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Title: The Ancestry of Modern Amphibia: A Review of the Evidence

Author: Theodore H. Eaton

Release date: September 8, 2011 [eBook #37350]

Language: English

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*** START OF THE PROJECT GUTENBERG EBOOK THE ANCESTRY OF MODERN AMPHIBIA: A REVIEW OF THE EVIDENCE ***

University of Kansas Publications
Museum of Natural History

Volume 12, No. 2, pp. 155-180, 10 figs.

-----------July 10, 1959-----------

The Ancestry of Modern Amphibia:
A Review of the Evidence

BY

THEODORE H. EATON, JR.

University of Kansas
Lawrence
1959

University of Kansas Publications, Museum of Natural History

Editors: E. Raymond Hall, Chairman, Henry S. Fitch, Robert W. Wilson

Volume 12, No. 2, pp. 155-180
Published July 10, 1959

University of Kansas
Lawrence, Kansas

PRINTED IN THE STATE PRINTING PLANT
TOPEKA, KANSAS
1959

27-8362

[Transcriber's Notes: Several typos have been regulated.
One typo of "ancester" for "ancestor" was corrected.
One instance of "salamanderlike" corrected to "salamander-like".
The captions on some images give relative size. Due to differences in monitor size/resolution, do not consider the images to be scalable.]

The Ancestry of Modern Amphibia:

A Review of the Evidence

BY

THEODORE H. EATON, JR.

INTRODUCTION

In trying to determine the ancestral relationships of modern orders of Amphibia it is not possible to select satisfactory structural ancestors among a wealth of fossils, since very few of the known fossils could even be considered possible, and scarcely any are satisfactory, for such a selection. The nearest approach thus far to a solution of the problem in this manner has been made with reference to the Anura. Watson's paper (1940), with certain modifications made necessary by Gregory (1950), provides the paleontological evidence so far available on the origin of frogs. It shows that several features of the skeleton of frogs, such as the enlargement of the interpterygoid spaces and orbits, reduction of the more posterior dermal bones of the skull, and downward spread of the neural arches lateral to the notochord, were already apparent in the Pennsylvanian Amphibamus (Fig. 1), with which Gregory synonymized Miobatrachus and Mazonerpeton. But between the Pennsylvanian and the Triassic (the age of the earliest known frog, Protobatrachus) there was a great lapse of time, and that which passed between any conceivable Paleozoic ancestor of Urodela and the earliest satisfactory representative of this order (in the Cretaceous) was much longer still. The Apoda, so far as known, have no fossil record.

Nevertheless it should be possible, first, to survey those characters of modern Amphibia that might afford some comparison with the early fossils, and second, to discover among the known Paleozoic kinds those which are sufficiently unspecialized to permit derivation of the modern patterns. Further circumstantial evidence may be obtained by examining some features of Recent Amphibia which could not readily be compared with anything in the fossils; such are the embryonic development of the soft structures, including cartilaginous stages of the skeleton, the development and various specializations of the ear mechanism, adaptive characters associated with aquatic and terrestrial life, and so on.

COMPARISON OF MODERN ORDERS WITH THE LABYRINTHODONTS AND LEPOSPONDYLS

Fig. 1. Fig. 1. Saurerpeton (× 1/2, after Romer, 1930, fig. 6); Amphibamus, the palatal view × 2-1/4, from Watson, 1940, fig. 4 (as Miobatrachus), the dorsal view × 2-1/2, from Gregory's revised figure of Amphibamus (1950, Fig. 1); Protobatrachus, × 1, from Watson, 1940, fig. 18, 19.

In both Anura and Urodela the skull is short, broad, relatively flat, with reduced pterygoids that diverge laterally from the parasphenoids leaving large interpterygoid vacuities, and with large orbits. (These statements do not apply to certain larval or perennibranchiate forms.) The skull in both orders has lost a number of primitive dermal bones in the posterior part; these are: basioccipital, supraoccipital, postparietal, intertemporal, supratemporal, and tabular. The exoccipitals form the two condyles but there are no foramina for the 11th and 12th nerves, since these are not separate in modern Amphibia. The opisthotic is missing in all except Proteidae (but see discussion of the ear). Although the skull is normally autostylic, a movable basipterygoid articulation is present among Hynobiid salamanders and in at least the metamorphic stages of primitive frogs, and therefore should be expected in their ancestors. The vertebrae are, of course, complete; see discussion in later section. The quadratojugal, lost in salamanders, is retained in frogs, and conversely the lacrimal, absent in frogs, occurs in a few primitive salamanders. The situation in Apoda is different, but postfrontal and jugal should be noted as bones retained in this order while lost in the others.

