The inﬂation of the cells with ﬂuid carries with it another result namely a great increase in size of the individual cells. This in turn causes a great increase in size of the notochord as a whole, showing itself particularly by increase in diameter but also by increase in length. '|‘he latter is not able to take place with perfect freedom and the result is that the individual cells tend to be compressed into the forin of transverse discs.

The notochordal rudiment at an early stage becomes covered by a thin, elastic, highly refracting, cutieular formation known as the primary sheath of the notochord (“ elastica ea:terna”). After the formation of this the superﬁcial layer of the notochord soon resumes its cuticle-forming activity but now in a somewhat modiﬁed form--a secondary or “ ﬁbrous ” sheath, thicker and more jelly-like in appearance, being produced internal to the primary sheath. In Cyclostomes and Sturgeons this secondary sheath remains throughout life without conspicuous change beyond increase of thickness a11d the assumption of a tough ﬁbrous character and is physiologically the most important part of the axial skeleton of the trunk region.

The superﬁcial layer of notochordal cells, lying in immediate contact with the inner surface of the secondary sheath, do not as a rule undergo the process of vacuolation which affects the inner cells. They remain as a layer of compact protoplasmic cells known as the notochordal epithelium.

In some Vertebrates (Dipnoi, Agar, 1906) a short stretch of notochord, from the tip backwards, degenerates within its primary sheath at an early stage, breaking up into loose mesenchyme. As the notochord behind the degenerated portion grows in length its front end is pushed forwards so as to re-occupy the vacated portion of primary sheath. The extent to which this process takes place throughout the Vertebrata in general, and also its meaning, are deserving of further enquiry.

Hypochord (Subnotochordal Rod)

In the anamniotic Vertebrates there is formed what is apparently an accessory notochord lying ventral to the true notochord and hence known as the Hypochord or Subnotochordal rod. This organ (see Gibson, 1910) arises after the notochord and in an entirely similar manner, '£.e. as a longitudinal rod of cells split off’ from the endoderm in the middorsal line and sometimes possessing a distinct groove along its lower surface facing the enteric cavity. On its surface it normally develops a primary sheath precisely like that of the notochord.

We may he sure, from its wide distribution amongst the more primitive Vertebrates (Lampreys, Elasmohranehs, Teleostomes, l)ipnoi, Amphibia) and the early stage of development at which it appears, that the hypochord is an organ of great antiquity in the Vertebrate stem, but we have no deﬁnite knowledge 01' its ancestral signiﬁcance. The fact that it does not occur in A'rnp/z/ioams has rendered possible the suggestion that it represents the longitudinal groove which in this animal runs along the mid-dorsal line of the pharyngeal wall. But this idea is negatived by the fact that the hypochord extends right back to the tail and is not merely a pharyngeal organ, a11d the probability seems to be that it has come down from a period in evolution long before the appearance of Avnplmloams. It is perhaps simplest to regard it merely’ as an accessory notochord.

Whereas the true notochord plays an important physiological role as the main part of the axial skeleton during early stages, and as the foundation for the vertebral column of later stages—the hypochord has no such justification for its persistence. It lasts only for a short time and eventually breaks up and completely disappears.

In the Aumiota there is no typical hypochord developed but it is possible that a thickening of the mid-dorsal endoderin which is frequently found in the pharyngeal region ((5.9. in the Second day Fowl embryo) may represent a last vestige of it.

Skeletal Developments of the Connective Tissue

Whereas the notochord is derived directly from the endoderm, the cartilaginous and bony components of the skeleton on the other hand are modiﬁcations of the mescnchyme or connective tissue, which forms a considerable proportion of the entire bulk of a typical vertebrate.

Connective tissue in its least specialized form may be seen in practically any late vertebrate embryo as a reticulum or spongework--—a syncytial framework—- of mucl1-branched cells, the processes of which are continuous from one cell to another, while the meshes are occupied by a clear ﬂuid or jelly-like matrix. Masses of this tissue form a kind of packing between and around the various epithelia of the body, while it also, in the form of discrete wandering cells, actually invades the epithelial tissues and colonizes them. Such immigrant elements are found for example between the muscle-ﬁbres, in the substance of the central nervous system, and even frequently between the epithelial cells of the epidermis.

The primitive or embryonic connective tissue undergoes gradual differentiation in accordance with the physiological role which it.has to play in diﬁ"erent localities. This differentiation ﬁnds expression in such superﬁcial features as shape and arrangement of the individual cells and more fundamentally in the peculiarities in metabolism which lead to its storing up particular substances in its protoplasm - pigment of chromatophores, fat of the cells of adipose tissue~—or again in the inﬂuence exerted by the metabolic activity of the cell upon the character of the matrix. This matrix is commonly described as intercellular, which is quite correct, b11t the important point is not the question whether it is inter- or intra-cellular but the fact that it is in iinmediate relation to, and under the inﬂuence of, the living protoplasm of the cell. The portion of matrix in contiguity with one of the irregularly shaped connective-tissue cells {is comparable with an intracellular vacuole the outer wall of which has thinned out and disappeared. The matrix has been l'or1ned by the breaking down of living substance and it seems merely a matter of phraseology whether we speak of it as modiﬁed protoplasm or as dead “ formed ” Inaterial.

The most familiar diﬁerentiation of the matrix of connective tissue consists in the development within it of thin tough ﬁbres, characterized by the physical property that they soften and dissolve, yielding gelatin, under the action of boiling water, and that they become further toughened by the action of tanning agents. These ﬁbres run indiscriminately in all directions or, in the more specialized conditions, are deﬁnitely orientated, as in the case of tendon where they are parallel and arranged in longitudinal strands, or of aponeuroses where they are arranged in thin layers, those of one layer perpendicular to those of the next. Other portions of the matrix take the form of elastic flbres———characterizcd by their elasticity, by their connexion together to form a network, by their being much less easily affected by boiling water, and by their not yielding gelatin.

The amount of matrix present ditfers greatly in different localities. It may be reduced to a very small amount-——to a mere demarcating line——between closely ﬁtting plate-like cells, as in the case of the endothelium covering the surface of a tendon, or it may be large in amount and comparatively rigid as in the case of the two great skeletal tissues cartilage and bone.

Cartilaginous or Chondral Skeleton

The cartilage is characterized by its cells taking on a rounded form and becoming separated by an abundant semitransparent,elastic, chondrin-containing matrix. The process of chondriﬁcation becomes apparent ﬁrst of all in the somewhat dense packing tissue (“ skeletogenous layer ”)‘ immediately surrounding the notochord. This connective tissue becomes_locally modified to form little blocks of cartilage known as the arch-elements (arcualia—Gadow, 1895), lying just outside the primary sheath and arranged in four longitudinal rows, two dorsal composed of the rudiments of the neural arches, two ventral»--the rudiments of the haemal arches. These arch-elements are apparently in the primitive condition duplicated in each segment, "Le. within the limits of a myotome or sclerotome there are situated two pairs of neural and two pairs of haemal arch-elemen ts.

1 The term prochondral is applied to the young cartilage in its early stages before the characteristic intercellular matrix makes its appearance.

There now takes place in two of the more primitive groups of Vertebrates——the Elasmobranchii (including the Holocephali) and the Dipnoi—--a remarkable process whereby the secondary sheath of the notoehord becomes converted into a sheath of cartilage. Certain of the cartilage cells in the arch rudiment take on an amoeboid character and burrowing their way through the primary sheath, apparently by the help of a digestive ferment, invade the secondary sheath (Fig. 145, me). Continuing their migration they become distributed equally throughout the whole substance of the secondary sheath, including those portions in the head region which will later on form part of the cranium. The immigrant cells ﬁnally settle down in the substance of the secondary sheath and the latter becomes a cylinder of cartilage. ‘

‘It is important, with an eye to the evolution of the vertebral column in Vertebrates higher in the scale, to bear in mind , that this invasion of the Secondary Sheath by ﬁn‘ Fm. 145. -- Part of a transverse section through a migrant cartilage cells Lepidosiren of stage 38, traversing one of the neural takes place at four points 91°“ "‘“““‘°“*'“~ in the transverse plane, rm, _notu(:1un:«lul epithelium; m.c, migrating ('m'l.il:1;.;'c celg; corresponding to the bases ii-1:Jli.'i§iiiiilgﬁgatiiihU’ "Mal mh’ ‘i’ ’""""“y ”'"”"'h’ 5’ of the four arch rudiments, and that this arrangement is repeated twice within the limits of one segment owing to the arch rudiments being so repeated. Consequently if we suppose the colonization of the secondary sheath to be restricted to the neighbourhood of the transverse plane in which the arch rudiments are situated the result would be the formation of two rings of cartilage within the limits of a single segment.

In the ease of Lung-ﬁshes and Holoeephali the chondriﬁed secondary sheath undergoes no further modiﬁcation but in typical Elasmobranchs it becomes divided up into segments, which form the centra or bodies of the vertebrae, in the manner to be described later on. In this process the originally uniformly ﬂexible notoehord with its sheaths becomes replaced physiologically by a series of rigid masses, ﬂexibility being given to the whole by the presence of the intervening joints. As this jointed condition of the vertebral column originated in evolution at a time when the longitudinal muscles of the body were already divided into myotomes, we may 294 EMBRYOLOG-Y OF THE LOWER VERTEBRATES "CH.

take it as probable, for obvious mechanical reasons, that the rigid skeletal masses arose in a position alternating with the muscle segments. The individual vertebral centra were in other words from the beginning iiitersegmcntal in position in relation to the general body iiietamerism. i In sketching out in somewhat greater detail the further development of the vertebral column the assumption will be again made use

of, as it was in dealing with the mesodcrm segments, that the trunk‘

region has in all probability departed least froin the primitive con dition, and the facts quoted will in the main be taken from this regioii of the body.

The student who goes on to peruse original memoirs will notice

' ' that this rule is by no

A. 3- _ A. 1.3- means always accepted. Seine

I

,1 l .——”' writers will he found to assume that the caudal region is more nearly primitive, and, in accordance with this assumption, to interpret the phenomena observed in the trunk vertebrae by those observed in the caudal, inFie. l46.—"'[\rr:-ingernent of dorsal arch-elements in Stead mice v6TSa"_ _ hinder trunk region of a 1’6C’I‘07n]/£.Il)')'l. larva 95 In l3l1lS COIIIIBXIOH 1l21I1115l'I mm. in length. (After Schauinsland, 1906.) [)3 borne jn f,ha,[',' the A, anterior, B, posterior neuralarcli-clenieiits;(hr, dorsal Vertebrate is above all I.‘.T..’3it‘f.l ?fEI$i§‘..5i.'.‘;‘i: ??..T‘3.f.lZ.'iIf‘r33E‘I§’3‘;’,§ll.:.1'$.13?-§T;i”"“' ‘Miss essentially a coelomate animal. No one doubts that whatever the common ancestor of the Vertebrates was like it was at least coeloinate. And most morphologists would admit further that the weight of evidence indicates that in this ancestor the splanchnocoele extended throughout the greater part of its length and that the existence of a considerable stretch of body towards the hind end devoid of sp1aii.chnoeoelc (13.6. a tail region) is secondary. But if the caudal region has in this way undergone profound secondary modification of its structure it is clear that it is not in this region of the body that we should expect to ﬁnd persisting primitive modes of development of the axial skeleton. It is now necessary to follow out the fate of the arcli-elements. As already mentioned the primitive arrangement of these appears to have been two pairs to each segment, above and below, so that corresponding with each myotome there were, on each side, two neural elements an anterior (A) and a posterior (B), and two liaemal elements an anterior (a) and a posterior (b).

Neural Arches

Apparently the most nearly primitive arrangement of the arches is that which occurs in the hinder trunk region of the Lamprey (Fig. 146). In this animal, as is well known, the dorsal (sensory) and ventral (motor) nerve-roots are still separate and are spaced out alternating with one another at approximately equal distances along the sides of the spinal cord. The dorsal arch elements alternate, in their turn, with the nerve-roots, so that there are, on each side, an anterior (A) and a posterior (B) neural archelement within the limits of a single myotome.‘ It should be noticed particularly that of these the anterior is situated between the sensory and the motor nerve-root belonging to the segment. This suggests a possible explanation of the later evolutionary history of these eartilages (A) which in the typical Fishes tend very usually

In writing these sections on the vertebral column much use has been made of Sclia.u1ns1and’s descriptions (1906) to which the student is referred for a more detailed account than is here possible.

Fro. 147.———A, arrangement of arch—elements in mid-trunk region of a Carcharias embryo

85 mm. in length; B, do. in anterior region of a Sturgeon (.~lm',oenser lmso) 36 mm. in length. (After Schauinsland, 1906.)

A, ante-rior neural arch-clement; B, posterior do. ; a, anterior haemal arch-eh-nu-nt; h, post:-xior do. ; d.o', sensory nu-rvo-root; v, blood-vessel ; wr, motor nerve-root.

to become reduced in size, even to the point of disappearance. It may be that this reduction in size is connected with the fact that in the Fishes, as indeed in all gnathostomatous vertebrates, the two nerve-roots have become approximated together to form a common sensori-motor spinal nerve. On the other hand this explanation would leave untouched the fact that a similar reduction in size may occur in the corresponding ventral or haemal arches.

The reduction in size of the “A” elements, which is of so frequent occurrence amongst the typical ﬁshes, is well shown in Figs. 147, A and B, which are based upon Schauinsland’s reconstructions. This marked reduction is by no means of universal occurrence. The two common Dog-ﬁsh-303/llmm and Acanthzas-— are familiar examples of ﬁshes in which the “A ” elements

1 In the anterior trunk region the arrangement is apt to be morliﬁed—the intersegmental vessel, which forms the anterior limit of the segment, coming to lie on the tailward side of the A cartilage of that segment (Schauinsland).

(“ intercalary pieces,” “ interdorsals ”) remain nearly as Well developed in the adult as the “B” elements} .

In Lung-ﬁshes (here and there) and in Urodele aiiiphibiaiis the “A” pieces can still be recognized (cf. Fig. 148); they haye also been observed in the embryos of various Reptiles. _In this case they usually lose their individuality at an early period, becoming completely merged in the deﬁnitive neural arch formed by the “ B ” elements lying next to them on their headward side, but in some cases, ag. in the tail region of Lacesrta, they have been found 130 persist as discrete structures even in the adult, forming a vestigial second neural arch behind the main arch.

The neural elements become prolonged dorsally and meet so as to form a complete neural arch and the apex of this becomes prolonged as an unpaired piece in the mesial plane to form the neural spine. The complete neural arch formed in this way frequently becomes segmented up into separate pieces of cartilage. The arcualia in such cases become each divided into a larger basal (basid0rsal—B, interdorsa.l—A,Ga dew) and a smaller apical (supradorsal) portion. The spine may segment into three superimposed rod-like portions.

HAEMAL ARCHES. —— In the

FIG. 148.—Arrangeineiit of arch-eleineiits ‘ 1 ' - 3 in anterior caudal region of a Siredoii 50 Cyc Ostonles typlcal haenlal {Hobbs

mm. in length. (After Schauinsland, are , absent’ although possibly 1906.) vestiges of them are represented

Reference letters as in Fig. 147. _ by a continuous ridge of cartilage

occurring in the tail region of

Petromyzon where the neural arches have also been reduced to a similar continuous ridge (Schneider).

Of haemal arch elements there were apparently primitively two pairs to a segment just as in the case of the neural arches. This seems to be clearly indicated by Callorhynchas (Fig. 149). It is also Well shown in the young Sturgeon (Fig. 147, B) where the anterior element (a) in each segment has undergone reduction in size exactly as was the case with the corresponding neural element (A). A similar condition is found in many Elasmobranchs, though not in all, the “ a ” elements being in some cases apparently completely absent.

. 1 The examination of one of these Dog-ﬁshes brings out another point of general importance namely that the arch-element as it increases in size is apt to spread round a nerve-root in its neighbourhood. The result is that in the adult the nerveroots may pass out, not between the arch—elements, but through them. The lesson to be learnt from this is that the topographical relatiop of skeletal elements to nervel3lI‘ll!1l{s is not to be taken as infallible evidence as to the primitive situation of such e ements.

In various Fishes, for example Laemargus and Amvla. ‘(also in some Amphibia, see Fig. 153, B), the haemal arch-element in the trunk region segments into two pieces—one of which carries the rib and may become shifted dorsally, while the other becomes displaced in a ventral direction. The ventral pieces come to form projections downwards from the centrum of the vertebra on each side of the aorta and have been termed “aortic supports." They may be termed haemal processes as they appear to be homologous with the knob-like structures bearing this name which are to be

seen in the caudal region of ag. Laemaw-gas, projecting inwards from.

the haemal arch into the tendinous septum which underlies the caudal aorta.

In the caudal region the haemal arch—elements are commonly much longer than in the trunk. They bend round to meet one another and are prolonged into a haemal spine. These features are associated with the extension of the body in a dorsal and ventral direction correlated with the use of this region of the body for the purposes of movement.

Towards the head end of the series it not uncommonly happens in Cartilaginous ﬁshes that the haemal arch - element becomes ,1 .= -.w - -. broadened out over the surface aéad "M zidb. ab £1. 5of the notochord indicating the beginnlngs of the evolutmn of F110 cm. embryo of Uallorhynchusa few segPerlchordal centra (593 below) ments posterior to the hind end of the This is well shown by Callorhym skull. (After Schauinsland, 1906.) chi”/3 Where iI10iPi9Ilt Reference letters as in Fig. 147. centra are distinctly seen, formed by the much-enlarged and fused haemal arch-elements (a and b).

In the air-breathing vertebrates there are no longer double sets of complete haemal arch -elements but a distinct trace of this condition is seen in such a Urodele Amphibian as Siredon (see Fig. 148) where a large perforation through the haemal arch element, traversed by the intersegmental blood-vessel, betokens its double origin.

A characteristic feature of the Amniota is that the haemal arch (the cartilaginous forerunner of the “chevron -bone”) tends to become displaced forwards so as to assume an intervertebral position or even [to become fused with the vertebra lying in front (AnguisGoette). ' '

VERTEBRAL CEN'1‘RA.—Except in the case of Cyclostomes, Holocephali and ‘Lung-ﬁshes, the elastic notochord becomes replaced physiologically during development by the series of vertebral centra. In the various subdivisions of the Vertebrata we ﬁnd two distinct methods by which vertebral centra are produced (1) by the segmentation of the cartilaginous secondary sheath (sheath centra; chorda centra——Gradow) and (2) by the enlargement of the bases of the arch—elements which grow round the notochord and give rise to centre outside the primary sheath——(perichordal centra; arch eentra———G-adow). ’

S1-IEATH CENTRA are seen in Elasmobranchs. In the region which. will develop into a eentrum the chondriﬁed secondary sheath becomes thickened so as to bulge inwards and constrict the notochord (Fig. 150). A more deeply staining “ middle zone” soon becomes distinguishable in this thickened part of the secondary sheath (Fig. 150, me) having a shape something like that of a dice—box, its central part lying much nearer to the axis of’ the

Flu. 150.-——Part of sagittal section through the secondary sheath of a Scyllium of 61 mm. total length showing an early stage in the development of a centrum. (After 0. Rabl, 1893.),

'i.2, inner zone: m..z, middle zone; o.z, outer zone; N, notochord; sl, pi-imary sheath.

notochord than do its two extremities. This middle zone becomes the main part of the Wall of the amphicoelous centrum, its substance becoming usually strengthened by the calciﬁcation of its intercellular matrix. _

The inner zone (Fig. 150, 73.2.’) may grow in thickness so as to cause greater and greater constriction of the notochord. This process attains to its maximum in the Skates where it extends inwards to the axis and causes the formation of thick septa which divide the notochord into isolated intervertebral fragments. More usually however the inner zone does not undergo this increase, it tends to become absorbed at each end and forms simply a ring of cartilage in the centre of the vertebra.

The outer zone in many Elasmobranchs becomes calciﬁed in parts: the calciﬁed regions often showing a regular arrangement ag. concentric cylindrical shells or radiating septa.

PERICHORDAL CENTRA.

AS a matter of fact the purely chordacentrous condition is merely a temporary one in the Elasmobranch, as in later stages of development the sheath centra become surV VERTEBRAL CENTRA 299

rounded by a layer of cartilage provided by the bases of the archelements, which spread over the surface of the sheath centrum (Goette, 1878). This outer layer of cartilage may undergo calciﬁcation later and become continuous anteriorly and posteriorly with the edge of the calciﬁed middle zone. Meanwhile the primary sheath of the notochord is liable to disappear so that there is no obvious clue left to the independent origin of the portions of the vertebral body derived from the sheath and the arch-elements respectively.