Thus, in spite of minor differences, the above list shows that there are numerous and detailed similarities between Anura and Urodela with respect to the features in which they differ from the Paleozoic orders. Pusey (1943) listed 26 characters which Ascaphus shares with salamanders but not with more advanced frogs; a few of these might be coincidental, but most of them are of some complexity and must be taken to indicate relationship. The main adaptive specializations of Anura, however, including loss of the adult tail, extreme reduction in number of vertebrae, formation of urostyle, elongation of the ilium and lengthening of the hind legs, must have appeared at a later time than the separation of that order from any possible common stem with Urodela, although they are only partially developed in the Triassic Protobatrachus.

Turning to the Paleozoic Amphibia, there are two groups in which some likelihood of a relationship with modern order exists. In the Pennsylvanian Trimerorhachoidea (Labyrinthodontia, order Temnospondyli) some members, such as Eugyrinus, Saurerpeton, and notably Amphibamus (Fig. 1) had short, broad heads, an expansion of palatal and orbital openings, posterior widening of the parasphenoid associated with divergence of the pterygoids, a movable basipterygoid articulation, and reduction in size (but not loss) of the more posterior dermal bones of the skull. In recognition of Watson's (1940) evidence that these animals make quite suitable structural ancestors of frogs, Romer (1945) placed Amphibamus in an order, Eoanura, but Gregory (1950) indicated that it might better be left with the temnospondyls. Association of the urodele stem with this group does not seem to have been proposed hitherto.

The other group of Paleozoic Amphibia that has been considered probably ancestral to any modern type is the subclass Lepospondyli, containing three orders, Aistopoda, Nectridia and Microsauria. In these the vertebrae are complete (holospondylous), the centra presumably formed by cylindrical ossification around the notochord, and there is no evidence as to the contributions from embryonic cartilage units. It is important to note at this point that precisely the same statement can be made regarding the vertebrae of adults of all three Recent orders, yet for all of them, as shown in a later section, we have ample evidence of the part played by cartilage elements in vertebral development. Therefore (a) we cannot say that there were no such elements in embryonic stages of lepospondyls, and (b) it would take more than the evidence from adult vertebrae to relate a particular modern order (for example, Urodela) to the Lepospondyli. Vague similarities to Urodela have been noted by many authors in the Nectridia, Aistopoda and Microsauria, but these are not detailed and refer mainly to the vertebrae. The skulls do not show, either dorsally or in the palate, any striking resemblance to those of generalized salamanders, and certainly most known lepospondyls are too specialized to serve as the source of Urodela. It is true that the elongate bodies, small limbs, and apparent aquatic habitus of some lepospondyls accord well with our usual picture of a salamander, but such a form and way of life have appeared in many early Amphibia, including the labyrinthodonts. The family Lysorophidae (Fig. 2), usually placed among microsaurs, is sufficiently close in skull structure to the Apoda to be a possible ancestor of these, but it probably has nothing to do with Urodela, by reason of the numerous morphological specializations that were associated with its snakelike habitus.

Fig. 2. Fig. 2. Lysorophus tricarinatus, lateral and posterior views × 2-1/2, modified after Sollas, 1920, Figs. 8 and 12, respectively; palatal view after Broom, 1918, × 1-1/2. For explanation of abbreviations see Fig. 3.

McDowell's (1958) suggestion that it would be profitable to look among the Seymouriamorpha for the ancestors of frogs seems to be based upon a few details of apparent resemblance rather than a comprehensive view of the major characters of the animals. In most points which he mentions (limb girdles, form of ear, pterygoid articulation) the present writer does not see a closer similarity of frogs to Seymouriamorpha than to Temnospondyli.

Still other opinions have been expressed. Herre (1935), for instance, concludes "on anatomical, biological and paleontological grounds" that the orders of Urodela, Anura, Apoda and Stegocephali were all independently evolved from fish, but beyond citing the opinions of a number of other authors he does not present tangible evidence for this extreme polyphyletic interpretation.