In the course of the further evolution of the vertebral body this outer layer of perichordal origin, which in an ordinary Elasmobranch like S’cyll'iwm or Acwntlmlas serves merely to reinforce the sheathccntrum, is destined to become all-important while the sheath portion is destined to disappear. A step in this direction has already been made by the Rays where (Torperlo-——Schauinsland) the secondary sheath remains thin and where the primary sheath soon disappears so as to bring about complete fusion between the thin sheath layer of cartilage and the much thicker external mass derived from the arches.

In those Teleostomatous ﬁshes which possess centra the spreading of the bases of the carrtt'la.gt'ncus arch-elements round the notochord is commonly not marked: possibly this is correlated with the precocious development of the bony centrum.

In the Urodele Amphibians the vertebral bodies develop in the manner illustrated by Fig. 151. A series of ring-shaped cartilages (“intervertebral cartilage,” Gegenbaur: Fig. 151, A, 0) make their appearance round the notochord in mid-segmental positions. These rings gradually extend for a considerable distance in a headward and tailward direction, immediately superﬁcial to the notochordal sheath, and between it and a thin, tubular, segmented sheath of bone (non-cellular) which has already made its appearance (Fig. 151, A and B, b). '1‘he intervertebral cartilage also increases considerably in thickness, bulging out between the adjacent somewhat expanded ends of the bony tubes already mentioned. In various of the more primitive Urodeles the vertebral bodies practically remain in this condition, ﬂexibility being given to the vertebral column as a whole by the intervertebral cartilages interposed between the rigid bony segments. In the more highly developed Urodeles on the other hand there is a tendency to form an opisthocoelous joint, ale. a joint concave on its tailward and convex on its headward side (Fig. 151, C). This may ﬁnd expression merely in a softening of the cartilage along what would be the surface of the joint, or a layer of the cartilage may be liquiﬁed so that the intervertebral cartilage is completely divided across into a smaller concave anterior part and a larger convex posterior part ﬁtting together by regular articular surfaces, forming in other words a completely developed joint.

1 In Petromyzon a few of the most anterior neural arches (e. g. 4th and 5th in an old specimen of 1’. _/luxwiateilis) have expanded bases which spread ventrally almost completely round the notochord so as to form a kind of arch centrum which carries rib-like projections laterally (schauinsland, 1906). 300 EMBRYOLOGY OF THE LOWER V]+]RTEBRATES en.

Fm. 151.-—Illustrating the development of the vertebral centre in Urodeles as seen in horizontal su-ctions. (Based on ﬁgures by Schauinsland, 1906.)

A, .S'u.lwmu-ml-ru, :32 mm. ; B, '.rc_:d.un, :30 mm. ; C, T: -itu-n, 16 mm.; In, home; r, c:u-t.il:1,«,:e; «-I, connective ti.~4s1u- ; -m, myotume; N, notochord; mr, nutoclun-«Iul L-:u't..iI.-:«_-e-. ; r. 1»1«;o«l-wssel. V VERTEBRAL CENTRA 301

The notochord becomes more or less constricted by the ingrowth of the intervertebral or joint cartilage which pushes the sheath in front of it. Besides this constriction of the whole notochord with its sheath the substance of the notochord becomes eventually, sometimes at a relatively late stage of development, interrupted by the development of 'int'ravertel)ral cartilage which may form a complete cartilaginous partition across the notochord at about the middle of each vertebra (Fig. 151, B, no). The origin of this cartilage is disputed. Some (Lwoff, Zykoff, Gadow) derive it from immigrant cartilage cells which have penetrated through the notochordal sheath from outside, while others (Gegenbaur, Field, Elmer, Klaatsch, Schauinsland) believe it to originate by the metamorphosis of actual notochordal cells, probably cells of the notoehordal epithelium. In spite of a possibly greater volume of evidence supporting the latter View it is difficult to avoid the impression that the former has in its favour the balance of a priori probability.

The Reptiles are commonly regarded as the least specialized of the three subdivisions of the Amniota and it may therefore be convenient to let them form the basis of our description. Schauinsland’s work may be referred to for more minute detail.

The sclerotome tissue grows actively and comes to be specially concentrated immediately round the notochord to form the perichordal layer. .This layer is at ﬁrst———in accordance with its origin from the sclerotomes——segmented (Fig. 152, A, sol) but the original segmentation soon disappears so that it forms a perfectly continuous investment to the notochord. A secondary segmentation now becomes visible in as much as the perichordal layer is decidedly thicker in a position corresponding to the middle of each original segment. These thickenings mark it off into a series of reel-shaped pieces each of which is a primary vertebral body (Fig. 152, B and C, pub). lt will be understood that the hinder half of each primary vertebral body is derived from the front half of a sclerotome while the front half of the same primary vertebral body is derived from the posterior half of the next sclerotome in a headward direction.

In other words each primary vertebral body is formed from the adjoining halves of two original segments, and as a result of this the primary vertebral bodies necessarily alternate in position with the myotomes, each myotome running from about the level of the middle of one primary vertebral body to a level about the middle of the next in the series (Fig. 152, B).

The portions of the sclerotomes lying outside the perichordal layer undergo fusion also. This outer part of the sclerotome bulges out between the myotomes while it extends dorsalwards so as to arch over the spinal cord. It is in the wall of the tunnel so formed that the neural arch-elements make their appearance while the sclerotome tissue ventral to them takes part in the -formation of the body of the deﬁnitive vertebra. The superﬁcial part of the vertebral body arising in this way from sclerotome tissue outside the perichordal layer 302 l4‘.MBRYOL()GY OF THE LOWER VERTEBRATES CII.

(Fig. 152, O, S) is best developed laterally (Sphenoalon) though it extends as a thinner layer over both the dorsal and ventral sides of the pcricliordal layer. Eventually chcndriﬁcal.i0n takes place and the vertebral body, derived partly from periclumlal and partly from sclerotome tissue lying outside and continuous with the neural arch portion, becomes converted into a mass ol' cartilage in which the only clue to its compound origin is the scmiewhat llattened shape of the cartilage cells in the inner part derived from the perichordal layer (Fig. 152, C, p.'v.b).

During the development of the vertebral centre the notochord becomes constricted. across much as in Urodeles. A complete septum of notochordal cartilage is Formed across the middle of each

FIG. 152.-—--Diagram illustrating the mode of development of the vertebral centra in a Reptile as seen in horizontal sections. (Based mainly on Schauinsland’s ﬁgures of

' S1‘;/I-emu/U-H, 1906.)

my, myotomo-; ,.\', iml()l'lH))'d; -}:.r.h, pI'im:u'_\' \'o-rlr-In-al |md_\'; N, Hllpl-‘1"ll(!l:ll pm-1:ir,m of Ct-‘l)l.)‘llln arising outsirlv ]"‘l‘l('liHl‘4l.‘ll lay:-r: S-.'/, -“[5119-1is"il11!«f‘1i0l1; -‘v'/, .~‘vla-ro1..unn-; r, blood-vessel. In cmnpm-in‘: the segim-nt.-ii re-I.-ition.s' of A and 13 the ii1i:.«-rse;.-nu-ntal l)lOU(l-\'u..s's|el8 (4?) form iiseful ];mdm;u-k,~.;,

vertebra in Sp/aenodon and in the Lacertilia. In the ordinary Lizards this appears to arise as a ring-shaped ingrowth of carti.lagc which constricts the notochord, pushing the primary sheath in front of it (Gadow, 1897) while in Spltenodon and also in the Geckos the cartilage makes its appearance i.nterna1 to the notochordal sheath (Howes and Swinnerton, 1901). It may be suspected that in the latter case immigrant cartilage cells have made their way through the notochordal sheath though this has not so far been demonstrated.

Ribs

The ribs are long cartilaginous projections from the vertebrae which run outwards and ventrally in the substance of the myosepta and serve to support and strengthen the wall of the splanchnocoele. As Goette (1878, 1879). ﬁrst showed, there are included under the name “ribs ” two morphologically different structures, which may be distinguished by the names dorsal or upper ribs and ventral or lower ribs. '

In Polypterus both sets of ribs are well developcd—-—the dorsal ones larger towards the head, the ventral larger towards the tail. In other vertebrates the rule is that only one set is developed, though the other may be represented by more or less distinct rudiments or vestiges. Thus in Actinopterygian ganoids, Teleosts and Dipnoans the ribs are ventral ribs while in Elasmobranchs, Amphibians and Amniotes they are dorsal ribs.‘

Both types are associated with the niyosepta but whereas the dorsal ribs lie at the level of the horizontal septum which divides the lateral musculature into a dorsal and a ventral half, the ventral ribs, on the other hand, lie along the peritoneal edge of the myoseptum where it abuts on the lining of the splanehnocoele.

Probably both sets of ribs are to be interpreted morphologically as outgrowths from the vertebrae and the balance of evidence appears to favour the view that both are fundamentally outgrowths from the series of haemal arch-elements.

Ventral Ribs.——-This is clearly the case with the ventral ribs which are simply the ventral prolongations of the haemal archelements, frequently jointed off from the basal stump of the arch (transverse process) by the conversion of a thin layer of the cartilage into ﬁbrillar material. In the skeleton of a Lung-ﬁsh, a Crossopterygian, or an Actinopterygian the ribs are seen to form a perfectly continuous series with the haemal arches of the tail region.

Dorsal Ribs.——The nature of the dorsal ribs tends to be obscured by the fact that their point of attachment to the vertebra shows much variation rag. they may appear to arise not from the haemal but from the neural arch. That we have to do here with a secondary shifting in a dorsal direction is indicated by various considerations. Amongst the Rays it can sometimes be seen that the ribs towards the head end of the series become more and more displaced dorsally, so that they come to project from the neural arch. Then it will be remembered that in various ﬁshes the haemal arch-element becomes divided into a ventral part (haemal process) and a dorsal part which latter carries the rib and may undergo a considerable displacement in a dorsal direction.

In Urodele Amphibians Goeppert has shown that the apparent attachment of the rib to the neural arch has come about in a somewhat complicated fashion as illustrated by Fig. 153. The most nearly primitive condition is that shown in the larva of such a perennibranchiate form as Necturus (Fig. 153, A). Here the haemal arch-element (h.a) sends oil‘ a strong outgrowth (r.b), the “ribbearer,” which passes in a dorsal direction closely applied to the surface of the neural arch, from which however it is marked off by a thin fenestrated layer of bone (b). It will be seen from the diagram that the bases of the neural and haemal arches and the base of the rib-bearer enclose a space through which runs the vertebral artery (am). The haemal arch-element passes horizontally outwards beyond the base of the rib-bearer and the rib itself forms merely a prolongation of the haemal arch-element, becoming segmented ell’ from its proximal portion (“ transverse process”) by the dc ve1opm.eut of an intcrealary zone of ﬁbrillar joint tissue. A little way out from its base the rib grows out “into a projection which is directed dorsally and fqtowards the median plane. This dorsal process is prolonged into a ligament which is attached at its end to a mass of bony tissue developed on the outer side of the rib~bearer and indicated in the diagram by the diagonal shading.

1 Distinct traces of dorsal ribs occur in various Teleosts, e.g. Salmonids and Clupeids. The numerous little bones found in the myosepta. of various Teleosts in addition to the true ribs are probably to be looked on as independent and secondarily developed “ tendon bones.

In the larva of Salama/n.d'ra, macalosa the condition is found which is illustrated by Fig. 153, B. The most important difference from the condition seen in Nectaras is that the basal part of the haem.al arch-element has become greatly reduced, and is new attached to the notoehordal sheath FIG 153 ——Illustrating the attachment merely- by a thin thread of bone.

cl‘ rib. to vertebra in the Urodela The nb'bearer grows out from the according to Goeppert (1896). haemal arch-element as before but it A, trunk vertebra of Ncvtnrus larva; B, iS.Sh0rter.a'nd is lnore completely fused trunk vertebra of Su.Imu.¢.m.d1'a. maculosa. Wllill lille neural arch. The dorsal larva; C, trunk vertebra of ’1'm'ton.alpesm'.s process of the has increased in larva. b,:bone; h..a, haomal arch-element; ,,_,,.., hnema, pmc,.___,,,; N, ,,0mc,,o,d; M,’ strengtlrand now extends right to the neural arch: 9', rib: r.b. rib-bearer; t, dorsal end of the rib-bearer and is

dorsal rocess ofrib: 'v.a., vertebralarter . . ' ' ,..EI2.°.:.°“£§£2.‘;“’ °*‘ A =39 §§JJ‘i§s3$Z§“§§ J£v3§;.E°d§3%lJl‘§a§é3

character with a practically equally strong dorsal and ventral attachment through the substance of the rib-bearer to the neural arch.

Finally in the larva of Triton alpestmls the condition is found which is illustrated by Fig. 153, C. The original basal part of the haemal arch-element which lay ventral to the vertebral artery has disappeared, so far as cartilage is concerned, its place being taken by a thin thread of bone. The rib-bearer is shorter and stouter than in Salcmnandra and its fusion with the neural arch still more complete» The double-headed rib has all the appearance now of simply articulating with a massive projection of the outer side of the neural arch: its original connexion with the haemal arch would never be suspected.

The question naturally arises whether in other Amphibians in which the transverse process and rib projects from the neural arch, the dorsalward shifting has come about in the same manner as is apparently the case in Urodeles. The probabilities appear to be against this. In the remaining two groups of Amphibia—the Anura and the Gymnophiona-——the transverse process, though it springs from the neural arch, lies still ventral to the vertebral artery, which suggests that there has taken place here a simple shifting dorsalward of the whole of the haemal arch carrying the rib, including its basal portion.

In the case of the Amniota, Schone (1902) has carefully investigated the development of Reptiles’ and has failed to ﬁnd anything corresponding to the rib-bearer of Urodeles. In all probability here as in Anura there has taken place a simple dorsal movement of the rib and transverse process.

The Amniote rib appears to arise generally in continuity with the anterior half vertebra. (a) 73.6. from material derived from the posterior half of the sclerotome. In the case of Sp/wnoclon (Schauinsland) the sacral and usually the caudal ribs, on the other hand, appear to contain material derived from both halves of the vertebra, the ribs being in these regions much broader than they are elsewhere and marked by a longitudinal groove indicating their double origin. In the last vertebrae of the tail these may give rise to two separate transverse processes attached to each side of

the vertebra tipped each one by a small rib-rudiment. The uncinate processes on the ribs of certain Reptiles and Birds

arise as independent centres of chondriﬁcation. They may later on ossify and fuse completely with the rib (most Birds) or they may never show complete fusion (Apteryw, Sphenodon). In Sp/Lenodon they become simply calciﬁed without undergoing true ossiﬁcation (Schauinsland).

STERNUM.——'.l‘he sternum of the Amniota arises typically by the fusion together of the ventral ends of a number of the anterior ribrudiments into a continuous plate on each side. The two lateral plates so formed undergo fusion across the mesial plane to form the deﬁnitive unpaired sternum, a plate of cartilage still continuous with the ribs. Eventually the sternum becomes segmented off from the ribs and may become calciﬁed by the deposition of limy particles in the intcrcellular matrix (Reptiles) or replaced by bone (Birds).

In Amphibia also the sternum arises by the fusion together of two longitudinal bands of cartilage but no connexion can be traced between these and the ribs. This peculiarity, as compared with the Amniota, is apparently to be correlated with the comparatively short extension of the ribs in a ventral direction which is characteristic of this group of Vertebrates. In the Fishes the sternum has not yet made its appearance.

Skull

The skull is a mass of condensed and strengthened mesenchyme serving essentially to support and protect the organs of the head. It protects the brain and sense organs: and it forms a support and framework for the masticatory and other apparatus connected with the mouth and pharynx. ln correlation with this its characteristics in detail are secondary to characters of the brain and other organs.

The skelctonization of the mesenchyme does not take place continuously but commences in irregular patches which gradually spread and eventually join together. Though there is frequently considerable agreement between different Vertebrates in the position of the centres of skeleton formation in the head there are in other

.cases equally well-marked variations between forms known to be

phylogenctically closely related. It is as a rule impossible to say deﬁnitely whether or not the first appearance of skeleton at particular points is of phylogenetic signiﬁcance or is on the other hand related merely to existing arrangements of the adult.

Under the circumstances all that will be attempted here is a short sketch of the general features of cranial development without entering at all into minute detail. For a full and detailed description reference should be made to the admirable work of Gaupp (1906).

As has already been indicated there is a marked tendency for the arch - elements to undergo fusion towards the head end, the axial skeleton being necessarily rigid instead of ﬂexible in the brain region. Eventually towards the front end of the series both neural arches and vertebral centra become completely fused together to form part of the skull.

The skull consists in its simplest form primarily of a chondrocranium———a trough of cartilage, the cavity of which is occupied by the brain and more or less open on -its dorsal side. Somewhere about the middle of the ﬂoor of the chondrocranium there exists a recess in which rests the infundibulum of the brain, and the portion of cranial ﬂoor lying behind this is distinguished by having the notochord embedded in it——this organ having its anterior limit just behind the tip of the infundibulum. We are thus brought into touch with a deep-seated distinction between the posterior or epichordal (chorda1——K6lliker) region of the cranium and the anterior or prechordal (Kolliker). We are probably justified in regarding the epichordal region of the cranium as being morphologically a metamorphosed portion of vertebral column in which the processes of ,fusion, already indicated as frequently occurring in the anterior region, have attained to their maximum. As will be explained later the process of incorporation of a few vertebrae (the number varying in different groups) into the binder end-"of the cranium can still be observed in ontogeny and it is probable that during the contemporary evolution of some of the lower Vertebrates (Elasmobranchs, Sturgeons) there is still going on a process of spreading backwards of the hinder limits of the skull with the incorporation into it of additional vertebrae.

As regards the evolutionary origin of the prechordal part of the cranium we have so far no clue.

The primary cartilaginous cranium does not remain by itself in any Vertebrate. There become inseparably fused with it the cartilaginous capsules Which surround and protect the nose (olfactory capsule) and the ear (otic or auditory capsule). Cartilage may also develop in the sclerotic of the eyeball but owing to mobility of the eyeball being necessitated by its having to be turned towards the direction from which impressions are received, the cartilage in this case does not undergo fusion with the chondrocranium.

’l‘herc are also associated with the cranium, and more or less closely connected with it, the series of hoop-like cartilages of the visceral arches‘ and ﬁnally in many of the subdivisions of the Vertebrata. important bony elements become added on to the chondrocranium. The description of the development of the skull will therefore fall naturally into three sections: (1) The Chondrocranium including the sense capsules, (2) The Visceral Arches, and (3) The Bony Skull.

THE CHONDROCRANIUM

The chondrocranium shows many differences in detail in the various groups of Vertebrates. The epichordal portion commonly makes its appearance as a pair of rods of cartilage——the parachordal cartilages—~—lying one on each side of the front part of the notochord. The prechordal portion similarly takes its origin in a pair of trabeculae which lie dorsal to the buccal cavity on each side of the infundibulum. Important differences are seen in‘the relations of these primary cranial cartilages in different members of the Vertebrata. Thus in Elasmobranchs, Ganoids, Teleosts, Reptiles and Birds the trabeculae are at ﬁrst quite isolated from the parachordals while in‘ Lampreys, Amphibians and Lungﬁshes they are continued at their hind ends into the parachordals (Sewertzoff).

Again in many Vertebrates, apparently in correlation with the great development of the eyes in early developmental stages, the cranial cavity no longer extends forwards between the eyes. Its Walls have come together to form an interorbital septum and foreshadowing this, the trabeculae are closely approximated or even fused in the median line. Gaupp applies the term tropibasic to such a type of cranium and contrasts it with the platybasic type in which the cranial cavity still extends forwards between the eyes and the trabcculae retain their primitive parallel position some distance apart. The skull in aetinopterygian Ganoids, Teleosts, Anmiotes and certain Elasmobranchs develops after the tropibasic type while in Amphibians, Lung-ﬁshes, Crossopterygians and some Elasmobranchs it retains the platybasic condition.

1 In the neighbourhood of the margin of the mouth there frequently develop in the lower Vertebrates (Fishes and Amphibians) isolated pieces of cartilage (labial cartilages). These are sometimes termed the precranial skeleton, and various speculations have been made as to their possible evolutionary signiﬁcance. Up to the present there appears to be no convincing evidence that they are other than mere secondary developments and consequently they will not be referred to further in this book.

As the platybasic type of cranium is admittedly the more primitive we shall deal with it first and will take as our example the cranium_ of the Lung-ﬁshes Lep'icl0si7'en and Protupterus as described by Agar 1906 .

( l.)llJVl1‘.|.(‘)PMl1lN'I‘01l' OHommocRAN1uM IN Lzrpmoszmav AND PROTOP'rImUs.——'1‘lie first rudiments of cranium become apparent about stage 31 in the form cl‘ a longitudinally situated condensation of mesenchyme——-the rudiment of the trabecula «lying upon each side beneath the thalamencephalon and mesencephalon. At its front end the trabeeula rapidly extends dorsalwards to form a vertical plate of prochondral tissue lying against the side wall of the thalamencephalon, and terminating in front against the optic nerve. The dorsal portion of this plate, just internal to the deep ophthalmic nerve, is the orbito-temporal process (Fig. 155, A, o.t). From the outer surface of the trabecula, just in front of the main portion of the trigeminal nerve, there projects outwards a horizontal shelf of cartilage (Fig. 155, A, gxr). This is the rudiment of the portion of cranium which contains the ganglia belonging to the Trigeminal and Facial nerves (Gasserian recess, Bridge). The cranial rudiment becomes prolonged backwards, the backward prolongation representing the parachordal cartilage of meroblastic Vertebrates.

This parachordal rudiment lies on each side of the front portion of the notoehord but, unlike what is more usual in other Vertebrates, it is separated from the notoehord by a considerable space (Fig. 154, A). The cranial rudiment so far described gradually becomes chondriﬁed. About this time there appears a condensation of mesenchyme round the outer side of the otocyst: this is the outer wall of the auditory capsule (Fig. 154, A, a.c). A little later than the stage mentioned a knob of cartilage begins to develop on each side of the notoehord at the level of the septum between metotic myotomes III and IV. This is an enlarged and precociously developed neural arch which, becoming, as will be seen presently, incorporated in the skull, is known as the occipital arch. The base of this spreads forwards along the dorsolateral surface of the notoehord to form the occipital plate (Figs. 154 and 155, B, o.p). .

By stage 34 the chondrocranium has reached the condition shown in Figs. 154 and 155, B. The trabeculo-parachordal cartilage has spread outwards and has become continuous with the rudiment of the auditory capsule so that the greater part of the lateral portion of the deﬁnitive chondrocranium is now laid down in cartilage. The two trabeculae have extended forwards, converging towards one another and passing in front into an unpaired mass of cartilage The ﬂoor of the cranium has made little pro for the most part, occupi

grese, its position being, ed by a. large bas1cran1a,l fontanelle.

FIG. 154.——Il1ustrating the development of the chondrocranium in Lung-ﬁshes. (After Agar, 1906.)

A, Protopte-ms, stage 31; B, Le1_aido.-£rcn., stage 3-}; C, L-ep-idosiren, stage 36 +. a.c, auditory capsule; (10.1), antorbital process; u-rt, foramen for artery; bc. , basicranial fontanelle; b.;;__ ‘nasilar plate; Hy, hyoid arch; £n.s, internasal septum;; M, mandibular arch; N, notochoni; oc.u, occipital arch; oc.r, occipital rib; o.p, occipital plate; pn..c, prenasal cartilag ; \'2.\'3.VII lat, foramen for exit of maxilla.r_\' and mandibular divisions of trigeminal nerve, together with buccal and superficial ophthalmic branches of Facial and communicating branch between Facial and Vagus ; VII hm,

foramen for hyomandibular branch of Facial; Vllsp, foramen for superior palatine branch of Facial.

lying between the olfactory organs—-the internasal septum (ring).

Posteriorly the occipital plates have spread forwards but are still separated by a distinct space l'rom the true chondrocranium. The precoeiously developed occipital arches (om) have reached a large size and the pair of corresponding ribs———the occipital ribs (oc.'r)—-— which are so characteristic a feature of the Dipnoan skull have also made their appearance.

In the next stage ﬁgured (Fig. 154, O) the occipital plates have become continuous with the parachordal cartilages forming a broad basilar plate (lap) in which is embedded the notochord, except its tip which is still to be seen projecting freely into the basieranial fontanelle but which later on disappears. The side wall is extending dorsalwards and has enclosed the roots of the trigeminal and facial nerves, forming the outer wall of the Gasserian recess. Further forwards the front part of the basicranial fontanelle has become in great part obliterated by cartilage continuous laterally with the anterior extensions of the trabeculae. The lloor of the cranium is still deﬁcient except anteriorly and posteriorly. Laterally a long antorbital process (cap) has grown out from the dorsal edge of the trabecu1a,.passing forwards into the upper lip.

The olfactory organ has by this stage become enclosed in a characteristic olfactory capsule. From the anterior end of the internasal septum a horn-like outgrowth spreads outwards and backwards to form the ventral edge of the capsule, meeting posteriorly an independently developed subnasal cartilage (Fig. 155, C, s.n.c). This horn-like cartilage is met by four cartilaginous outgrowths from the dorsal side of the internasal septum which arch forwards and outwards over the olfactory organ. The roof of the olfactory capsule owing to this mode of origin has a characteristic fencstrated appearance. Between and in front of the olfactory capsules the internasal septum comes to project forwards slightly as the prenasal cartilage (Fig. 154, C, pn.c).1

In the last stage ﬁgured (Fig. 155, C) the chondrocranium has reached practically the condition of the adult. The occipital arches have extended dorsally so as to fuse, on the one hand, with one another to form the median supraoccipital ridge, and, on the other, with the auditory capsule. A horizontal shelf . of cartilage has grown outwards from the side wall of the cranium and quadrate cartilage (see below) enclosing a space (P.0) in which lies Pinkus’s organ (see p. 133). The dorsal portion of the internasal septum extends backwards slightly as the mesethmoid cartilage (me).

1 When investigating the development of Lcpidosiren in South America in 1896 I was struck b the fact that badly macerated skeletons of about this stage, with the lower jaw an other cartilaginous arches detached, as is commonly the case, and with the olfactory capsule frayed out at its edge, presented a remarkable resemblance to the remains of the curious little “ lamprey ” Palaeospondylus described by Traquair (1898). The resemblance was such as to» eave little doubt in my mind that Palaeospondylus is really a Dipnoan—--either larval or an adult form of small size and primitive structure. This conclusion is supported independently by the investigations of W. and I. Sollas (1903) who conclude that Palaeospoadylus is an Amphibian. Any one without practical knowledge of young Lung-ﬁshes would quite naturally suppose their imperfect remains to be those of young Amphibians. V CHON DROCRAN I UM 31 1

FIG. 155.—I11ustra.ting thé development of the chond1‘0cra.nium in Lung-ﬁshes. (After Agar, 1906.)

A, 1"rotoptems, stage 31; B, Lepi.dn.sn1rcn, stage 34; C, Lepidosivre-n, stage 38. um, :mdit.m-_v u:xpsul.e; gar, ﬂoor of Gusseritm rm.-.\..~“.s; Hy, hyoid at-ch; Lo, interopercular; me, mesethmoid; M, uumdibular m-ch; N, notochord; o, ope-.rcula.r; oc.a., occipital arch; ocxr, occipital rib; o.p, occipital plate; o.t, or-bito-temllporal; _p._q, pectoral girdle; P1). pm-ziticm of I’inkus's or-gnu ; p.q, palat()q11:ulr-ate; (J, quadrate; s.n.c, subnasul c1u'til:l-ge; l, ﬂrst. hraun,-lniul arch ; III, fu1':ll!ll‘l1 for Oculomotor; V, \'l l. l'uz-.-unina for T1-igeminal and Facial. 312 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

In the case of the young Protopterus the cartilage goes on extending considerably with growth. In the region of the auditory capsule it spreads dorsalwards and reaches the middle line so as’ completely to roof in the cranial cavity at this level. Further forwards in the region of the Gasserian recess the side wall of the cranium also extends dorsalwards, though in this region there remains a wide deficiency in the cartilaginous roof.

In 1;epz'do.s~e"ren the increase in cartilage is less marked, in fact the ehondrouranium of the adult remains in many respects in the same condition as that of the larval Protopterus.

The Dipnoan ehondroeranium obviously belongs to that type in which the primary basal eartilages of the skull are continuous on each side—almost or quite from the beginning, the separation into distinct trabecular and paraehordal portions, if visible at all, being conﬁned to a very brief period, and in which the cranial cavity extends forwards between the orbits (platybasic type). Seeing that a similar type of chondrocranium occurs in the majority of the holoblastic lower Vertebrates the probability is that it represents a more neaiily primitive condition than the tropibasic type, with paraehordal separate from trabecula, which is more usual in the meroblastie vertebrates.

DEVELOPMENT or TIIE CHONDROCRANIUM IN ELASMOBRANCIIS.-— As the chondrocranium has for its main function the support and protection of the brain, and develops in close relation with it, it will be of interest to compare with the development of the Dipnoan cranium that of one of the meroblastie Vertebrates in which the brain is modiﬁed in early stages by a greatly developed cerebral ﬂexure. The Elasmobranchs are admittedly the most nearly primitive of such forms and may therefore most suitably be taken as the example.

Here (Pristiurzos and Aca/nth'£as——Sewertzoff, 1899) the ﬁrst indications of skull development make their appearance about stage 25 (see Chap. XI.), as a concentration of mesenchyme on each side of the notochord about the level of the otocyst. This spreads, headwards and tailwards, as a paraehordal strand of prochondral tissue, extending anteriorly as far as the Facial nerve and continuous posteriorly with the rudiment of the vertebral column. As the paraehordal plate takes deﬁnite form it develops in its occipital portion segmentally arranged rounded swellings which project dorsally between the nerveroots and correspond in position with the intermuscular septa.

The prochondral paraehordal plates gradually become chondriﬁed and at the same time they extend outwards and dorsalwards to form the basilar plate. As they do so the metameric projections ﬂatten out and disappear in the anterior portion while posteriorly they become more pronounced, growing up dorsally between the nerve-roots and ﬁnally meeting over the roots so as to enclose them in distinct foramina. In the region behind the deﬁnitive skull the swellin gs in question do not fuse but develop into discrete arch-elements. The last of the swellings to be included in the skull would appear.to be, as a rule, in Sharks and Dog-ﬁsh that between metotic myotomes 7 and 8 (Braus, 1899) though in all probability variation occurs as between different genera. and species and possibly even between individuals of the same species. The trabeciilae are strikingly different in their relations during early stages from those of the Dipnoan. Instead of being continuous with the parachordals they are at ﬁrst separated from them by a wide gap in which appears on each side a small nodule of cartilage the Polar cartilage (van Wijhe, 1905). Further the long axes of trabeculae and parachordals instead of being in line are practically at right angles to one another. It is probable that both of these peculiarities are to be associated with the greatly developed cerebral ﬂexure. The fore-brain has as already described been bent downwards into a kind of retort shape," the ﬂoor of the thalamencephalon coming to face in a tailward direction. As the thalainencephalic floor has undergone this displacement the tra- beculae have been carried with it, so as to assume a practically dorsiventral direction, and this same movement has probably brought about the severance of their original continuity with the parachordals. It will be noticed from Fig. 156

FIG. 156.——Clioiidroc1'aiiium and visceral arch skeleton of

that the d1SPla(?ement an embryo of Acam-thins. (After Sewertzolf, 1899.) has gone even (1.19, auditory capsule; 131, B5, bram_.-liial arches; II, hynid; M, than has been 1nd1" mandibular arch;n.t,urbito-teinporal;1».¢-,paraclim-clal; Ir, l.l'H.l)I'(f.lll:l.

cated so far, for the _ _ _ _ trabecula has been translated bodily in a tailward . direction so that

it lies in a plane considerably posterior to the level of ‘the anterior end of the parachordals. _

At the front end of the parachordal a plate of cartilage (Fig. 156, 0.15) develops in the side wall of the cranial cavity corresponding generally with the orbito-temporal plate of the Lung-ﬁsh (_Alisphenoid plate, Sewertzoif ; Sphenolateral, Gaupp). This is described by van Wijhe as being an outgrowth from the parachordal, while Sewertzofl" states that it is at ﬁrst distinct. .

The auditory capsule originates according to Sewertzoff as a simple outgrowth from the parachordal which gradually spreads outwards and dorsalwards round the otocyst, while according to van Wijhe the ﬁrst trace of cartilage is on the outer side of the otocyst and is independent. in

The cartilage belonging to the various elements which have been mentioned spreads outwards from each till they form a continuous trough-like chondrocranium. The trabeculae become continuous 314 EMBRYOLOGY or THE LOWER vsnrssaarns on.

with one another ﬁrst towards their morphologically anterior endsa vacuity persisting for a time beneath the infundibulum. As might be inferred from the study of Fig. 54 (p. 93), which shows how the ﬂoor of the thalamencephalon gradually assumes its deﬁnitive horizontal position, the trabecular portion of the cranial ﬂoor pawl passu. swings forwards and comes to be more nearly in line with the parachordal portion. The displacement of the trabeculae which we have associated with the exaggerated cerebral fiexure is then a temporary phenomenon which tends to become corrected during subsequent development. The cartilage formed by the fusion of the anterior ends of the trabeculae becomes prolonged forwards between

FIG. 157.--Diagrams illustrating the early development of the chondrocranium of Birds. (Based on ﬁgures by Sonics, 1907.)

A, Chick, 11 mm.; B, Duck, 13 mm.; 0, Duck, 15 mm; D, Duck, 14_mm.; E, Chick, 12 mm. a.c, auditory capsule; ucr, acrochordal cartilage; i.o.s, interorbital septum; mo, mesotic cartilage; ma, neural arch; p, polar cartilage; p. f, pituitary foramen; p.b.f, posterior basicranial fontanelle; p.c, pa:-achorclal; tr, trabecula.

the olfactory organs as a rod of cartilage, the rostral cartilage, which represents the ventral edge of the internasal septum.

The outer wall of the olfactory capsule appears as an, at ﬁrst independent, -piece of cartilage on the anterolateral side of the olfactory organ which gradually spreads round the organ in question and becomes continuous with the rest of the cranium.

It is unnecessary to— follow out in detail the modelling of the deﬁnitive cranium but it should be noticed that the cranial cavity gradually becomes‘ roofed in by the upgrowth of its side walls, and that, in some cases at least (Pvastim-us), this rooﬁng-in process becomes completed ﬁrst in the region between the auditory capsules. This fact is of interest when correlated with the persistence of this portion of the chondrocranial roof in I’rotopterus——suggesting that this is probably the most archaic portion of the cranial roof of the Vertebrate. At the same time the possibility must not be lost sight of that instead of being of ancestral signiﬁcance this feature may be associated merely with particular activity of cartilageformation in the region of the otocyst, connected with the need of protecting that superﬁcially placed organ of sense.

DEVELOPMENT or THE CIIONDROCRANIUM IN BIRDS.-—AccOI‘ding to Sonics (1907) the ﬁrst cartilage to make its appearance is anunpaired plate arranged in a frontal plane and surrounding the notochord at its highest point in the cerebral or mesencephalic ﬂexure. Sonics terms this (Fig. 157, acr) the acrochordal cartilage and states that it makes its appearance in the 5-day embryo of the chick. What appears to correspond to it in Apterya: is described by 'J‘. J. Parker as the prochordal cartilage, though in this case it lies quite anterior to the notochord. Very soon after the acrochordal cartilage, the parachordal makes its appearance——-ensheathing the notochord. As this is thickest laterally and very thin ventrally and especially dorsally (where indeed it may be absent) it presents when viewed as a transparency from the dorsal or ventral side a misleading paired appearance. In Apteryw however the parachordals have apparently retained the actual paired condition.

For a time the parachordal and acrochordal cartilages are separated by a wide gap but later (11-12 mm.) this becomes ﬁlled in by the development of the paired elongated mesotic (basiotic) cartilages (Fig. 157, B, mo). In the Duck these are at ﬁrst independent, but in the Chick they appear to be, even at the time of their ﬁrst appearance as cartilage, continuous with the parachordals. Extending forwards they become continuous with the acrochordal, bounding upon their mesial side a space in which no cartilage is present~——the posterior basicranial fontanelle (Fig. 157, E, pbj). Postero—externally the mesotic cartilage ﬁts round the lagena, forming the rudiment of the cochlear part of the auditory capsule.

The parachordal cartilage spreads out on each side forming the basilar plate of cartilage and in embryos of about 7 days (13-14 mm.) two pairs of neural arch-elements make their appearance as lateral projections near its posterior end (Fig. 157, E, n.a)—-the posterior, situated between the Hypoglossal and the First Cervical nerve, developing ﬁrst. In the Kestrel (Tvlmmnculus alaualarius) Suschkin (1899) found three such occipital arches (Fig. 158, ma) and Gaupp looks upon this as probably the typical number for Birds.

The acrochordal spreads out and forms a transversely situated plate of cartilage.

The trabeculae appear in the chick embryo of about 11 mm. as paired parallel rods of cartilage underlying the fore-brain. Posteriorly each passes into a swelling lying lateral to the pituitary body and as in the Duck and Starling (Stm-nus) this forms at ﬁrst an independent piece Sonics terms it the polar cartilage. Even in the Duck embryo this polar cartilage (Fig. 157, C, 10) becomes very soon continuous with the trabecula in front and with the acroehordal cartilage behind. The connective tissue between the anterior ends of the trabeculae gradually chondriﬁes in continuity with them in both Chick and Duck (Sonics). In the Kestrel Suschkin found a, for atime independent, intertrabecular plate of cartilage in this position (Fig. 158, vltr). This intertrabecular tract of cartilage serves to bound anteriorly the fontanelle (Fig. 157, D, pf) in which the pituitary body lies and through which pass the two internal .‘.tl.1‘Ol3l.(l arteries. Posteriorly this fontanelle is demarcated from the posterior basieranial fontanelle by the acrochordal cartilage later the posterior boundary of the sella twcica. It appears to be character FIG. 158. ———-Early smge in the development of the chmulrocraniiun of the Kestrel (Tinmmculus alcmdw-n‘.-us). A, side view; B, dorsal view. (/\l“r.-er Suisttliliin, 1899.)

Mr, auditory capsule; itr, intertrabecular c:zi-tilug-u; w.u., neural ‘arch:-s: tr, trabecula; III, foramen for oeulumotor nerve.

istie of Birds that this dorsum sellae undergoes a considerable amount of reduction during later development.

In Chick embryos of about 12 mm. a patch of cartilage has made its appearance external to the otocyst between the lateral and the superior (anterior) semicircular canals which gradually spreads forming the external wall of the auditory capsule and closely moulded to the surface of the canals. This periotic cartilage (Fig. 157, E, (ac) is for a time separated by a wide gap from the

basilar plate but this gap gradually becomes more and more encroaehed ‘

upon until reduced to a. narrow ﬁssure through which cranial nerves IX, X, and XI ﬁnd their exit. A.part from this ﬁssure the basal and periotic cartilages become continuous. As the wall of the auditory capsule extends dorsally it remains incomplete at two points where perforated by the Facial and ‘Auditory nerves.

The roof of the chondrocranium is represented by a quite inconsidcrable tectum synoticum, which originates as a pair of at ﬁrst separate cartilaginous rods (Chick 21 mm.). 'l‘hese very soon become continuous with one another and with the auditory capsule.

Development of Chondrocranium in General

The three examples of chondrocranial development which have been dealt with will suffice to give a general idea of the process with its variations.

A survey of the known facts in Vertebrates generally shows that the ﬁrst rudiments of the chondrocranium consist of paired elongated pieces of cartilage (preceded by prochondral tissue) lying on each side of the mesial plane and on the morphologically ventral side of the brain. These rudiments are divisible into a (para)chordal portion lying at the side of the notochord, and a prechordal portion lying anterior to this. A break in the continuity of the cartilage frequently occurs somewhere about the limit between these regions and this had led to the regarding of the portions so separatedtrabecula in front and parachordal behind - as being fundamentally distinct morphological elements. As a matter of fact the break, when it does occur, appears to vary in position: thus in I’etrom,g/zen the “trabeculae” extend back for some distance beyond the tip of the notochord, so that their hinder parts are parachordal in position. In many cases the break is visible only for a very short period, while in others (Lepidosiren) there is complete continuity between trabecula and parachordal. On the whole it appears justifiable in the present state of our knowledge to regard the break in continuity between trabecula and parachordal not as marking a demarcation between two originally distinct morphological elements but rather as a secondary solution of continuity correlated with exaggerated cerebral (mescncephalic) ﬂexure.