More notable are the views of several Scandinavian workers (Säve-Söderbergh, 1934; Jarvik, 1942; Holmgren, 1933, 1939, 1949a, b), of whom Jarvik, in a thorough analysis of the ethmoid region, would derive the Urodela from Porolepid Crossopterygii, and all other tetrapods from the Rhipidistia; Säve-Söderbergh and Holmgren, the latter using the structure of carpus and tarsus, see a relationship of Urodela to Dipnoi, but accept the derivation of labyrinthodonts and other tetrapods from Rhipidistia. All of this work is most detailed and laborious, and has produced a great quantity of data useful to morphologists, but the diphyletic theory is not widely adopted; the evidence adduced for it seems to consist largely of minutiae which, taken by themselves, are inconclusive, or lend themselves to other interpretation. For instance Holmgren's numerous figures of embryonic limbs of salamanders show patterns of cartilage elements that he would trace to the Dipnoan type of fin, yet it is difficult to see that the weight of evidence requires this, when the pattern does not differ in any fundamental manner from those seen in other embryonic tetrapods, and the differences that do appear may well be taken to have ontogenetic rather than phylogenetic meaning. Further, the Dipnoan specialization of dental plates and autostylic jaw suspension, already accomplished early in the Devonian, would seem to exclude Dipnoi from possible ancestry of the Urodela, an order unknown prior to the Mesozoic, in which the teeth are essentially similar to those of late Paleozoic Amphibia, and the jaw suspension is not yet in all members autostylic.

THE EAR

Fig. 3. Fig. 3. Occipital region of skulls of Megalocephalus brevicornis (× 3/10, after Watson, 1926, as Orthosaurus), Dvinosaurus (× 1/4, modified after Bystrow, 1938; the lower figure after Sushkin, 1936), and Necturus maculosus (× 3, original, from K. U., No. 3471).

Abbreviations Used in Figures

b'd.c.—basidorsal cartilage (neural

b'oc.—basioccipital

ce.₁₋₄—centrale₁₋₄

ch.—ceratohyal

clav.—clavicle

clei.—cleithrum

cor.—coracoid

d.c.₁₋₄—distal carpal₁₋₄

diap.—diapophysis

exoc.—exoccipital

ep.—episternum

hyost.—hyostapes

i.—intermedium

Mk.—Meckel's cartilage

n.—notochord

om.—omosternum

op.—operculum

opis.—opisthotic

par.—parietal

par. proc.—paroccipital process

peri. cent.—perichordal centrum

p'p.—postparietal

prep.—prepollex

pro.—prootic

p'sp.—parasphenoid

pt.—pterygoid

p.t.f.—post-temporal fossa

postzyg.—postzygapophysis

qj.—quadratojugal

qu.—quadrate

ra.—radiale

r.hy.—hyomandibular ramus of VII

rib-b.—rib-bearer

r.md.—mandibular ramus of VII

sc.—scapula

sc'cor.—scapulocoracoid

s'd.—supradorsal cartilage

s'd.(postzyg.)—supradorsal (postzygapophysis)

soc.—supraoccipital

sp.c.—spinal cord

sq.—squamosal

s'sc.—suprascapula

s't.—supratemporal

sta.—stapes

ster.—sternum

tab.—tabular

uln.—ulnare

v.a.—vertebral artery

xiph.—xiphisternum

I, IV—digits I and IV

V, VII, X, XII—foramina for cranial nerves of these numbers (in Fig. 4, VII is the facial nerve)

In temnospondylous Amphibia the tympanum generally occupied an otic notch, at a high level on the skull, bordered dorsomedially by the tabular and ventrolaterally by the squamosal. In this position the tympanum could receive airborne sounds whether the animal were entirely on land or lying nearly submerged with only the upper part of its head exposed. Among those Anura in which the ear is not reduced the same is true, except that the tabular is lost. In Temnospondyli (Fig. 3) the posterior wall of the otic capsule was usually formed by the opisthotic, which extended up and outward as a buttress from the exoccipital to the tabular, and sometimes showed a paroccipital process for the insertion, presumably, of a slip or tendon of the anterior axial musculature. The stapes, in addition to its foot in the fenestra ovalis and its tympanic or extrastapedial process to the tympanum, bore a dorsal process (or ligament) to the tabular, an "internal" process (or ligament) to the quadrate or an adjacent part of the squamosal, and a ligament to the ceratohyal. Some of these attachments might be reduced or absent in special cases, but they seem to have been the ones originally present both phylogenetically and embryonically in Amphibia.

Among typical frogs (Fig. 4) the base, or otostapes, is present and bony, the extrastapedial process (extracolumella, or hyostapes) is usually cartilaginous, the dorsal process (processus paroticus) is of cartilage or ligament, but the other two attachments are absent in the adult. The exoccipital extends laterally, occupying the posterior face of the otic capsule. Between it and the otostapes is a small disc, usually ossified, the operculum, which normally fits loosely in a portion of the fenestral membrane, and is developed from the otic capsule. The opercularis muscle extends from this disc to the suprascapula, in many but by no means all families of Anura.