The parachordal cartilage in the case of the Elasmobranchs passed backwards by perfectly insensible gradations into the cartilage of the vertebral column. In that portion (occipital region) which lies between the hinder limit of the deﬁnitive cranium and the vagus nerve there appear for a time evidences of segmentation, corresponding with that of the vertebral column, and it is therefore justiﬁable to regard this portion of the parachordal cartilage as representing a region of fused vertebrae. In -the anterior or mesotic portion there are no visible metameric swellings but, as the relations to the notochord are otherwise identical, it is difficult to refuse a homology in this case which is granted in the case of the hinder portion. Here again, then, we should be inclined to regard the distinction between the mesotic and the occipital portions of the parachordal as merely a secondary differentiation in what was once a continuous structure or series of structures: in other words we should regard the whole of the parachordal region of the cranium as representing a modiﬁed portion of vertebral column which has been absorbed into the cranium.

The foundations then of the vertebrate chondrocranium are laid in the form of paired basal eartilagcs which are eventually continuous throughout parachordal and trabccular regions but which may for a time consist of separate portions lying one in front of the other. As chondriﬁcation spreads from each of these primary elements, they become united together in a continuous plate of cartilage, forming the ﬂoor of the chondrocranium. From this in turn chondriﬁcation spreads upwards to form the side walls and roof, and forwards into the ethmoid and nasal regions. To the brain-case so formed there become added the protective capsules of the olfactory organ and otocyst. As each of these organs is a development of the external skin, we may assume with a considerable degree of probability that their cartilaginous capsules were originally independent of the cranium.

Any repetition however of this completely independent stage of the sense-capsules in question has apparently become obliterated from ontogenetie development. Portions of the sense capsule may arise from separate centres of chondriﬁcation 8.5;. in the case of the auditory capsule the first rudiment may be in the form of an independent patch of cartilage in the region of the lateral semicircular canal. Even in such cases however the inner portion of the capsule develops in continuity with the chondrocranium. Again the Dipnoan arrangement, where the otic capsule is without any wall upon its mesial side so that it takes the form merely of a bulging of the lateral cranial wall, is to be looked upon as secondary.

Skeleton of the Visceral Arches

The anterior portion of the alimentary canal forms a tube leading from the mouth back underneath the cranium, its lateral walls perforated, and therefore weakened, by the visceral clefts. The coelomic space being no longer present in this region somatopleure and splanchnopleure are in continuity, a continuous mass of mesenchyme ex tending from ectoderm to endoderm. This mass of tissue is divided by the clefts into the series of visceral arches and each of these is characteristically strengthened by a tract of tissue in‘its interior undergoing condensation and chondriﬁcation to form half-hoop shaped cartilaginous arches. These arches are named according to the mesenchymatous arch in which they lie-—Ma.ndibular (I), Hyoid (II) and First branchial (III), Second branchial (IV) and so on. The skeletal branchial arches differ in number in different verte brates, just as do the corresponding mesenchymatous arches (see p. 153). In the Lamprey,‘ which probably in this respect shows the most nearly primitive arrangement, the two half-hoops of a pair become continuous with one another ventrally. In the gill-breathing ﬁshes the hoop typically becomes divided by joints into four segments on each side, with a median ventral copula——no doubt an adaptive arrangement to facilitate the movements of respiration. Where branchial respiration is reduced the arch has reverted to its primitive unsegmented condition (Lepidosiren, Amniota) and no trace of segmentation appears during ontogeny.

1 There is in the writer's opinion no sufﬁcient evidence to doubt that the visceral -skeleton of Cyclostomes is homologous with that of Gnathostomes.

In Elasmobranchs (Dohrn, 1884) chondriﬁcation begins on each side and then spreads dorsally and ventrally. Segmentation takes place first into a dorsal and ventral half and later each of these segments again. The gill rays develop independently of the hoop and only come into contact with it later. .

The hyoid arch corresponds closely with the branchial arches in its mode of development.

The arches so far dealt with——branchial and hyoid———having to do primarily with the function of branchial respiration show their typical development in Fishes. With the disappearance of this f'unction they become degenerate. This degeneration makes itself manifest in (1) reduction of segmentation, (2) tendency to fusion between successive arches and (3) reduction in number from behind forwards.

Thus in a Newt four cartilaginous branchial arches make their appearance but they are for a considerable period continuous dorsally and ventrally with their neighbours in the series, and they develop only one joint upon each side c'.e. the half-hoop consists of two segments instead of four. In a Lizard only two cartilaginous branchial arches make their appearance, and in a Bird only one.

The hyoid and the anterior branchial arches have probably been saved from complete disappearance in the higher Vertebrate by the fact that they have taken on important functions in connexion with the tongue and have become specialized in accordance therewith. Thus in the case of the frog tadpole there is found, when the branchial apparatus is at the height of its development, a continuous cartilaginous hyobranchial skeleton, in which may be recognized parts corresponding to hyoid arches, copula between these, and 4 pairs of branchial arches continuous ventrally. At the time of metamorphosis this becomes greatly modiﬁed to give the adult condition (Gaupp, 1894): the mid-ventral portions become greatly expanded to form a ﬂattened plate—the so-called “ body of the hyoid ”: the hyoid arch becomes an elongated slender rod which serves to suspend the apparatus from the skull: the branchial arches disappear except the ventral end of the second which persists as a stump (“ Postero-median process ”).

MANDIBULAR ARCH.-—-The usually accepted idea of the mandibular arch is to regard it as a half-hoop shaped cartilage resembling the other arches, to which is added a forwardly projecting outgrowth— the palato-pterygoid bar-——which forms the primitive upper jaw

.skeleton. In actual ontogeny there is always a less or greater

amount of departure from this general scheme.

In the Amphibians and Lung-ﬁshes the hoop-like character of the main portion of the arch has been most completely retained. Here (Fig. 155, A) the arch develops on each side as a curved bar of cartilage—-a mid-ventral copula having been detected in certain cases. The cartilage soon becomes completely continuous at its 320 EMBRYOLOGY OF. THE LOWER VERTEBRATES CII.

upper end with the chondrocranium and its dorsal end becomes segmented oli", as the palate-quadrate cartilage, from the larger ventral portion —-Meckel’s cartilage-—which forms the primitive skeleton of the lower jaw.

In the animals mentioned the lower jaw remains throughout life connected with the cranium through the dorsal portion of the original arch. This must be looked on as in all probability the primitive mode of attachment of lower jaw to skull and such skulls may therefore bc termed protostylicﬂ

Both in Lung-ﬁshes and Urodele amphibians the palate-pterygoid process is much reduced. In Urodeles it makes its appearance only at a late stage of development and is of comparatively small size. In Lepidusirem. and P7-otopterrus it has become eliminated almost entirely from development, being represented for a short time by a slight condensation of tissue which never becomes chondriﬁed. This is probably to be interpreted as a modiﬁcation of development induced by the precocious development of the bony skeleton of the upper jaw which in the forms mentioned replaces functionally the originally cartilaginous skeleton.

The Elasmobranch ﬁshes do not exhibit this reduction of the palato-pterygoid bar for this becomes the functional upper jaw. On the other hand an important modiﬁcation of development has taken place in correlation with the fact that in these ﬁshes the original dorsal end of the mandibular arch has lost its primitive function of suspending the jaw, this function having been taken over by the enlarged dorsal end of the hyoid arch (Hyostylic type of skull). In correlation with this the portion of the mandibular arch lying above the pterygoid outgrowth is, all through development, greatly reduced. It is apparently represented by the prespiracular cartilage, which develops comparatively late.

The mandibular arch makes its appearance in Acanthias (Sewertzoff, 1899) as a G—shaped rod of cartilage lying in the rim of the buccal opening on each side (Figs. 156 and 159). The lower half of this segments off as Meckel’s cartilage, while the upper half, which develops from behind forwards, clearly represents the pterygoquadrate bar. This becomes continuous with and later articulated towards its anterior end with the trabecula--a doubtless secondary connexion with the cranium seeing (1) that it arises from the anterior and later developed portion of the palate-pterygoid outgrowth and (2) that in primitive sharks such as Notidanus, in Lung-ﬁshes, and in Urodele amphibians, the attachment of mandibular arch to skull is further back in the auditory region~—-in fact in the region of the original dorsal end of the mandibular arch.

In the lower Vertebrates apart from those mentioned the development of the cartilaginous mandibular arch takes place on

1 Graham Kerr, 1908. Attention is drawn in this paper to the need of an additional term to designate the more primitive ty e of so-called autostylic skull. A similar suggestion had, however, already been m e by Gregory (1904). V . THE SKELETON 321

similar lines. In the Reptiles and also in Birds the palato-pterygoid outgrowth is again reduced in size———in correlation with the fact that in the Tetrapod Vertebrates the tooth-bearing function of the original upper jaw or palato-pterygoid bar has been taken over by the secondary upper jaw composed of bones such as the maxilla and premaxilla. '

BONY OR OSSEOUS SKELETON

Bone, like cartilage, is a modiﬁed connective tissue. In its typical form it differs from cartilage in the facts, that its matrix yields on being boiled a larger proportion of gelatine, that the matrix is rendered rigid by being strongly calciﬁed, and that the cytoplasm projects as slender branching processes which ramify

FIG. 159. —Skeleton of visceral arches and pectoral girdle of 20'5 mm. embryo of Spinax. (After Braus, 1906.) I:I_, [;5__ In-um-lnial :u'clw.'~':: Hy, ll_\'0l(l: I, labial cartilage; M, nuuulilmlar :1l"(‘.ll: p, palato-pterygoid lmr ; ,.._/; rudiment of ]-«'x't‘.a_n'ul lin ; p.g, pectoral girdle; (3, knob for attachment to trabecular region of skull. through the matrix and are commonly continued into those of other cells. Many dill'erent varieties of bony tissue exist. In ordinary bone the cell elements are completely surrounded by the calciﬁed matrix. On the other hand some of the cells may have the main part of their cell-body outside the calciﬁed mass, only a slender prolongation being surrounded by it (Bones of Lepidosteus _and Amie). Or this peculiarity may apply to all the cells (Dentine of higher Vertebrates) or ﬁnally no cells or parts of cells are enclosed within the ‘hard matrix—-as is often the case in early stages of development ‘and as occurs in the adult condition in many Teleostean fishes.

Probably the most archaic type of bony skeleton in existing Vertebrates is seen in the Placoid scales Of the Elasnlobra-nchs and consequently the mode of development of these will logically fall to be considered first.

The appearance of the‘ scale is foreshadowed by a localized eorldensation of the dermal connective tissue immediately beneath

VOL. 11 Y 322 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

the epidermis. Presently this begins to bulge upwards like a dome into the epidermis. The epidermal cells imniediately liounding this little dermal elevation take on a columnar shape; they constitute the enamel epithelium (Fig. 160, e). The (dermal) cells‘ on the surface of the dome or papilla, immediately underlying the enamel epithelium, also become distinct and form a. definite layer of odontoblasts. ‘

The hard substance of the scale makes its appearance as a cone of dentine fitting over the surface of the dermal papilla and in turn ensheathed by the enamel epithelium. The dcntine cone, which usually becomes directed tailwards, gradually thickens, encroaching upon the dermal papilla or pulp which it surrounds. It lies

FIr_:. 160.——-Longitudinal vertical section through the skin of an crI1l'n‘_\'nni«: Shark to show a developing placoid scale. (From Balfour’s _IvJm.l2r.qnlo_:/y: ligun-. li_\'(_iL'gl_‘lll_)(l.l1I‘ afti.-r Hertwig, 1874.)

l'.', epidermis; «J, enamel epithelium; 0, enamel ; p, dermal papilla.

immediately outside the odontoblasts and as it increases in thiclmess the outer portion of some of the odontoblasts persists as a ﬁne thread of cytoplasm extending out through the substance of the dentine, so that when dried the dentine is seen to be traversed by innumerable ﬁne slightly diverging canals each of which contained a protpplasnniic thread.

The hard material of the dentine is cominonly regarded as calciﬁed matrix but there is evidence which points rather to its being formed of modiﬁed cell cytoplasm. This point will be returned to in connexion with the development of the teeth.

Towards the surface of the cone the calciﬁed substance changes its character. It becomes extremely hard (consisting of very dense calcium carbonate), transparent and highly refracting, and the terminal branches of the tubules within it are reduced to an extreme degree of ﬁneness. This outer layer is commonly known as enamel. It may be comparatively thick, or on “the other hand it may be extremely thin as for example in the scales of Acantlums except the V PLACOID SKELETON 323

enlarged spine-like scales in front of the dorsal ﬁns, on the anterior face of which it is well developed. -The enamel is in turn covered on its surface by an extremely thin membrane-like layer———the enamel cuticle-—and Huxley (1859) made out the important point that this is continuous with the basement membrane of the epidermis outside the limit of the scale rudiment.

In the teeth of the higher animals, which as will be seen later are simply modiﬁed placoid scales, the enamel is sharply marked off from the dentine and it is usual to regard it as of totally different origin namely as a kind of cuticular formation by the inner ends of the enamel epithelial cells. The chief reasons for this view are the sharp differences in appearance and composition from the dentine in these higher Vertebrates, and the fact that the cells of the enamel epithelium undergo a shortening as the enamel layer thickens—as if the inner ends of the epithelial cells were undergoing conversion into enamel from within outwards.

It is however curiously diﬁicult to ﬁnd evidence sufficiently convincing to justify the almost universal acceptance of this idea even as ‘regards the higher Vertebrates. And in the case of the Fishes the evidence—---such as the location below the basement membrane and the frequently quite gradual transition between the so-called enamel

and the den tine—stron gly supports the idea that the former is simply a modification of the outer layer of the dentine.

The basal edge of the cone of dentine comes to spread outwards all round parallel to the surface of the skin as irregular trabeculae forming a strong basal plate by which the scale is ﬁrmly ﬁxed in the dermis. This basal plate is usually of homogeneous appearance but its substance shows a gradual transition to the typical dentine of the spine, and in the case of 0a.llo7'7z.3/'n.clu4.s (Schauinsland, 1903) the basal plate as a whole shows, just as it does in the ancient fossil Coelolepids, dentinal structure. There seems then no reason to doubt that the basal plate is in its nature closely allied to dentine or in other words that it is bone in the broad sense of the term.

TEE'1‘II.—A section across the jaw of an ordinary Dog-ﬁsh is suﬁicient to demonstrate the important morphological fact of the homology of the teeth and the placoid elements of the skin. Teeth are simply placoid elements belonging to that portion of the outer skin which is carried inwards to form the stomodaeum. Or conversely the spines of the placoid scales are simply teeth which have not been carried inwards into the ston1odaeu1n. In accordance with this the placoid scales were long ago (1849) named, by Williamson, dermal teeth. The demonstration of the homology in detail will be found in a classical paper by O. Hertwig (1874).

The lining of the buccal cavity being morphologically part of the outer skin the probability is that originally teeth or placoid elements were distributed equally all over it. But in the evolution of the Vertebrata there has clearly taken place a restriction of the teeth to particular parts of the lining where they can be most 324 EMBRYOLOGY OF THE LOWER VERTEBRATES on.

effective. In some of the lower ﬁshes (many Elasmobranchs, e.g. Acanthvlas) teeth of a simple character, practically unmodiﬁed plaeoid elements, are still to be found scattered over the roof of the buccal cavity and even extending back into the pharynx. Unfortunately the development of these has not been worked out in detail. In Teleostean ﬁshes however a very simple type of tooth development has been described ag. in the Pike (Esoa: lucius). The teeth are here no longer scattered equally over the buecal lining; they are restricted to the dentary, maxilla, vomer, palatine, and the inner surface of the visceral arches. The teeth on the roof of the month arise as simple conical dermal papillae which project into the epidermis and develop enamel, dentine, and an irregular trabe—

FIG. 161.-~~—Early stage in the development of the tooth in (A) '_..'u/‘ulm/1/..s* and (B) Lr:.pz'¢_/n.s-irm. (A after Semen, 1899.)

«I, dent'.inc; (M1, 0cl0ntul')lasts.

cular bony base on the same general lines as described above for the typical placoid element.

Relatively primitive conditions are found again in the Dipnoi and Amphibia (Urodela and Gymnophiona) in the latter of which the teeth may be very widely distributed (3.9. on preniaxilla, maxilla, vomer, palatine, pterygoid, parasphenoid (Spelerpes), as well as on the dentary and occasionally on the splenial. In the simplest cases the tooth originates as a simple conical or rounded dermal papilla which projects upwards into the ectoderm (cf: Oemtodus, Fig. 161, A) but in other cases an onward step has been made and the “ ectoderm ” in the region where the papilla develops tends to grow down below the general level of the ectoderm into the underlying connective tissue of the dermis (of. Lepidosiren, Fin‘. 161, B . ' ..

In )the Amniota this tendency becomes more pronounced, the ectoderm covering the tooth-germ not merely projecting downwards into the underlying mesenchyme but becoming constricted off from v THE TEETH 325

the rest of the ectoderm so as to remain connected with it only by a narrow stalk or isthmus.

The tooth is built up of precisely the same elements as the placoid scale~—-dentine, enamel and basal plate. I ts modiﬁcations are such as to make it more efficient for its special purpose. The projecting spine becomes exaggerated to form the functional part of the tooth: it remains conical, or it becomes a flattened blade with plain or serrated edge, or it becomes a low ﬂattened crushing plate.

To secure greater strength the pulp may become traversed by hard trabeculae (vaso—dentine). .

Regarding each of the three elements mentioned above there is a certain amount of controversy. As regards the dentine there is the question of its origin-——whether it is to be regarded as calciﬁed matrix or as modiﬁed cytoplasm. The evidence ol' Le/7id0sz'7'c7b which on account of the size of its cell elements is always of weight in such questions~—scems very clearly on the side of the latter view. As shown in Fig. 161, T3, the cytoplasm of the odontoblast passes uninterruptedly into the calciﬁed dentine, the spaces between the odontoblasts on the other hand dying away as the dentine is approached. But if in a relatively archaic creature like Lepidosiren the main part of the dentine is undoubtedly modiﬁed cytoplasm this at once raises a strong presumption in favour of the same being the case in the higher Vertebrates even if it be not actually obvious.

Again as regards the enamel it is taught practically universally that it is formed after the manner of an internal cuticle by the cells of the enamel epithelium. This idea has come down to us from the days of the early investigators who devoted themselves especially to the investigation of Man and those Vertebrates most closely allied to him. In those days the structure of the lower animals was interpreted according to the data obtained from Man and his allies. The whole outlook was the opposite of that which holds in these evolutionary days when the accepted principle of all morphological work is to interpret the higher and more complex animals by data obtained from these lower in the evolutionary scale. Applying this principle to the case of the teeth of the most archaic Vertebrates we see in the Elasmobranch ﬁshes that the outermost layers of the dentine develop the special modiﬁcations already

‘alluded to——extreme denseness and hardness, transparency and high

refraction, reduction of the proportion of organic material, reduction of the tubular cavities. Here the enamel is undoubtedly modified dentine.

But if this be so there are only two alternatives open to us in interpreting the enamel of the higher Vertebrates. It is either to be regarded as a further stage in the differentiation of the outer layer of dentine or it is to be regarded as something quite new, a new substance formed by the enamel epithelium. This latter is the generally accepted View and in accordance with it the hard layer on the teeth of ﬁshes was given by Williamson the name 326 EMBRYOLOGY OF THE LOWER VEBTEBRATES on.

Ganoine to distinguish it from the true enamel of the higher Vertebrates.

As regards the basal plate the main question at issue is the evolutionary one whether or not the view of Gegenbaur should be accepted that these basal plates constitute the iirst phase in the

. evolution of the bony skeleton. This question will more suitably be

discussed in connexion with the bony skeleton in general.

Lastly questions of general interest are raised by these exceptional cases where the developing tooth cannot be traced into immediate relationship with the ectoderm. In Lepidosiren and P'ro£opte'ru.<: as well as in the Urodele Amphibians portions of the lining of the bueeal cavity which give rise to the teeth have the appearance of being derived in the embryo from cndoderni. Again in Teleostean fishes teeth are developed far back in the pharyngeal region, in other words in a portion of the alimentary canal which is lined with endoderm.

Such cases obviously cause serious trouble to those who apply

the germ layer theory rigidly. They explain them by supposing

that there takes place in development an actual spreading inwards of ectoderm over the surfaces on which teeth will‘ develop. As indicated in Chapter III. in dealing with the buccal lining of Urodeles and Lung-ﬁshes the writer of this volume believes that the evidence adduced so far of the ingrowth required by this explanation is not to be relied upon. He would rather explain such cases as due to the more or less broad debatable zone between the ectoderm and cndoderin, the influence of one layer being liable to spread into the other and there being no sharp line the position in regard to which decides deﬁnitely to which layer a particular organ belongs. EGG-TOOTH or REP'I‘ILIA.—-—In the embryos of Reptiles there appears a precociously developed “ egg-tooth” at the tip of the

upper jaw which has for its function the rupture of the egg-shells

In Geckos there are a pair of these present, attached to the premaxilla close to the mesial plane. In other Reptiles the left eggtooth appears only as a transient rudiment and the functional (right) tooth takes up a practically median position so that it appears to be unpaired. It is of interest that this holds also for snakes in which there are no deﬁnitive teeth in the premaxillary region (Rose, 1894). POISON FANG OF VIPERIDAE.—The poison fang of the Viperidae is highly specialized for the injection of poison, its pulp being traversed by a longitudinal tube, composed of dentine and attached to the outer wall of the tooth along its anterior face. The inner tube---or poison canal——passes at each end into an open groove the openings so formed serving for entrance and exit of the poison respectively. The main features of the developmentare illustrated by the transverse sections shown in Fig. 163 (p. 329). The poison canal makes its appearance as a longitudinal infolding of the dentine, the ectoderm of the tooth-germ seeming to push the dentine in before it to form a groove (Fig. 163, 7). The groove deepens and its V v THE TEETH 327

lips meet (6) so as to convert it into a tube. From its mode of formation thi.s tube is at first ﬁlled with ectoderrn of the toothgerm. Eventually however this ectoderm disintegrates and leaves an open tubular cavity‘ (2).

Up till this stage the tooth is still enclosed in the ectodermal germ which has increased much in size (2) but eventually this

‘ectodermal mass also disintegrates with the exception of its outer most‘ layer, so as to give rise to the cavity of the sheath in which the functional tooth is contained. As the tooth becomes functional this cavity comes to communicate with the duct of the poison-gland so that it receives the poisonous secretion, and owing to the poisoncanal retaining the form of an open groove towards the basal end of the tooth it in turn receives the poison from the cavity of the sheath.

'F‘I(:. 162.———Diagram illustrating tooth .\'1lm'C.<sin1l in an El:Is1noln':u1ch (A. primitive, J3, existing condition) ; an Amphibian ((_') ; and n l'i('}IillL' (l.uc¢-Wu) (1)),

41.11, lh-ntal gmova-: «Ll, «la-nml hnnina ; ,u..~'. plavoid .»-.-_-.-ah‘-; I, tooth.

Enamel is present as a thin layer towards the point of the fang: traced towards the base it passes into a simple ﬁne cuticle-like basal

membrane. SUCCESSION or TEE'1‘H.-—In cases where the teeth have become restricted to special areas, and more particularly in cases where from

their shape and from the habits of their owner they are liable to be.

broken off or damaged by wear or otherwise, it is usual to ﬁnd a special arrangement for the replacement of the lost or injured teeth by new ones. Such an arrangement is seen in its simplest form in an ordinary ])og-ﬁsh or Shark (Fig. 162, A and The portion of skin——-ectoderm with its strong and ﬁbrous underlying dermis———to which the tooth-bases are attached is gradually, by processes of differential growth, caused to shift its position in an outward direction over the edge of the jaw which supports it. This is brought about by the skin UI1d€l.'g()lll:_[' :1. continual slow process of absorption or atrophy along the outer margin of the jaw (about the point 328 EMBRYOLOGY OF THE LOVVER VERTEBRATES CH.

marked by a slight indentation of the surface in Fig. 162, B), while there takes place a compensating process of growth, or formation of new skin, along the inner margin of the jaw, near the bottom of a deep groove (Fig. 162, A, d.g). The young skin arising in this region, like young skin elsewhere, produces placoid elements and it is these which, growing older as they gradually move forward over the jaw surface, become the functional teeth. Under normal circumstances the rate of outward progress is such that by the time the tooth is becoming inefficient through wear it gets into the absorptive region and is shed.

It should he mentioned that, to make it more easily intelligible, the above account has been simpliﬁed i11 one important detail. The replacement groove is as a matter of fact in the Elasmobranchs mentioned no longer an open groove. lts walls have become fused together, so as to obliterate its cavity and form a solid lamina of eetoderm which dips down into the mesenehyme round the boundary of the mouth, just within the jaw, as shown in Fig. l62, P».

In Amphibia the general arrangements for replacement of the teeth are similar to those of Elasmobranchs, as may be gathered from Fig. 162, C, but an advance beyond the Elasmobranch condition is found here in that the functional tooth is ﬁrmly fused to the jaw. It remains stationary throughout its period of active functioning and it is only at the end of that period, when it is lost either by being broken off or by a process of natural shedding accompanied by resorption, that the next replacement tooth in the series moves up to take its place.

In Reptiles (Fig. 162, D) again the general arrangement is similar except that economizing of material has now taken place, the dental lamina being relatively reduced in bulk between the toothgerms, so that the latter project prominently from the lamina instead of being embedded in its substance as was the casein the Amphibian.

Amongst the Lizards certain modiﬁcations occur which are of importance as foreshadowing arrangements which occur in Mammals. Thus it may happen (Iguana, Leche, 1893) that the first generation of teeth to be formed never become functional but disappear before hatching. Again the replacement mechanism may become reduced in the anterior part of the series (Agama-—~Carlsson, 1896; Ohamaeleo-— Rose, 1893). In the Chameleon the ordinary replacement mechanism is no longer functional except at the extreme hind end of the jaw, where alone new teeth are produced.

The large poison-fangs of poisonous snakes are peculiarly liable to injury and we ﬁnd, as might be expected, that the replacement mechanism is in their case particularly well developed. The dental lamina (Fig. 163, (U), which is very extensive and thinned down to such an extent as to become perforated by numerous openings in its more superﬁcial and no longer active portions, is curved scrollwise upon itself and upon its concave surface develops tooth-germs in V i THE TEETH 329

rapid succession, as many as ten being visible at one time in the ordinary Viper. As the tooth-germs develop and approach the surface they take up a position in two rows (3, 5, and 2, 4, in Fig. 163)

The maxilla, which carries the functional fang, has two bases of attachment for teeth, an inner and an outer, and these are made use of alternately——a functional tooth with external attachment being succeeded by one with internal and conversely.

The replacement takes place approximately synchronously in the two maxillae a pair of teeth attached to the right-hand bases of attachment of the two maxillae (in other words attached to the outer base of attachment on the right maxilla and to the inner base of attachment on the left maxilla) being replaced by a pair attached to the left-hand bases of attachment (inner on right maxilla, outer on left maxilla), In consequence of this F1c..163. ——I’art of transverse section tlirongh upper arrangemtant the individual Jaw of a young Viper. (After Rose, 1894.) teeth of 3 functional pair "Fhe ('ll'.\-’6l(')1)lll_',f'_ to-eth arr nninlwrml in m-ch-rot.‘ so-qin-lice.

- IV). 8 is not shown. lmrk tunn.:¢-ctodvnn; pale him.are the Same dlstance from mesenchymt-. |.h-I1t'im'- is shown in black. The.-. cnamvl 0118 another as their pI‘ede- which is present. as a thin sheath over the apical l‘ll‘l of the “"33” 3"?‘ th"h'.*3“°°?SS°1‘S-. E33333-SZTJIZTi'.‘.'.T‘l21i..iii-1.71"‘.?ff???fT'iiifii'i“UT-£'l'f.’.'i3Z}.’.'.7I.§’3’?II

In this Inodlhcamon of 0 this has bemiiiv (‘.(lll\‘(!l'LI‘(l intoa lulu‘. (pm) still Iillml with the p1‘in1itiVe linear 0(.'l'.-U1lt'I‘lll (_‘t‘-ll:':l.‘,.lll :2 the cells luu-v de;_.--ein-1-:itml. lea\'iii;_-; :1 arrangement of the reP1eee- I;l°;?iT',.'i"‘SII",,‘i.Lii.l.§f}.it°i.§iIf §’.‘.l'.3t°‘iI;i'Ii'lJ.’.".iL';ll5I3 if,’ i3'.?..‘."i’i'$ ment teeth We have doubt‘ (~.a.\'it.y of the tOOt-ll-Sllﬂltll (S). The functional tooth (I) in less a nlechanigln to secure l-l|1'—.\‘8('ll()ll he-re ilgm-ad lwlmigs to tlic unto!‘ series. in whit-h

rapid in this connexion it 18 of , interest to notice that the replacement of the functional tooth is not dependent upon its having already suffered injury or become worn out but takes place at regular intervals (about six weeks in the case of the European Viper, Kathariner) while the snake is leading an active life. .

In the Crocodiles the dental lamina becomes broken up into a network, and ﬁnally reduced to a strand of tissue running longitudin ally along the jaw, slightly to the inner side of the tooth-bases. A V TOOTH-PLATES 331

The originally separate denticles develop as already explained (p. 324) in typical placoid fashion, giving rise to little hollow cones of dentine. Trabeculae of bony tissue (“trabecular dentine,” or

FIG. 164.—~Illustra.ting the dental arrangements in young Lung-ﬁshes. (A .'l.ll(l B :ll'lu1' Sc-.n1nn, l_{\‘!)9.)

A, ronl nfnlmlt-l1 (of :1. Ca-mtodus of stage -15, showing Hui .<ep:1r:ile rnliivnl lo'~.'l.h ; IL 1:.-will of roof of mnuth frnm :i h'll;_5lll.l}' ynll-I120!‘ specimen (stage 46) after the sull fi.~'s11r‘.s' h:i\'n been l_‘ll‘ll.l'l?l(l :1.\\':i_\' h_\' Hm notion of dilute :1lk:Ili : (‘., LepidU.s‘i’I'8'lL, niact-~ml:ed upper jzuv of 5mm_: .»'pm-inn--.n, .~zlmwin;_-; l.ln- pnintvzl L‘.usp.s' still ['m~.s'o-nl. ml lhv luUl.lI-plat:-s; nIf1._ :1nlvrim' nuris; n/_/'13, pUHII‘I'inI‘ n:u'i.~a.

“pulp dentine") spread inwards from the bases of these cones through the underlying mesenchyme, so as to join up the various dentioles by a loose calcified spongework. As development goes on the trabeculae of this thicken, the pulp-filled meshes become proV TOOTH-PLATES 33 1

The originally separate denticles develop as already explained (p_. 324)_i_n typical placoid fashion, giving rise to little hollow cones of dentme. Trabeculae of bony tissue (“trabecular dentine,” or

FIG. 164.-——ll1ustra.ting the dental axrmngeinents in young Imn;_.;-lislu-s. (A and B allot‘ Sunmn, .l8!l‘.l.)

A, roof of mouth ofa Ceratodus of stagt: -Is, slum-ing thu .~wp:n':L1uwnlivsll tvvth : ls, tw-*l.h of roof of mouth from El. sllglitly }’()x1hRer sP*‘cln1en(atM§e 46) :xI‘lm- the .-on tissllc-s haw law-H ('|I*:ll'Ptl :n\‘:n_\' l»_\' the action of dilute» nlk.-zli: C, Lepi¢lo.z:inrn, nmcvmted tumor‘ _i.‘l\\ or .\oIHI:." -‘lN‘t'iIHt‘II, -lNH\'iH_=.'_' ll!" l"'i"“"l ('.11Hp.~i still 1)l'('.\'¢'lll ml 1..l|«- Loot-ln-]Il:lLc-.-; u/fl. !llllI‘l‘ll|l‘ nnris: u/_/"~', post:-riu1'11:u'is.

“pulp dentine”) spread inwards from the bases of these cones through the underlying mesenchyme, so as to join up the various denticles by a loose calciﬁed spon §_v'v.\\'<'11‘l<. :\:-: development goes on the trabeculae of this thicken, the pulp-lilled meshes become pro332 EMBRYOLOGY OF THE L()WER VERTEBRATES CII.

portionally reduced, and the trabecular mass becomes the compact substance of the adult tooth. In the functional tooth the tips of the original denticles have completely disappeared.

In Lep7§a?o.s'7§ren and Protopterus the separate denticle phase of development is not so distinct as in Ueratodus but a reminiscence of it is seen in the pointed cusps which are present on the teeth in early stages (Fig. 164, C).

THE BONES IN GENERAL.--.The view is now accepted by many morphologists, following Hertwig and Gregenbaur, that the true bony skeleton has come about in evolution by the spreading inwards of bone-forming activity from the skin, where it arose in association with the coating of placoid scales which occurs in the lowest Gnathostomata. The probability of this view being correct is rendered apparent by a Sl1I‘\'ey of the phenomena of development of some of the bones in the lower Vertebrates. Both in Lung-ﬁshes and in Amphibians the bones of the skull which carry teeth are found to arise in development in the form of more or less trabecular bony

tissue which spreads outwards from the tooth-bases in the same way as i has already been described as occur2 ring in the development of the compound tooth in Lung-ﬁshes (Fig. 164) i ‘O. Hertwig (1874*‘) found for . example that the vomer, palatine 3:1 and opercular of Urodele Amphibians are developed in this way, forming perforated bony plates studded with conical teeth (Fig. 165). In the case of dentary, maxilla, and premaxilla, part of the bone arises in exactly the same way, while part on the other hand spreads through the mesenchyme without having teeth on its surface. It is to be noted that these bones at ﬁrst, as frequently happens in the development of bony tissue, have no cells actually enclosed in the calciﬁed substance. Later on the teeth in some cases disappear, leaving behind merely the basal plate of bone which gradually increases in thickness. On turning to the Anura it is found that the bony trabeculae develop precociously and form the basal plate of bone while the teeth belonging to it are delayed in their appearance and may even be omitted.

The embryology of the Amphibia then teaches us (1) that typical bones may be developed from the basal trabeculae‘ connected with placoid elements and (2) that a secondary modiﬁcation may arise in which the tooth formation is delayed or suppressed, the trabecular basal plate simply developing by itself and becoming converted into the deﬁnitive bone.

L The facts as narrated by Hertwig for Amphibia do not stand alone. On the contrary an exactly similar mode of development is seen in

FIG. 165.—--Vomer of a 2'5 cm. larva of Axolétl (X45). (After 0. Hertwig, 1874*.) s V ORIGIN OF THE BON Y SKELETON 333

the “membrane” bones of the roof of the mouth in Teleosts, and in the tooth-bearing bones of Lung-ﬁshes. Again there are present minute enamel-tipped teeth scattered over the surface of the dermal bony plates of Urossopterygians and various Siluroid Teleosts such as Lorz'car'ia, Hg/postoma, Oallvlchthys.

Such facts as those just enumerated seem to justify the acceptance, as a Working hypothesis, of the view that at least the more superﬁcially placed dermal bones of the Vertebrata have actually arisen in the course of evolution from the basal trabeeulae or plates connected with placoid scales.

Admitting this a further question presents itself. What was the evolutionary origin of the more deeply situated masses of bony tissue, for example those which replace cartilage? Has the tissue which gives rise to these gradually been infected with bone-forming activity which has spread inwards from the skin? Or has this bone-forming power in the deeper tissues arisen independently? It is in this connexion extremely instructive to study the gradual spreading of the irregular shreds of bony material from the tooth-base of a Lepidosiren. They gradually spread onwards through the connectivetissue matrix like crystals forming in a ﬂuid, and there is no apparent reason why such spreading should not continue for relatively great distances, provided the necessary pathway of connective tissue is present. It appears in fact thoroughly reasonable to regard the deeper portions of the bony skeleton, like the more superﬁcial, as having arisen in evolution by the spreading inwards of bone-forming activity from the skin.

In considering this important morpliological problem, the origin of the bony skeleton, it must be borne in mind that the all-important fact, which far outweighs all other evidence available, is that in the Elasmobranchii, the group of gnathostomatous Vertebrates which is admittedly the most archaic, the placoid scales are the only elements of the osseous skeleton which have as yet made their appearance. There is no suggestion that the ancestors of existing Elasmobranchs ever possessed a bony skeleton apart from the’ placoid scales. Consequently in the Vertebrate groups which have been evolved subsequently to the Elasmobranchs the bony tissue must either be a further development of the bony basal plates of the placoid scales, or else a new independent development. If the former View is shown to have in its favour a reasonable degree of probability we are bound to accept it as our working hypothesis until a better is suggested, for it alone of the two views mentioned is really constructive, the other offers no explanation but merely the negation of an explanation. In the opinion of the present writer the reasonable degree of probability has been amply demonstrated by the facts which have been quoted.

It is also necessary to avoid attaching too great importance to the differences in detail which have arisen in the. evolutionary history of bony tissue under different circumstances. Such differ334 EMBRYOLOGY OF THELOWER VERTEBRATES cu.

ences may become conspicuous and highly characteristic —— for example the difference in relation to the calciﬁed material——--whether the cell elements are completely surrounded by it as in the ordinary bone of the higher Vertebrates, or have merely a prolongation of the cell—bo(1y embedded in it as in ordinary dentine.

Such dit'l'ercnces in detail may be of great interest in themselves. For example the bony tissue forming the scales of Lrpidosteus is characterized by the fact that some of the bone - cells show the dentinal characteristic that the main part of the cell-body lies on the surface of the calciﬁed material and only a prolongation of it is enclosed within the hard substance. Now Goodrich (1913) has made out the important fact that this peculiarity is not conﬁned to the scales but extends to the whole of the bony skeleton. Such a fact is obviously a strong additional evidence of intimate evolutionary relationship between the scales and the rest of the bony skeleton.

Again such detailed differences may raise interesting problems, for example Whether the “ordinary bone ” type or the dentinal type (as is perhaps probable) is the more primitive type of bony tissue.

Interest in such details must not be allowed to obscure the main conception of bony tissue as contrasted with cartilaginous, or the problem of its evolutionary origin. As regards that origin We seem Justified in believing that bone formation has during the evolution of the Vertebrata spread from the dermis—fro1n the neighbourhood of the placoid scale bases——into the deeper tissues and so given rise to the deeper portions of the bony skeleton.. On the other hand we do not appear to be justified in regarding the evolution of the deeper parts of the skeleton as being due to a sinking downwards of actual individual placoid elements. Nor, in the author’s opinion, is there reliable evidence, so far, hearing on the further problem whether or not the first scleroblasts or bone-formin g cells of the Vertebrata were immigrants from the ectoderm. This view, which was supported by Gegenbaur, has a considerable amount of a- priori probability in its favour in view of the facts of skeleton formation in the lower invertebrates.

It is no longer possible in the present state of knowledge to classify bones, as did the older workers, simply into two sharply deﬁned sets membrane bones and cartilage bones. The most that we can do is to recognize various stages in the process of shifting inwards from the skin, from which as already indicated they probably arose in the early stages of their evolution.

Firstly We have the most primitive type which may be termed dental bones, which are superﬁcial in position and which still are connected at one period or other with teeth. Typical examples are the bones already referred to in the roof of the mouth in Amphibians.

A second category consists of bony plates which have lost their tooth structures and have sunk down to a deeper level. These frequently become applied to the surface of the cartilaginous skeleton, remaining separated however from the cartilage by a layer of un~ V B\ON ES AND SCALES 335

modiﬁed connective tissue. Such may be termed investment bones (Allostoses, Gaupp).

Finally a third category of bones are the substitution bones (corresponding roughly to the old group of cartilage bones; Autostoses, Gaupp). ln these the formation of bone has spread into the connective tissue in immediate contact with the cartilage, and as the tissue is formed, room for it is made by the destruction of the previously existing cartilage, which it therefore comes to replace.

While it is convenient to recognize these three types of bone development, and probably justifiable to interpret them as representing successive steps in the evolution of bone, it must not be supposed that they are absolutely distinct : intermediate forms occur frequently and a single bone of the adult may arise during ontogeny in part according to one type and in part according to another.

Bony tissue being rigid and inextensihle, it is essential to the functions of movement and growth, that it should not be continuous throughout the body. It consequently. takes the form of separate bones, the junctions between which are specialized either for movement, or for addition of new bony tissue at their margins. Each bone arises by the spreading outwards of bony tissue from one or more centres of ossiﬁcation. The study of the arrangement and homology of the various bones constitutes an important part of the science of Comparative Anatomy———particular1y important for the reason that it is the bony skeleton alone which is as a rule preserved in the fossil remains of Vertebrates belonging to past phases of Evolution.

lt should be borne in mind that a single bony plate in such a part of the skeleton as the skull may represent ossiﬁcation which has spread out irregularly from the bases of a large number of the original placoid elements. In View of this it will be realized that great caution must be exercised in homologizing apparently similar bones in different groups of the lower Vertebrates. Thus the same name ——implying homology-——is commonly given to similar bones in the skull of a (lrossopterygian, an Actinopterygian, and a Lung-ﬁsh or Amphibian. There is no guarantee of any precise homology in such cases and the student should be on his guard against taking very seriously the nomenclature of such bones as expressing exact and Well-determined homology.