Fig. 4. Fig. 4. Diagram of middle ear structures in Rana (upper figure, after Stadtmüller, 1936, and lower left after DeBeer, 1937), and Ambystoma (lower right, after DeBeer, 1937); all × 4. For explanation of abbreviations see Fig. 3.

Among Urodela (Fig. 4) the middle ear cavity and tympanum are lacking, and the stapes (columella) consists of no more than its footplate and the stylus, which is attached to the border of the squamosal, thus corresponding to the "internal" process. In families in which individuals metamorphose and become terrestrial (Hynobiidae, Ambystomidae, Salamandridae, Plethodontidae), an operculum and opercularis muscle appear in the adult, just as in frogs, except that in Plethodontidae, the most progressive family, the operculum fuses with the footplate of the stapes. Among neotenous or perennibranchiate urodeles there is no separate operculum or opercularis. The evidence given by Reed (1915) for fusion of the operculum with the columella in Necturus appears inconclusive, in spite of the great care with which his observations were made. On the other hand, Necturus and Proteus alone among living salamanders have a distinct opisthotic on the posterior wall of the otic capsule (Fig. 3), as do the Cretaceous Hylaeobatrachus and the Eocene Palaeoproteus. Probably these Proteidae should be regarded as primitive in this respect, although many other features may be attributed to neoteny.

There is a contrast between Anura and most Urodela in the relative positions of the stapes and facial nerve, as shown in DeBeer's (1937) diagrams. In the latter (Ambystoma) the nerve is beneath, and in the former (Rana) above, the stapes. Judging by figures of Neoceratodus, Hypogeophis, and several types of reptiles and mammals, the Urodela are exceptional. Necturus, however, has the nerve passing above its stapes, and this may be primitive in the same sense as the persistent opisthotic. There can be, of course, no question of the nerve having worked its way through or over the obstructing stapes in order to come below it in salamanders; rather, the peripheral growth of neuron fibers in the embryo must simply pursue a slightly different course among the partially differentiated mesenchyme in the two contrasting patterns.

Although DeBeer (1937) shows in his figure of Hypogeophis (one of the Apoda) an operculum, this is apparently a mistake. The stapes has a large footplate, and its stylus articulates with the quadrate, but no true operculum or opercularis has been described in the Apoda. The facial nerve passes above the stapes. It does not seem necessary to regard the conditions in this order as related directly to those of either salamanders or frogs, but a reduction of the stapes comparable to that in salamanders has occurred.

The presence in both frogs and terrestrial salamanders of a special mechanism involving the opercularis muscle and an operculum cut out in identical fashion from the wall of the otic capsule behind the stapes seems to require some other explanation than that of a chance convergence or parallelism. Although the stapes and otic region are readily visible in a number of labyrinthodonts and lepospondyls, no indication of an operculum seems to be reported among them. But in the Triassic Protobatrachus (Fig. 1), which is unmistakably a frog in its skull, pelvis and some other features, Piveteau (1937) has shown, immediately behind the foot of the stapes, a small bony tubercle, which he and Watson (1940) designated opisthotic. Very clearly it served for insertion of a muscle, and it is equally clear that the bone is a reduced opisthotic, carrying the paroccipital process already mentioned as characteristic of it in some temnospondyls. Since the remainder of the posterior wall of the otic capsule consists of cartilage, meeting the exoccipital, it may be that the opisthotic becomes the operculum in frogs. Protobatrachus was too far specialized in the Anuran direction, although it still had a tail, and the forelegs and hind legs were nearly the same size, to be considered a possible ancestor of the Urodeles. But at one stage in the general reduction of the skull in the ancestry of both groups, a condition similar to that in Protobatrachus may have characterized the otic region, long before the Triassic.

In the argument thus far we have considered terrestrial, adult amphibians, since it is only in these that either the normal middle ear and tympanum, or the opercular apparatus, is present. But among the urodeles several neotenic types occur (this term applies also to the perennibranchs). For most of these there is nothing about the otic region that would be inconsistent with derivation, by neoteny, from known families in which adults are terrestrial; for example, Cryptobranchus could have had a Hynobiid-like ancestor. But this, as mentioned above, does not hold for the Proteidae, which possess an opisthotic of relatively large size, distinctly separate from the exoccipital and prootic. Either this bone is a neomorph, which seems improbable, or there has not been in the ancestry of this particular family an episode of reduction comparable to that seen in the terrestrial families, where there is an operculum instead of a normal opisthotic. Therefore the Proteidae probably are not derived from the general stem of other salamanders, but diverged sufficiently long ago that the bones of the otic region were reduced on a different pattern. They need not be removed from the order, but, in this respect, recognized as more primitive than any other existing Urodela or Anura. A recent paper by Hecht (1957) discusses many features of Necturus and Proteus, and shows that they are remote from each other; his evidence does not seem to prove, however, that they were of independent origin or that they need be placed in separate families.