FISH SCALEs.————In the Fishes, that is in those Gnatliostomata in which the skin has not yet become specialized for Respiration (Amphibians), or for protection against desiccation (Reptiles), or for diminishing loss of heat (Birds and Mammals), there is commonly present a coating of dermal bones which most usually take the form of scales. Such scales are in the most general terms simply plates of bone in one or other of its varieties. The development of what is probably the most primitive type-—the placoid scale—--has already been dealt with. It need only be added that individual scales, interspersed regularly amongst the others, pause in their development, and 336 EMBRYOLOGY OF THE LOWER VERTEBRATES Cu.

only proceed with the process when room is provided by the already developed scales becoming spaced out during the growth of the bod .

Tlfhilc the placoid scale is simply an individual dermal tooth the ganoid scales as seen in the surviving .l’0lg/ptems or Lejmltlosteus are on the other hand tooth-plates, numerous minute dentieles being associated with each sca.le. In these ﬁshes also there is a certain amount of independence between the dermal plate of bone and the actual dentieles which are at first quite separate from it (N ickerson, 1893 ; Goodrich, 1908). The reduction in size of the dental cones and the loss of their attachment to the bony plate are steps towards their complete disappearance which has been reached in the scales of ordinary Teleostean lishcs.

In the ganoid scale of I’o/;c/pter-as or lugnidosteus the protective power of the bony plate has been greatly increased by its superﬁcial layers undergoing modilication of an analogous kind to that of the superﬁcial layers of the dentine cone in the teeth of ﬁshes. This portion of the scale is extremely dense, hard and enamel-like and is without cells embedded in it. Like the corresponding layer in the tooth of a ﬁsh it is commonly known by Williamson's name Ganoine. The advisability of using this name, rather than enamel, rests mainly upon the assumption that enamel is a substance fundamentally

dilferent, derived from a different eell—layer, from bone or dentine. If

it be the case however that enamel is merely the superﬁcial layer of dentine which has undergone secondary modiﬁcation then there seems no particular harm in adhering to the custom—-until- recent years quite general-—-—of using the word enamel for the superﬁcial layer of the ganoid scale.

Ganoid scales are still comparatively thick and bulky structures but in the typical Teleosts the scales have become very thin plates of bone so modiﬁed as to be very tough and ﬂexible, and overlapping like slates on a roof so as to be able to slide over one another during flexure of the body. This overlapping has been rendered possible owing to the surface of the scale being no longer inseparably linked to the ectoderm by the development of teeth. The scale is developed in the thickness of the dermis and it is only at its posterior edge, if anywhere, that it is even in early stages connected with the epidermis.

Vestiges of dermal dentieles have been described in Teleostean ﬁshes and these deserve fuller investigation. Marett Tims (1906) describes a stage in Gadus in which the scale consists of separate platelets each with a tooth-like spine projecting from it, while in such South American Siluroids as Uallvlc/Ltlz,y.s and Loricaria the plates of the bony cuirasse bear numerous small spines which appear

to be typically tooth-like in structure. The scale is a plate of bone immersed in the dermis and it

therefore naturally grows by the addition of new bone all over its surface. In the ganoid scale the quality of the bone differs on the V THE SKELETON 337

inner and outer surfaces, that formed on the outer surface being the enamel or ganoine already referred to. In the highly evolved Teleost, where the scale has increased in area at the expense of thickness, the addition of new bone on the Hat inner and outer surfaces of the scale is relatively small in amount as compared with that round the edges. \

In accordance with variations from time to time in the metabolic activity concerned in the production of the new bone the latter tends to show variations in rapidity of growth, density and other characters, and consequently to show a more or less distinct layered arrangement. Where there are periodic variations in the metabolism of the ﬁsh-—associated it may be with sexual‘ activity or with food supply or with changes in the physical environment (6.;/. seasonal changes of temperature)»-these variations may be duly chronicled in the contemporary layers of the scales. Such scale records are often particularly distinct and easily observed in the scales of the Teleostei owing to their thin ﬂat character and the predominance of growth at their edges. "

The development of the Cycloid scales of Dipnoi has not been investigated in detail. So far as the main features of their development are concerned they apparently resemble the scales of Teleosts. Like them they are, except at their posterior edge, deeply embedded in the dermis. On their outer surface they are prolonged into numerous, often recurved, spines which in all probability represent true denticles although they have lost their primitive relation to the epidermis.

BONY VER'1‘l«:nRAI. COLUMN.——II1 all gnathostoniatous Vertebrates, except the Elasmobranchs (including Holocephali) and Sturgeons, the vertebral column becomes in great part bony. The process of ossiﬁcation is found in its first beginnings in the Lung-ﬁshes, where the arches become ensheathed in bone.

In the bony Ganoids and Teleosts ossiﬁcation usually commences in the connective tissue bounding the surface of the areualia, the ﬁrst shreds of bone being completely coll-less. From the arches the bone spreads over the surface of the chordal sheath (in Amia it develops here iirst -Schauinsland) to form the rudiment of the bony centrum. In 6'0'reg()'Iuts it is stated (Albrecht, 1902) that for a time two bony rings can be distinguished round each centrum (of. variation in Am/(Ia. mentioned below on p. 339). From the thin superﬁcial sheath of bone an irrogl1la1' spongework of bony trabcculae spreads outwards and forms the bulky centrum of the deﬁnitive vertebra. As this process goes on the basal portions of the cartilaginous arches become surrounded by bone and may persist as four tracts of cartilage running outwards through the bony centrum (e.g. Esom—Pike). Most usually the arches become completely bony: the original bony sheath covering their surface becomes perforated on its median side by invading vascular connective tissue which destroys the cartilage and deposits bone in its place.

VOL. II Z 338 EMBRYOLOGY OF THE LOWER VERTEBRATES C11.

The neural spine even when segmented in the cartilaginous condition becomes ensheathed in a continuous layer of bone.

In the case of Teleosts the cartilaginous stage of the haemal arches is frequently completely eliminated from development, the arches being laid down as bone in the connective tissue.

ln the Urodele Amphihia bone makes its appearance as a cellless sheath round the surface of the centrum, which gradually increases in thickness and becomes cellular, enclosing connectivetissuc cells, and also spreads over the surface of the areualia. The cartilage becomes gradually absorbed and replaced by the bone.

ln S'phenucl072., which may be taken as an example of the more primitive Reptiles, a bony sheath similarly develops round the eentruin, but according to Sehauinsland it consists at first of a distinct dorsal and ventral half. The bony tissue of the dorsal portion spreads upwards so as to enclose the bases of the neural archelements but the main portion of the arch-element on each side becomes enclosed in an independent bony sheath of its own. This latter appears first on the outer side of the cartilaginous arch and may persist as a separate bony element for a long period, even throughout life in the Crocodiles and various other Reptiles.

Bone formation also spreads inwards into the substance of the cartilaginous centrum along what possibly corresponds to the boundary between the primary centrum and the chondriﬁed tissue external to it (Fig. 152, p. 302). Thus arises a deep-seated centre of active bone formation.

From these various centres ossiﬁcation spreads, the cartilage being gradually supplanted by bone. Not the whole of the bone so deposited is permanent: a great part of that lying outside the primary centrum becomes again absorbed, leaving a superﬁcial tract connected with the more central portion only by sparse bony trabeculae, the meshes being occupied by intrusive connective tissue.

An interesting adaptive feature is found in the tail region of certain Reptiles (Lizards, Sphe’It0/.l07t) which enables the possessor to break off its tail suddenly when seized by an enemy. In these animals the halves of the centrum derived from successive sclerotomes have reverted to a condition of incomplete fusion—the ossiﬁcation being more or less interrupted in the plane of contact of the two successive sclerotomes by a transverse septum of cartilage. As at the same time the corresponding connective-tissue septum between consecutive myotomes remains weaker than usual a violent contraction of the caudal muscles is able to tear across both cartilaginous and connective-tissue septum and break off the distal portion of the tail.

In the case of the Birds it would appear that the main centre of ossiﬁcation of the centrum corresponds to the deep-seated one in Sphenodon, the superﬁcial bone-forming activity being much reduced. A characteristic feature of the Birds, associated primarily with their peculiar respiratory movements, is the extensive fusion which takes place between the vertebrae of the trunk region. v THE DEFINITIVE VERTEBRA 339

THE OoMPo‘s1'r1oN or THE DEFINITIVE VERTEBRA.--—-A fascinating but difficult chapter in Vertebrate morphology is that which deals with the composition of the deﬁnitive vertebra. We have already, in describing the development of the cartilaginous vertebral column, mentioned the elements which go to build it up—-neural, haemal, and central. The difficulties of interpretation arise from the fact that great variety shows itself in the ultimate fate of these elements and in the manner in which they undergo l'usion with their neighbours. This can perhaps best be illustrated by the case of Amie as described

FIG. l66.——Variation in vertebral column of A inria, according to Schauinsland (1906).

A, tail region of a 7-5 nnn. larva; B, postc,-.rier trunk region of an 18 cm. specimen ; 0, mid trunk 1-egion(lS (:.m.); 1), anterior trunk region (18 cm.). Fig. A is more highly magniﬁed than B, C, and D. The position of the boundaries between successive myot.-omes or segnients is indicated by the intersegmental blood-vessels (-19). A, Ii, neural arch-elements; a, h, haemal arch do. ; a, 3, central do.

by Schauinsland. Here in some cases two amphicoelous centre (a. and ,8) are developed corresponding to a single segment, each one carrying its pair of neural and pair of haemal elements, those attached to the anterior centrum (A and ca) being relatively small, those on the posterior centrum (B and b) on the other hand well developed. Variations from this diagrammatic arrangement are found in different parts of the body. In the tail region (Fig. 166, A) the original condition frequently persists although in aged individuals the arch-elements (A, a) of the , anterior vertebra of the segment are liable to become completely overgrown and hidden by bone. On the other hand there frequently 340 EMBRYOLOGY OF THE LOWER VERTEBBATES CH.

takes place fusion between adjacent centra so that compound centra are produced. Most usually in this case it is thetwo centre (a, B) of one segment which undergo fusion but in some cases the posterior centrum of one segment fuses with the anterior centrum of the next so that the resulting compound vertebral centrum (/3 a) belongs to two successive segments. Again in some cases as exempliﬁed by the specimen ﬁgured (Fig. 166, A) three successive centra may undergo fusion.

Towards the front end of the tail and throughout the trunk region the two centra of one segment undergo fusion but apparently the hinder ccntrum has undergone reduction in size with the result that its neural arch-element (B) becomes displaced on to the top of the smaller anterior element (A) (Fig. 166, B, (3).

Towards the extreme front end of the trunk the neural element B becomes practically intervertebral in position (Fig. 166, 1)). It is to be noticed that in these cases, where the element 12’ has been displaced, the bony splints which develop on its surface never spread downwards from it, so that it remains throughout life without any continuity of structure with the rest of the vertebra.

Towards the tip of the tail there is, apparently no regularity, all kinds of fusions and modifications of the various elements taking

lace. P To sum up we see in Amvla two complete potential vertebrae corresponding to each segment,‘ each with its central, its neural and its haemal elements.

The two vertebrae of a segment may be represented by the

A B formulae and !l3'where a and /3 are the centra, A a11d;1>’_{tl1e neural a 5 '

arch-elements and a and b the haemal arch-elements. In the trunk region the ordinary compound vertebra may be represented thus

AB

in./3 but in occasional cases fusions take place so as to produce vertebrae ab

BA ABA ABAB of the type or of the type pnﬁti or'a-[id/3 . Such a fusion as ba. aba _c-zlbalii

that shown in the last formula produces a vertebra with a very long body upon which may persist four sets of neural and four sets of haemaleleinents. The great range of variation seen in Amie from the presumedly original condition, even in different regions of the vertebral column of one individual, emphasizes the need of much caution in the laying down of general principles regarding the composition of the deﬁnitive vertebra. It seems justifiable to admit the two pairs of neural and two pairs of haemal arch - elements into the general

1 Diplospondylous condition-—von Jhering. v THE SKELETON 341

scheme of a vertebral segment in addition to the central element. But a difficulty is at once raised by the not infrequent appearance (as in Amid and many Elasmobranchs) of two centra within the limits of a segment. To get over this it has been suggested that primitively there were actually present two complete vertebrae, each with centrum, neural arch and haemal arch, within the limits of a single segment (dispondylous or diplospondylous condition). Physiological considerations however support the probability of there having been primitively a single vertebral centrum, extending from about the middle of one pair of myotmnes to about the middle of the next pair. If it is borne in mind that the material of the anterior and posterior halves of the centrum is derived from two independent sources—-successive pairs of arch-elenients or of sclerotomes—it will seem reasonable to explain the occasional duplicity as due primarily to absence of the complete fusion which normally comes about between the halves of the centrum derived from the two sources, the two halves proceeding with their development independently. Conversely a more complete fusion, extending over a number of these potential half-vertebrae instead of merely two of them, would lead to cases of elongated definitive vertebrae carrying a number of arches.

BONY Sl(ULL.——Tl10 caution expressed on p. 335 is especially necessary in connexion with the bones of the skull. Here we have a department of morphology which took shape in the early days of that science. The efforts of the older anatomists were devoted to the working out of homologies between the bones of different groups of Vertebrates and individual bones were given the same name-—they were decided to be homologous——mainly on the basis of similarity of relations in the adult animal, with only the most slender basis of either palaeontological or embryological knowledge. The consequent uncertainty as to the precise homology of similarly named bones in different groups of Vertebrates makes it in the author’s opinion impossible to write a satisfactory account without treating each of the main groups in detail by itself. As to do this would require more space than is available he would refer readers who desire such information to Gaupp’s volume and the literature there cited and will confine himself here to a very brief sketch.

In the lowest Gnathostomata, as represented at the present day by the Elasmobranch ﬁshes, the skull retains throughout life its cartilaginous character, the bony tissue being conﬁned to the placoid elements of the skin. In the other groups of Gnathostomata the purely cartilaginous condition is temporary, the cartilaginous skull becoming strengthened and in places, though never entirely, replaced b bone.

y In the floor of the chondrocranium there make their appearance a mid-ventral row of replacement bones the basi-occipital, the basisphenoid, and the presphenoid. Laterally to each of these elements the cartilage becomes replaced by a pair of bones known respectively 342 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

. as the exoccipitals, the alisphenoids and the orbitosphenoids. In

the occipital region the cartilaginous roof gives way to a replacement bone——tl1e supraoccipital--—but in the corresponding region further forwards the cartilage either does not develop or if it does develop never becomes replaced by bone.‘

In addition to the three groups of replacement bones mentioned, the cartilage of the sensory capsules gives way to replacement bones. In the wall of the auditory capsule there develops anteriorly a prootic and in the remaining part of the capsule wall there develop other ossiﬁcations differing in number in dilferent groups——as many as four in the ease of Teleostean ﬁshes ———~ epiotic, opisthotic, sphenotic and pterotic. The wall of the olfactory capsule similarly becomes replaced by ethmoid, b«_mos—varying much in the difl'erent groups. The wall of the eyeball in a few cases develops a ring of ﬂattened replacement bones in the substance of the sclerotic.

In addition to the replacement bones already indicated there develop others in connexion with the visceral arches. Thus we ﬁnd the upper portion of the mandibular arch becoming replaced by the quadrate, the upper portion of the lower jaw by the articular and the palato—pterygoid outgrowth by palatine and pterygoid elements which however exhibit great diﬁ"erences in their mode of development. The segments of the hyoid and branchial arches become replaced by various hyal and branchial bones in the bony ﬁshes.

The bony skull is completed by numerous more superficially placed bones—-some belonging to the ordinary investment type, others retaining their dental character. The cranial roof immediately in front of the occipital region is typically covered by a pair of parietal bones; in front of these are a pair of frontals. In the Amniota particularly are developed such additional elements as squamosal, postfrontal, jugal. The Ethmoidal region develops such bones as nasal, prefrontal, lachrymal, septomaxillary.

In the region of the buccal cavity we ﬁnd a particularly rich development of investment and dental bones. The function of upper jaw, originally exercised by the palate-pterygoid bar, becomes taken over by new bones--the maxilla and premaxilla~—-lying external to it, the palate-pterygoid bar becoming shunted inwards except its hinder quadrate portion and no longer forming the margin of the buccal cavity. Behind the maxilla or jugal there may develop a quadrato-jugal: in the region of the palate-pterygoid parts of the palatine and pterygoid are of this origin and so also are the vomer and parasphenoid.

Just as the primitive upper jaw becomes replaced functionally by bones of superﬁcial origin, so also with the lower jaw-the original Meckel’s cartilage becoming ensheathed by splenial and dentary (the latter taking on the tooth-bearing function) with such other bones as angular, supra - angular, and coronoid. In

1 The pleuroccipital bone of the Dipnoi arises as afelose investment of the occipital arch (Agar, 1906). V BONES OF SKULL ' 343 '

the region of the Hyoid arch the Teleostomatous ﬁshes with their greatly developed operculum develop a series of opercular bones.

Of these various bones mentioned in relation with the buccal cavity and pharynx the majority show more or less distinct evidence of their dental origin [l’remaxilla, Maxilla, Dentary, Palatine, Pterygoid, Vomer, Parasphenoid, ()pereular——cf. Hertwig,18'74*]. In some cases this maybe apparent only in part of the bone, the rest developing as an ordinary investment bone, while in a few cases bone which is in one part of the investing type may in another part present all the features of a replacement bone.

The student should recognize that the ossiﬁcation of the skull, though tlillering greatly in degree in diﬂerent Vertebrates, is never complete. In the adult Elasmobranch the cranium is entirely cartilaginous, bone being confined to the placoid scales : in a Sturgeon there is still a well-developed chondroeranium but the surface of the head is covered with large bony plates: in such a T eleost as the Salmon the chondroeranium also persists to a great extent but extensive tracts of the cartilage are replaced by bone while the superﬁcial plates of bone are now in much more intimate relations to the surface of the cartilage: in such a Teleost as a God again the cartilage is reduced in the adult to such an extent as to be quite inconspicuous. It never however completely disappears and the macerated skull of a Vertebrate as seen in an osteological or palaeontological collection is imperfect, being without parts which maybe of great morphological signiﬁcance.

AUDITORY SKELETON.-——ln those Tetrapoda in which a tympanic membrane is present the vibrations of this membrane are transmitted through the tympanic cavity to a movable portion of the wall of the auditory capsule by a special arrangement of skeletal structures. These reach their highest development in the auditory ossicles of the Manimalia which have attracted much attention from students of mammalian anatomy and have been the centre of much controversy as to their phylogenetic origin. In the non-mammalian Vertebrates the two outer members of the chain of ossieles—the malleus and incus—have not yet made their appearance so that we are only concerned in this volume with the inner or stapedial portion which is represented in the Sauropsida and most of the Anura by the columella. auris. It will be convenient to study the development of this in the case of the Lacertilia in which it has been recently investigated by Versluys (1903), Cords (1909) and Goodrich (1915).

It will be recalled that the tympanic cavity is the dilated outer end of the spiracular or hyomandibular gill pouch, and the Eustachian tube is the inner or pharyngeal portion of this pouch. The pouch is for a time open to the exterior, forming an ordinary spiracular cleft, bounded in front by the mandibular and behind by the hyoid arch. In the hyoid arch is situated the main branch (hyomandibular) of the Facial nerve and from this, near its dorsal end, there comes off a branch—the chorda. tympani——-which runs in a ventral direction ‘344 EMBRYOLOGY OF THE LOWER VERTEBRATES on.

behind the cleft to its lower limit and then curves forwards beneath the cleft towards the region of the lower jaw and ﬂoor of the buccal cavity.

The external opening of the spiracular cleft gradually closes, from below upwards, as is usual with this cleft, a stage being passed through in which only the dorsal end of the cleft is open - precisely as in the adult of an ordinary Elasmobranch. As the lower limit of the opening gradually shifts dorsalwards the ehorda tympani remains in close relation with it so that the portion of the nerve on the ventral side of the opening assumes a more and more dorsal position. Eventually even the dorsal vestige of the cleft closes so that the spiracle has now reverted to the condition of a pouch. Owing to the shifting in position of the ehorda tympani as it followed the

retreating lower edge of the spiracular opening this nerve now .

passes forwards dorsal to the main portion of the pouch, instead of entirely ventral to it as it did originally.

The dilatation of the outer end of the pouch to form the tympanic cavity is brought about mainly by active growth of the lower portion of its posterior wall. This bulges outwards and spreads forwards and dorsalwards beneath the epidermis, from which however it remains for a time separated by a considerable thickness of mcsenchyme. Later on this thins out relatively so that the three layers bounding the tympanic cavity on its outer side—endoderm, mesenchyme, ectoderm——form a thin 1nembrane——-the tympanic membrane. As the tympanic dilatation goes on expanding in a dorsal and anterior direction the ehorda tympani becomes displaced in front of it still further from its original position.

In the mesenehyme of the hyoid arch there takes place a gradual condensation to form the rudiment of the skeletal arch. The lower and main portion of this condensation becomes the cartilage of the deﬁnitive main cornu of the hyoid. lts dorsal portion also becomes converted into cartilage, taking the form of a stout red the inner (“stapedial”) end of which ﬁts into the fenestra ova.lis——a vacuity in the wall of the auditory capsule——while its outer portion (“extra-columella,” Gadow) extends outwards towards the skin, embedded in the mesenchyme of the posterior wall of the spiracular pouch or tympanic cavity. Finally the lining of this cavity grows actively dorsally and ventrally to the columella so that it bulges backwards both above and below the columella. The pockets of tympanic lining so formed meet round the columella and fuse together so that the columella, instead of being embedded in the hind wall of the cavity, new passes right through it, enclosed in a delicate sheath of mesenchyme covered with endoderm. The extension of the tympanic cavity backwards past the columella causes an extension of the tympanic membrane in the same direction so that the point at which the tip of the extra-columella reaches the skin, instead of being situated behind the tympanic membrane as it was originally, comes to be about the centre of that membrane. V AUDITO RY SKELETON 345

The general mode of development of the columella and the cavities associated with it as seen in Lcu:e"t(t appears to be typical of the Sauropsida in general. It is now necessary to refer to a few additional details. _

The inner end of the eolumella (stapes) fits into the fenestra ovalis. It is for a time, during prochondral or cartilaginous stages or both, continuous with the Wall of the auditory capsule and is probably to be interpreted as a portion of this wall which has become separate and movable.

C‘»hondriﬁcation of the columella commences in the Lacertilia from three centres according to Versluys and it is to be noted‘ that the separation between extra-columella and stapes arises secondarily within the region of cartilage which develops from the innermost centre.

In Birds an interesting variation has been discovered (Goodrich, 1915) in the relations of the chorda tympani. In the Duck these are normal, agreeing with what has been described for Lacerta. In the ordinary Fowl and the Turkey however the stage in which the chorda tympani is posterior to the hyomandibular cleft is omitted from development. Even in early stages it is found to pass in front of the pouch or cleft.

This is one of those cases which emphasizes the need of caution in regarding the course of a nerve as a necessarily deciding factor in discussions as to the morphological nature of particular organs. Position in regard to a particular nerve-trunk often affords us most valuable evidence regarding the primitive position of an organ. Here, however, we have it impressed upon us that we must never rely absolutely upon such a piece of evidence taken by itself. Were we to do so in this case we should be led into the absurdity of concluding that the tympanic cavity of the Turkey is not homologous with that of the Duck.

As a matter of fact nerve-trunks do not always form impassable barriers to the evolutionary change in position of organs. A skeletal structure may spread round a nerve-trunk (e.g. neural arches of Dog-ﬁsh) and becoming absorbed behind it may come to be transposed entirely past the nerve. In the case of the chorda tympani and the tympanic cavity it is clear that the nerve lay primitively behind and below the cavity and we may probably take it that, in accordance with the general principle that nerve-trunks tend to shorten and so economize material, in the course of evolution it became shifted dorsalwards through the mesenchymatous middle layer of the outer wall of the tympanic cavity before it became thin and membranous, so as eventually to lie completely dorsal and anterior to the tympanic membrane.

Incidentally the variation from normal development occurring in the Turkey and Fowl is one of those cases apparently impossible to explain on the outgrowth theory of nerve-development, but readily understandable on the view of nerve - development supported in 346 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

Chapter II., according to which new nerve-paths may arise in response to the short circuiting of nerve-impulses.

A tympanic cavity with membrane and columella occurs in many of the Anura——as for example the ordinary Frogs and Toads (Rana, Bufo)--while in others such as the genera 1>’ombz'na.to7' and Atnlopus (“ P/W3/n?I.9cus") it is absent. In the Urodele Amphibians the tympanic cavity and membrane have not yet made their appearance. The inner end of the columella is however represented by a movable plate of cartilage ﬁtted into the fenestra and in various genera the extra-columellar portion is represented by a rod-like outgrowth from this. The former apparently develops from the auditory capsule while regarding the latter there is much diflerence of opinion as to the extent of its relation to the cartilage of the hyoid arch. The disagreement between different observers probably means that there are actual differences between diiferent genera of Amphibia. This is quite what is to be expected, for whenever we ﬁnd a single organ of which part is derived from one embryonic source and part from another the proportion contributed by the two sources is liable to vary, so that in one case it may be the portion derived from the one source which is conspicuous and in another case that derived from the other.

The tympanic ring‘ within which the tympanic membrane is stretched arises in the form of an outgrowth from the rudiment of the quadrate, 73.5. from the upper portion of the skeleton of the mandibular arch. This outgrowth separates off and grows round the outer end of the hyomandibular pouch in the form of a crescent the two horns of which eventually meet to form a complete ring.

SKELETON or THE MEI)IAN on UNPAIRE1) FlNS.———The median ﬁn, thin and membranous as it is in its most highly evolved condition, is supported by characteristic skeletal arrangements. Into these two distinct elements enter, one mesial represented by rays of cartilage or bone (radials), the other superﬁcial and of dermal origin.

The mesial ﬁn-rays are frequently i11 close ' relation to the neural and haemal arches and it is reasonable to suppose that in the process of evolution, as the hind end of the body became extended in a dorsal and ventral direction, so as to attain to the ﬂattened form conducive to efficiency in propelling the body, the neural and haemal spines underwent a corresponding extension for the purposes of support. This view is corroborated by the existing Dipnoi in which the mesial ﬁn remains a comparatively slightly diﬁ"erentiated extension of the body dorsally and ventrally and in which the mesial supporting elements are simply the prolonged neural and haemal spines, each secondarily subdivided into three segments. The same is the case in Fishes generally so far as the ventral portion of the caudal ﬁn is concerned in which the mesial supports develop also for the most part as typical haemal spines.

The mesial supports of the dorsal portion of the median ﬁn on the contrary do not in Fishes generally show this relation to the i oped at particular points

V MEDIAN FIN SKELl£'I.‘ON 347

vertebral arches. They arise, any. in Elasmobranchs, in ontogeny as independent rods of cartilage without deﬁnite relation to the metamerism of the body and later on become segmented into three pieces. In those cases, so far as they have been investigated, in which the radial elements are connected with a continuous basal plate of cartilage, this latter appears to arise in ontogeny as a continuous plate, though there is no reason to doubt that it arose in phylogeny by the fusion together of the basal portions of originally separate rays.

This want of correspondence of themesial elements of the dorsal ﬁn skeleton with the vertebrae is probably sufﬁciently explained as a secondary result of the prolonged working of the general principles which have governed the evolution of the median fin and which ﬁnd their expression in the tendencies (1) of the continuous ﬁn to become specially devel and to die away in the intervening spaces, (2) of the resulting separate ﬁns to have their base of attachment to the body shortened and (3) of these ﬁns to be situated on the body at the points

where they are mechanic- s

most effective. FIG. 167.——Two sticeessive stages in the development DERMAL SUPPORTS OF of the lepi(lotl'iclnia of Srrlmu.

MEDIAN FINS. __ The A, Sahnon (afte-r Harrison, 1893); B, 'l‘rout.(aft:-r(l0odricl1, . ﬁ b . . 1904). h.m, lmsa.-nu-nl. llll‘llll_|l':|nl‘: m'I_, m-hulv1'n1 : I, lvp1«'lonledlan ns 9138 PH’ triuhial rudiment: ; ma__'.~', lIln'.-‘o*.lIt'll_\'lIlt? of dc-r1ni.~'.

marily mere extensions of

the body in the vertical plane it would only be reasonable to expect that they would show traces of skeletal elements comparable with the placoid elements or their derivatives characteristic of the rest of the surface. And in fact the dermal skeletal supports of the median ﬁns can, some of them, he clearly recognized as homologous with scales, while in others although this may no longer be recognizable their origin is found to be closely associated with the basement membrane as was the case with the dermal teeth.

_It will be convenient to consider ﬁrst of all the dermal skeletal elements in which the direct relation to scales is most clear. Such are the bony ﬁn-rays of Crossopterygian and Actinopterygian ﬁshes. In an ordinary Telecst (Fig. 167) the ﬁn-rays of this type (lepidotrichia, Goodrich) appear in their earliest stage, as shown by 348 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

Harrison (1893), in the form of a localized thickening of the basement membrane underlying the ectoderm. This thickening becomes more and more marked and eventually separates oil’ round its edges in the manner shown in Fig. 167, ll, mesenchyme insinuating itself all round between the ray and the basement membrane, so that the former eventually lies free from the basement membrane (or in some cases still connected with it by narrow bridges) deep dow11 in the mesenchyme. The ray soon,beoo1ncs calciﬁed. New layers are deposited on its inner and outer surfaces, mesenchyme cells become included within its substance and it becomes a plate of ordinary bone. The rays are elongated structures which develop from the [in base towards the tip. They often become jointed, either by calcification being interrupted at intervals (Goodrich) or by a secondary solution of continuity (Harrison).

ltays are formed in the manner described on each surface of the thin membranous ﬁn. The rays of opposite sides correspond exactly in position and become later on [used across the mesial plane so as to form a single unpaired ray whose paired origin is indicated only by its forking at its inner end to embrace the tip of the median radial, the process of fusion between the two elements not taking place at this proximal end. In the dorsal and anal ﬁns and in the ventral part of the caudal ﬁn the lepidotriehial ﬁn-rays correspond segment-ally with the true median skeletal elements the tips of which they embrace as indicated above.

In the more primitive Toleostoines the identity in nature of these ﬁn-rays with the scales which cover the rest of the body is still more obvious. ln Pol;/pterus and Lepidosteus they develop a coating of ganoine and even hear distinct small dentieles on their surface. It is also interesting to notice that in the anal ﬁn and ventral part of the caudal ﬁn of Poly/pterus the ﬁn-rays at their proximal ends merely pass in beneath the edges of the body scales and do not take .on any relation to the true median skeletal elements. The palaeontological fact may be recalled in passing that in some of the extinct ﬁshes a perfect gradation can be traced between the ﬁn-rays and typical body scales (see Goodrich, 1904).

In addition to the ﬁn-rays just described, the homology of which with scales may be taken as well established, it is very usual to ﬁnd another type of ﬁn-ray in which this homelogy is not so obvious. This is exempliﬁed by the horny ﬁn-rays (see Goodrich, 1904) which occur in the ﬁns of Elasmobranehs (including Holocephali), in the “adipose” ﬁn of Salmonids and Siluroids, and towards the margins of the ﬁns generally in adult Ganoids and Teleosts. These horny ﬁn—rays develop either as thickenings of the basement membrane or at least in immediate contact with it. Mesenchyme cells insinuate themselves between the ray and the basement membrane as the ray separates oﬁ". The ray gradually becomes farther removed from the basement membrane and mesenchyme cells collecting round it deposit fresh layers on its V FIN-RAYS 349

surface so that its diameter becomes increased. In the ﬁns of Elasmobranchs and in the adipose ﬁns of '_l‘eleosts these horny ﬁnrays become much elongated, but ordinarily inlthe Teleostoinc they become relatively shortened during development, apparently being absorbed at their proximal ends while they grow at their distal ends, so that in the fully developed lin they form merely a marginal fringe-—the individual horny rays being concentrated about the ends of the lepidotriehia.

The ﬁn-rays in question have‘the main feature in common with the lepidotriehia that they arise in very close relation to the basement membrane and later on separate from it and sink into the underlying mesenchyme. It is probably allowable to look upon them as being of the same nature morphologically as the lepidotriehia but as having evolved still farther from the primitive scale-like condition. In Lung-ﬁshes horny ﬁn-rays occur of somewhat intermediate character in the form of slender parallel rods irregularly jointed and branched distally. In the later stages of their development these rays are apt to assume a bony character, becoming strongly calciﬁed and enclosing branched bone corpuscles in their substance. The early development of these rays has not, so far, been worked out

‘ in Oaratodus in which they are best developed. In Protopte'rus

Goodrich found them in early stages in at least very close proximity to the basement membrane.

We may probably look upon the dermal fin-rays of ﬁshes as belonging to one morphological category, representing structures of originally placoid nature which have sunk down into the mesenchyme and degenerated, or-——to use a preferable expression--become specialized, into more or less horny structures. The earliest stage in ‘this process we should see in the lepidotriehia of Teleostomatous ﬁshes where the scaly nature is still quite clear. The ﬁn-rays of Lungﬁshes would represent a farther stage, in which the scale homology is no longer clear, and the horny rays of Elasmobranchs and Teleostomes would represent the ﬁnal stage, in which all trace of the original nature had disappeared except the origin in close association with the basement membrane.

The lepidotriehia of the Teleost and its horny ﬁn-rays would represent different generations, the lepidotriehia being a later generation which have, as it were, had less time for modiﬁcation. In this connexion it should be mentioned that the horny ﬁn-rays of the Elasmobranch do not all belong to one generation. Their production from the basement membrane may go on for a long period so that instead of a single layer a thick mass of rays may be developed.

SKELETON OF THE PAIRED LIMBS

I. FINs.—-To be consistent with the plan adopted in this book we should commence with the development of the paired ﬁn in its most

nearly primitive existing form. Before this can be done it is necessary 350 EMBRYOLOGY OF THE LOWER VERTEBRATES OH.

to decide which is the most nearly primitive of the various forms of paired ﬁn met with in surviving ﬁshes. The present writer takes the view that undoubtedly the most primitive type of paired ﬁn known to occur in existing Vertebrates is the paddle-like limb of Ceratodus.

Physiologically this type of ﬁn is as clumsy and archaic an organ in‘

comparison with the paired ﬁn of a Shark or Actinopterygian ﬁsh as is the most primitive type of savage’s paddle compared with a racing car. Further we know from the data of palaeontology that the Oeratodus type of limb is of great antiquity and that it was a common type of ﬁn amongst the more ancient Sharks and Ganoids as well as amongst the Lung-ﬁshes. There are only two possible explanations of its occurrence in the three groups mentioned. Either (I) it is an archaic type of 1111 inherited from the common ancestors of those groups or (2) it has been evolved independently in the three groups. The latter explanation seems very improbable-—~for such a type of organ would become evolved independently in different groups, only if it were physiologically very eﬁicient. But it seems quite impossible with knowledge of the structure of the limb of Cemtoalus and its use in the living animal to regard it as an organ of great locomotor efficiency. Apart from this consideration we have the historical fact that this type of ﬁn has vanished away entirely in the two successful types of ﬁsh, the Sharks and the Teleostomes, and has persisted unchanged only in one of the surviving Lung-ﬁshes. There seems then no escaping the ﬁrst of the two possible conclusions mentioned above, that the paddle-like ﬁn of Oemtodus and the ancient Lung—ﬁshes, Ganoids and Sharks is a common heritage from the ancestral group out of which these ﬁshes evolved and is therefore the most archaic of the known types of paired ﬁn.

DEVELOPMENT or THE PECTORAL LIMB SKELETON IN CERATODUS. The skeleton of the limb makes its ﬁrst appearance (Semen, 1898) about stage 45 (Fig. 201) as a rod-like condensation of connective tissue along the axis of the limb which tapers gradually towards the apex. Histological diﬁerentiation, by which this rod-like structure passes through a prochondral into a completely chondriﬁed condition, proceeds from the base towards the apex. While in the prochondral condition the rod is a continuous structure, chondriﬁcation takes place from separate centres, with the result that the rod becomes converted into a series of blocks of cartilage, each separated from its neighbours by a thin layer of unchondriﬁed tissue. The basal block, lying within the body wall and spreading in a ventral direction, is the rudiment of the pectoral girdle; the rest of the series forms the axis of the limb.

The lateral rays make their appearance later, the development again proceeding from base towards apex, and those on the preaxial or deﬁnitively dorsal side preceding those on the postaxial or deﬁnitively ventral. Each ray spreads out from the prochondral tissue between two segments of the axis and it is noteworthy that rays develop from the ﬁrst (proximal) of these intersegmental joints although in V PECTORAL LIMB SKELETON 351

the course of further development these, doubtless to give greater mobility to the ﬁn, disappear. In the details of its development each ray repeats that of the main axis.

In addition to the normal rays, which are attached to the axis at the level of the intersegmental spaces, occasional rays make their appearance opposite the segments themselves. According to Semen these sprout out from the thin superﬁcial layer of the axial tissue which like that between the segments persists for long in an unchondrified condition. These extra rays are most frequent on the postaxial side of the limb which in the pectoral limb becomes ventral, in the ease of the pelvic limb dorsal (see Chap. VII.).

Growth of the ﬁn and of its enclosed skeleton continues for a long period-—-even after the adult condition is attained. As regards the skeleton this continued process of growth takes place by‘ two methods (1) by a simple continuation of the extension at the apex, and (2) by the already formed elements of the cartilaginous skeleton, axial orradial, continuing their individual growth in size.

As the deﬁnitive condition of the ‘skeleton is reached, the interscgmental tissue chondriﬁes, towards the apex forming soft hyaline cartilage with a sparse matrix and towards the body taking the form of ﬁbro-cartilage. Towards the base of the limb this ﬁbre-cartilage develops many ﬂuid-ﬁlled cavities so as to assume an almost spongy character and in this way give greater mobility. This is specially marked at the junction with the shoulder girdle and between the ﬁrst and second segments of the limb—axis and in these -two cases the apposed surfaces of hyaline cartilage are curved and concentric so as to afford a distinct development in the direction of a true ball and socket joint.

The details of development of the pelvic limb skeleton apparently agree with those of the pectoral. In this case also the girdle arises in the form of two originally separate halves.

ELASMOBRANCIIII.——The earliest stage in the development of the pectoral limb and its girdle in Elasmobranehs is that described by Ruge and by Braus (1904) in Spinaw where there exists a condensation of connective tissue in the form of a curved rod on each side of the body close under the skin, in the position shown in Fig. 159, pg (p. 321). This forms the rudiment of the pectoral girdle. From it there grows outwards a short projection into the limb-rudiment which as it is clearly homologous with the axial cartilage of Oemtoolus we may call by the same name. The girdle rudiment increases in length both dorsally and ventrally, and ventrally the two rudiments come to be in apposition. On each side a tract of cartilage now develops in the prochondral rudiment: the two cartilaginous rudiments show a similar dorsal and ventral extension and presently they also come into apposition ventrally and form a continuous structure across the mid-ventral line.

In other Elasmobranchs (see Mollier, 1894) the conditions appear to be similar on the whole to those described in Spmaw. 352 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

The prochondral rudiment of the axial cartilage extends out into the limb-rudiment, forming a broad plate which tapers oil’ posteriorly (Fig. 168). The condition is in its essentials the same as that in 0e-ratodas except that here the axial rudiment is laid back along the side of the body. The prochondral ﬁn-rays arise, as in Ceratodus, in the form of outgrowths from the axial element. These are restricted to the outer (preaxial) side of the limb. They develop in Spi'na.:z3 (Braus) in series from before backwards except that anteriorly, in the region which will give rise to mesopterygium and propterygium, a few rays develop in the opposite sequence from behind forwards.

The chendriﬁeation of the limb skeleton appears to take place in 1l['u.stelus and ’1'o'rpedo continuously but in 5Ep'i'ru(.33 it sets in ﬁrst in the axial portion and then in the rays in the same succession as they ﬂrst appear. 'l‘he separate segments of the rays in Spirnaaz also Fm163___SMi0-nthrong}, develop in succession as separate centres of

pectoral lin of Torpedo chondriﬁcation.

<;:1::r5':;'I*af;‘::l161 To understand the morphological relations

.” - Q ' of these earl sta es it is advisable to refer

Moll1er,l«.94.) y - . _ _ _ back to the paddle type of limb as it exists

Tl‘ -h 1 Ir l'me1t . . . omif, _,“,’f:,‘.’,,;:,’,‘,1‘i,‘,“_..,,,,:,‘:,,',, ' 111 the ancient sharks oi the genus Pleura cant/ms. Here (Fig. 169, B) we ﬁnd a limb resembling generally that of C'emto(lus but diﬂ'ering from it in two conspicuous details. (1) The skeletal axis has become relatively larger and clumsier, its original elements having probably undergone extensive processes of fusion both with one another, as shown by the fact that the eartilages of the axis are in places less numerous than the lateral rays, and also with the basal portions of these lateral rays. (2) The rays on the pestaxial side of the limb are much reduced in number, only a few persisting towards the limb apex. The tendency of the postaxial rays to disappear in these archaic sharks (and the same tendency is seen in Lung-ﬁshes) justiﬁes us in believing that the external side of the pectoral limb-axis in the young Elasmobranch is morphologically p’I’6a.’13ial. This conclusion raises the interesting question Are there any vestiges of postaxial rays to be found in existing Elasniobranchs ‘? This question has to be answered in the affirmative. In Oentrophorus (Fig. 169, C) Braus ﬁnds a number of postaxial rays near the tip of the ﬁn in a late stage of development; in Spiaaa: at least one similar piece of cartilage occurs; and even in the adults of various Sharks Gegenbaur and Bunge found similar vestiges. As vestigial organs are notoriously variable more extended investigations into the occurrence of such vestigial postaxial rays are very desirable. They should be carried out on as many different species of Shark as possible and V SKELETON OF THE PAIRED FIN S 353

on as large as possible a number of individual specimens of each 8pe(31(3S.

The skeleton of the pelvic girdle arises in a manner similar in its main features to that of the pectoral girdle. It is however characteristic of Elasmobranehs (except Holocephali) that the portion of the girdle dorsal to the attachment of the limb undergoes atrophy in later stages of development. As in the pectoral ﬁn an axial cartilage appears with fin rays sprouting from its external side. Here also a separate cartilage develops anteriorly with a few rays attached to it but it is doubtful whether it is justifiable to homologize this in detail either with the propterygium or the meso pterygium of the pectoral ﬁn. The cartilaginous skeleton ol' the clasper arises in continuity

FIG. ‘I69.-——Pectoral fin skeletons of : A, (}eratmlu.s- (Semen) ; B, l’lmI.1'rI,cantlm.9 (Fritsch) ; C, (}’0nt'rophrn'u.s' mnliryo (Braus); D, Actmt/u'u.s (Gegenhaur); E, Olatloselache (Bashford Dean) ; F, I’ul_z/pterus larva. (Budgett) ; G, I’olypteru.s' (Wiedersheim).

The outer or preaxial side of the limb is to the left, except in A.

with the rest of the ﬁn skeleton and appears to consist of the tip of the limb axis with possibly a few modiﬁed rays. The claw-like structures are simply modiﬁed placoid scales.

TELEOS'1‘0MI.—-—As regards 1’olg/ptcms, commonly regarded as the most archaic of existing Teleostomes, our knowledge of the development of the limb skeleton is fragmentary. In the larva of stage 36 (Fig. 197) the skeleton of the pectoral limb is in the form of a thin lamina of cartilage with small irregularly scattered perforations. This is connected with a shoulder girdle rudiment consisting of a simple curved rod of cartilage. In the 30 mm. larva described by Budgett (1902) the girdle has become shortened into a compact block of cartilage and the cartilaginous plate lying within the limb itself has become thickened along its anterior and mesial edges. These thickened portions are separating off to form the rod-like “ proptery voL. II 2 A 354 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

gium ” and “ metapterygium ” (Fig. 169, F). The main portion of the plate is becoming split up towards its margin by a series of slits into a number of radiating pieces which represent the separate radii of the fully developed ﬁn (Fig. 169, G-). The close correspondence between the ﬁn skeleton at this stage of its development and the fin skeleton of a shark is obvious from Fig. 169.

In Actinopterygians the pectoral limb skeleton is in the prochondral stage a continuous mass, of which the anterior and mesial part separates oil’ to form the pectoral girdle, while the distal portion spreads outwards to form the rays.

The pelvic limb skeleton shows a fundamentally similar origin from a continuous proehondral rudiment, but here the skeletal rudiment appears first in the projecting limb and only secondarily spreads within the body wall into the region of the pelvic girdle. It appears to the present writer that no special weight need be attached to such cases where the skeleton develops earlier in the limb than in the body wall: they are probably to be regarded simply as special cases of the frequent tendency for highly specialized organs to be laid down precociously in development.

II. LIMBS or TIIE ’]‘Er1:AroDA.-—-In the Amphibia also the pectoral girdle and the skeleton of the limb itself are foreshadowed by a single condensation of mesenchyme which extends in a dorsal and ventral direction to form the girdle and out into the limb to form its skeleton. N 0 general rule can be given as to the relative time of development of the various parts. In Bombinator according to Goette the girdle rudiment appears ﬁrst and the limb skeleton sprouts from it: in Proteus according to Wiedersheim the limb skeleton appears first and the girdle later. In the girdle rudiment the dorsal or scapular portion becomes apparent ﬁrst. Chondriiication takes place separately in the girdle and the limb, the joint remaining unchondriﬁed.

The cartilaginous pectoral girdle of the Amphibian, as of other quadrupeds, takes on the form of a A upon each side of the bodythe three branches of the A being known as scapular, coracoid and precoracoid portions respectively and the glenoid articulation for the limb being situated at the meeting point of the three portions. As the two ventral branches of the A are in some cases continuous with one another at their tips through a strong membrane, it seems not improbable that they had originally the form of a continuous ﬂattened plate of cartilage, of which the central portion has now disappeared, leaving the thickened marginal parts as precoracoid (anterior) and coracoid (posterior) respectively. On this view the epicoracoid when present would represent the persisting thickened ventral margin of the primitive girdle.

In actual ontogeny the three branches spread gradually outwards from the original rudiment, while the epicoracoid when present is formed by the coracoid spreading forwards at its ventral end and fusing with the end of the precoracoid. The two lateral halves of v SKELETON OF THE‘ LIMBS 355

the girdle come to overlap one another in the mid-ventral line and in the case of the higher Anura complete fusion takes place.

Amongst the Reptilia the ﬁrst rudiment of the pectoral limb skeleton has been investigated by Mollicr (1895) and found to consist of a condensation of mesenchyme in the glenoid region corresponding partly to the glenoid portion of the girdle and partly to the basal portion of the limb skeleton——the two being thus again continuous at lirst. The girdle portion of the rudiment spreads ventrally to form the coracoid region, then dorsally to form the scapular. The chondriﬁcation of the various parts takes place in the order of their appearance.

In (Jhelonians the girdle takes on the typical A-shaped form with a more or less pronounced projection from the lower end of the coracoid forwards towards the lower end of the precoracoid which apparently represents the epicoracoid of Amphibians. In Sﬂmzodon and in Lizards on the other hand the ventral portion of the cartilaginous girdle consists of a ﬂattened plate which may become perforated by several foramina. Whether this flattened ventral portion corresponds to coracoid and precoracoid is doubtful. It seems on the whole more probable (Goette) that the precoracoid has disappeared in these forms owing to its functional replacement by the clavicle, a process seen in its incipient form in Anura. This view is supported by the occurrence of a distinct strand of condensed connective tissue in the position where the precoracoid should be though in this case it does not become chondriﬁed but becomes replaced by bone (clavicle) at a later stage.

In Birds the girdle forms a simple curved rod without any bifurcation into coracoid and precoracoid portions ventrally.

Each lateral half of the. pelvic girdle of quadrupeds is, like the pectoral girdle, typically of a A-shape, the three limbs being known here as ilium (dorsal, more correctly iliac bone or iliac cartilage), pubis (anterior) and ischium (posterior). The frequency with which the pubis and ischiuni are continuous at their ventral ends suggests that here also they represent the persisting thickened marginal parts of a once ﬂattened plate-like ventral portion of the girdle.

As in the case of the pectoral girdle the three processes are formed by simple spreading outwards from the original rudiment. In Amphibia chondriﬁcation takes place apparently from a single centre on each side (’1'rv}ton, Bunge, 1880) giving rise to a pair of longitudinal plates of cartilage which meet ventrally.

In Reptiles each half of the pelvic girdle passes through the typical A-shape. The ventral end of the pubis, like that of the ischium, meets its fellow across the mid-ventral plane forming a symphysis. In some cases, e.g. Sphenodon and certain Chelonia, the pubic sy‘1nphysis becomes connected up with that of the ischia by a longitudinal bar of cartilage. ln the_Crocodiles the pubic portion of the girdle becomes eventually segmented off at its dorsal end from the

rest of the girdle. 356 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

In Birds the pelvic girdle during the prochondral stage passes through the }\-shape, the right and left halves distinct from one another and each at first continuous with the skeleton of the limb.

Pubis, iliuin and isehiuni usually chondrify separately but in many ‘

cases (e.g. in the Coniinon Fowl usually) ilium and ischiuni may become chondriﬁed in continuity, and less frequently all three elements ehondrify in continuity. A highly characteristic feature of the avian pelvis is that the pubis swings in a tailward direction about its attached dorsal end until it assumes a position parallel with that of the pubis. ln the pelvis shown in Fig. 170, B, this rotation is just commencing.

The Gheiropterygium (Huxley), or skeleton of the limb in Amphibia and Aniniota, consists of three distinct portions corresponding respectively to the Upper Arm or Thigh, the Forcarin or Leg, and the Hand or Foot. As these portions are looked upon as homologous in the fore and hind limbs it is convenient to have a niorphological name

for the corresponding parts of the two

[2 B "L-=.s_ sets of limbs, and such names have

_ . _ been proposed by Emery and Haeckel

F”:' :70‘ i"‘Si‘1“;tT£l"“’}ffhP°l:‘“1g’g33l"‘-l --- Stylopodium, Zeugopodiuni or

“"',”’_"’_‘l" ‘(B “_ "_ Zygopodiuni, and Autopodium. In

;.;.:.;:'“  the autopocuum there may rurmer

' be recognized Basipodium (carpus or

tarsus), Metapodiuni (nietacarpus or inetatarsus) and Acropodium (phalanges). _ _ _ _ p

The limb skeleton is typically at first quite continuous. A rodshaped condensation‘ of inesenchyme appears ﬁrst in the limb stump -——the rudiment of the stylopodiuin (femur or humerus)———and as the limb grows this spreads outwards, bifurcating as it does so to form the rudiinents of the zygopodial skeleton: wi.tli further growth the two limbs of this unite distally to form the rudiment of the autopodial skeleton. Chondriﬁcation takes place from the base of the limb outwards, each separate element of the adult making its appearance as a separate chondriﬁcation centre.

The skeleton of the autopodium originates in a ﬂattened platelike extension of the prochondral zygopodial skeleton. In this the various carpal or tarsal elements make their appearance as separate centres of chondriﬁcation. It seems unnecessary in a general text-book like the present to go into the great variations in detail which are found amongst the various tetrapods in regard to the skeleton of carpus and tarsus. It need only be said that the striking variations found in different groups from the schematic arrangement, such as is illustrated by Fig. 171, seem to have been brought about by enlargement or reduction 0'1’ individual elements, or the fusion together of originally separate elements. V SKELETON 0}" THE LIMBS 357

From the plate-like rudiment of carpus or tarsus there spread out radiating extensions normally ﬁve in number to form the skeleton of the digits. In the Amniota these appear practically synchronously although in Amphibians there is a tendency for them to develop in regular sequence according to the number of the digit (Rabl, 1901). In the substance of these the phalanges make their appearance as discrete chondriﬁcations.

In the Birds the loss of individuality of the digits involved in the conversion of the tip of the pectoral limb into a rigid support for the ﬂight feathers has been accompanied by processes of reduction and fusion of the orginal elements. In the proehondral stage ﬁve digits are laid down but only 11, Ill and IV proceed with their development. Of these metacarpal ll

becomes reduced to a small stump project— IL Ill 15/f ing from III: metacarpals III and IV I o 0 0 V become fused with one another at both 0 0 0 0 0 ends: and the three distal carpals liecdlile O 0 0 0 0 fused with the metacarpals to form the O 0 O 0 0 C5 carpo-metacarpus characteristic of the Bird. CL 0.0000‘? _o Ce

In the hind limb of Birds there are "6’-,_.-0 Q .0 -.- u" also laid down proehondral rudiments of O. i‘ the ﬁve digits and again I and V become R Q U. reduced although not so completely as in ' the fore limb. V reaches the stage of a H

small metacarpal nodule of cartilage which FIG. 171. —— Cartilaginous 916 however soon disappears. Metacarpals II, Ilwnt-*4 whivh «M9101» in “W

I’ - ‘ ‘ , forelimb of I'.'m_?/szthe tigureis Ill and I\ fuse w1th- one another and cnmbincdfrom se\,em1stag,.s_

with a cartilage which represents the distal (After Mehnort, 1897.) pow of ttiagsals to 1l\}1‘p1ttl1elcpagacteristic 6,.’ ,,,.,,t,.,,,,.; P1,,’ ,,:_.,m, ,.,,.,,,,1;; arso—me a arsus. e a arsa isappears i, i_nt.ernu-dium'; H_. mnu-rush: . except in its distal portion. And finally T’ "“““““’ U’ “"“" "’ the two proximal carpals which are visible for a time fuse with the end of the tibia to form the tibio-tarsus. BONY SKELETON on THE LIMBS. PECTORAL GIRDLE.-—In the Sturgeons the original cartilaginous pectoral girdle persists, lying close under the skin of the posterior branchial recrion. Plates of bone corresponding exactly with those on the rest of the skin develop superﬁcial to the girdle and serve to reinforce it. Of these bony plates there are two principal ones on each side, one in the region of the glenoid surface the cleithrum (Gegenbaur) and one extending ventrally to meet its fe11ow—-—the clavicle. In existing Crossopterygians where the evolution of the bony skeleton has reached a higher level than in the Sturgeons the same two bony elements develop but here the original shoulder girdle-its function being to a great‘ extent talienl over byil the cleithgum ——f_bte1c1:omies tlgelativeelylr rec 11CB( in size. t ies on t e inner sur ace 0 e c ei rum an its cartilage gives place in part to two replacement bones--the scapula dorsal, and the coracoid ventral. It is to be noted also 358 EMBRYOLOGY or THE LOWER VERTEBRATES on.

that the cleithrum sinks more deeply into the tissues while the clavicle remains superﬁcial.

In the higher bony ﬁshes Ganoids and Teleosts—-the conditions are very similar to those ol']’oly;ute'mzs-—tl1e primitive shoulder girdle being small and usually becoming replaced in great part by bone (scapula and coracoid) and the main supporting function being exercised by the independently developed cleithrum.

In the Dipnoi more nearly primitive conditions are retained as the original cartilaginous girdle remains well developed throughout life and retains its continuity with its fellow ventrally. (lleithrum and clavicle however are also developed and they show a higher condition in that they are developed in intimate contact with the surface of the cartilaginous girdle, the clavicle ensheathing the anterior face of the coracoid portion.

In Amphibians the scapula becomes replaced incompletely or completely by hone which spreads dorsalwards from the region of the glenoid articulation. The coracoid may remain cartilaginous (most Urodeles) or become replaced by bone. The precoracoid also tends to be strengthened by the formation of bone. ln the common frog (Rana) and Toad (Bu;/b) the bone (“clavicle”) is in the form of a splint lying along the anterior side of the precoracoid and originating in the connective tissue some little distance from the cartilage. In other cases the bony tissue completely surrounds and to a great extent invades and replaces the cartilage. We may infer with considerable probability that the bone in question was originally in phylogeny a “niembrane” bone and that becoming more and more intimately related to the precoracoid cartilage it has in the latter form become more or less completely a “cartilage ” bone——a good example of the type of evidence which has led morphologists to minimize the importance of the distinction between these two types of bone.

In the Amniota scapula and coracoid are replaced nearly or quite completely by bone. A clavicle like that of Amphibians develops in relation to the precoracoid in Reptiles except Crocodiles. ln Birds What appears to be the same element (furcula) is widely separated from the eoracoid, probably for mechanical reasons connected with ﬂight, while a separate centre of ossiﬁcation appears at the apposed ventral ends of the two bones. In Reptiles a somewhat similar ele1nent——the episternum—n1akes its appearance and is continued tailwards along the mid-ventral surface of the sternum and it is possible that in Birds the ossiﬁcation lying between the ventral ends of the clavicles represents the anterior segmented off portion of this and the keel of the sternum the rest.

PELVIC GIR1)LE.——The cartilaginous pelvic girdle becomes replaced by bone less or more completely without receiving any reinforcement from investing bones. The iliac, pubic and ischial portions ossify each from its own centre except in Amphibia where the pubic region remains cartilaginous.

In bony Teleostomatous ﬁshes eaclf half of the pelvic girdle V THE SKELETON 359

hecomos replaced by a plate of bone the morphological nature of which has been much discussed. Detailed studies of its development in a variety of different teleosts and in the more primitive ganoids are much needed.

LITERATURE

Agar. Trans. Roy. Soc. Edin., xlv, 1906. Albrecht, A. Entwickelung des Achsenskele-ties dcr Telcostier. (Diss.) Strassburg, 1902.

Braus. Morph. Jahrb., .\xvii, 1899.

Braus. Haeckelfestschrift (J cnaer Denkschriften, xi), 1904. Braus. l[cl‘twigs Handbuch der Entwicklungslehrc, iii, 1906. Budgett. Trans. Zool. Soc. Lond., xvi, 1902.

Bunge. Entwickcluingsgcscliiclite des licckeilglirtc-ls der Amphihic-n, Rt-ptilien

nnd V ogel. (Dis:-3.) Dorpat, 1880.

Garlsson. Anat. Anzciger, xi, 1896.

Carlsson. Anat. Anzeigr-r, xii, 1896*‘.

Cords. Anat. Hefte (A1-h.), xxxviii, 1909.

Dohrn. Mitt. Z001. Stat. Ncapel, v, 1884.

Gadow. Phil. Trans. Roy. Soc., B, clxxxvi, 1895.

Gadow. Phil. Trans. Roy. Soc., B, clxxxvii, 1897.

Gaupp. Schwalbcs Morph. Arbeiten, iii, 1894.

Gaupp. Hertwigs IIandb11ch der Entwicklungslchre, iii, 1906. Gibson. Anat. Anzeiger, xxxv, 1910.

Goeppert. Gegcnbaurs Fcstschrift. Leipzig, 1896.

Goette. Arch. mikr. Anat., xv, 1878.

Goette. Arch. mikr. Anat., xvi, 1879.

Goodrich. Quart. Journ. Micr. Sci., xlvii, 1904.

Goodrich. Proc. Z001. Soc. Lond., 1908.

Goodrich. Proc. Zool. Soc. Lond., 1913.

Goodrich. Quart. Journ. Micr. Sci., lxi, 1915.

Gregory. Biol. Bull., vii, 1904.

Harrison. Arch. mikr. Anat., xlii, 1893.

Hertwig, O. J enaische Zeitschr., viii, 1874.

Hertwig, 0. Arch. mikr. Anat., xi, Suppl., 1874*.

Howes and Swinnerton. Trans. Z001. Soc. Lond., xvi, 1901. Huxley. Todd's Cyclopaedia of Anatomy and Physiology, v, 1859. Kerr, Graham. Proc. Roy. Phys. Soc. Edin., xvii, 1908.

Leche. Anat. Anzciger, viii, 1893.

Marsh. Odontornithes. Washington, 1880.

Mehnert. Morph. Jahrh., xiii, 1888.

Mehnert. Schwalhes Morph. Arheiten, vii, 1897.

Mollier. Anat. Hefte (Arb.), iii, 1894.

Mollier. Anat. Heftc (Arb.), v, 1895.

Nickerson. Bull. Mus. Comp. '/.001. Harvard, xxiv, 1893.

Rabl, C. Morph. J ahrb., xix, 1893.

Rabl, C. Zeitschr. vsiss. 7.001., lxx, 1901.

Rose. Anat. Anzeiger, vii, 1892.

Rose. Anat. Anzeigcr, viii, 1893.

Rose. Anat. Anzeiger, ix, 1894.

Schauinsland. Zoologica, xxxix, 1903.

Schauinsland. Hertwigs Handbuch dcr Entwickelungslehre, iii, 1906. Schéne. Morph. Jahrh., xxxi, 1902.

Semon. Forschungsreisen in Australien, i. Jena, 1893—1913. Sewertzoff. Kuplfers F estschrift. Jena, 1899.

Sollas, W. and I. Phil. Trans. Roy. Soc., B, cxcvi, 1903.

Sonics. Petrus Camper, iv, 4, 1907.

Suschkin. Nouv. Mém. Soc. des Naturalistes dc Moscou, xvi, 1899. Time, Marett. Quart. Journ. Micr. Sci., xlix, 1906.

Traquair. Proc. Roy. Phys. Soc. Edin., xii, 1893.

Versluys. Z001. Jahrb. (Anat.), xix, 1903.

Wijhe, van. Comptes rendus 6"” Congrbs intcrnat. Zool. 1904, Berne, 1905. Williamson. Phil Trans. Roy. Soc., ex], 1849.

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

- Currently only Draft Version of Text -

Reference

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

Cite this page: Hill, M.A. (2024, April 26) Embryology Text-Book of Embryology 2-5 (1919). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Text-Book_of_Embryology_2-5_(1919)

What Links Here?