VERTEBRAE AND RIBS

Development of the vertebrae and ribs of Recent Amphibia has been studied by Gamble (1922), Naef (1929), Mookerjee (1930 a, b), Gray (1930) and Emelianov (1936), among others. MacBride (1932) and Remane (1938) provide good summaries. In this section reference will be made to the embryonic vertebral cartilages by the names used for them in these studies, although the concept of "arcualia" is currently considered of little value in comparative anatomy.

Fig. 5. Fig. 5. Development of Anuran vertebrae. Upper left, late tadpole of Xenopus laevis; lower left, same just after metamorphosis; upper right, diagram of general components of primitive Anuran vertebra. (After MacBride, 1932, Figs. 35, 38, 47D, respectively.) Lower right, section through anterior portion of urostyle, immediately posterior to sacral vertebra, in transforming Ascaphus truei (original, from specimen collected on Olympic Peninsula, Washington). All × 20 approx. For explanation of abbreviations see Fig. 3.

The centrum in Anura (Fig. 5) is formed in the perichordal sheath (Rana, Bufo) or only in the dorsal portion thereof (Bombinator, Xenopus). The neural arch develops from the basidorsal cartilages that rest upon, and at first are entirely distinct from, the perichordal sheath. Ribs, present as separate cartilages associated with the 2nd, 3rd and 4th vertebrae in the larvae of Xenopus and Bombinator, fuse with lateral processes (diapophyses) of the neural arches at metamorphosis, but in Leiopelma and Ascaphus the ribs remain freely articulated in the adult. Basiventral arcualia have been supposed to be represented by the hypochord, a median rod of cartilage beneath the shrinking notochord in the postsacral region, which at metamorphosis ossifies to produce the bulk of the urostyle. Fig. 5, lower right, a transverse section taken immediately posterior to the sacral ribs in a transforming specimen of Ascaphus, shows that the "hypochord" is a mass of cartilage formed in the perichordal sheath itself, and very obviously is derived from the ventral part of postsacral perichordal centra; there are, then, no basiventral arcualia, and the discrete hypochord shown in MacBride's diagram (Fig. 5, upper right) of a frog vertebra does not actually occur below the centrum, but only below the notochord in the postsacral region.

Fig. 6. Fig. 6. Development of Urodele vertebrae. Upper figures, Triton: at left, larva at 20 mm., at right, diagram of components of vertebra (from MacBride, 1932, figs. 17, 47C). Middle figures, Molge vulgaris larva: left, at 18 mm.; middle, at 20-22 mm.; right, at 25 mm. (from Emelianov, 1936, figs. 33, 36, 38 respectively). Lower figures, Necturus maculosus larva: left, at 21 mm.; right, at 20 mm. (from MacBride, 1932, figs. 41.5, 41.3 respectively, after Gamble, 1922). All × 20 approx. For explanation of abbreviations see Fig. 3.

In Urodela (Fig. 6) the pattern of vertebral and rib development is more complex, and there has been much controversy over its interpretation. Neural arches and perichordal centra form in the same manner as in frogs, but with the addition in certain cases (Triton) of a median supradorsal cartilage, which gives rise to the zygapophyses of each neural arch. Difficulty comes, however, in understanding the relationship of the ribs to the vertebrae. Each rib, usually two-headed, articulates with a "transverse process" that in its early development seems to be separate from both the vertebra and the rib, and is therefore known, noncommittally, as "rib-bearer." This lies laterally from the centrum, neural arch, and vertebral artery; upon fusing with the vertebra it therefore encloses the artery in a foramen separate from the one between the capitulum and tuberculum of the rib (the usual location of the vertebral artery). At least four different interpretations of these structures have been suggested:

(1) Naef (1929) considered the rib-bearer a derivative of the basiventral, which, by spreading laterally and dorsally to meet the neural arch, enclosed the vertebral artery. He then supposed that by reduction of the rib-bearer in other tetrapods (frogs and amniotes) the vertebrarterial foramen and costal foramen were brought together in a single foramen transversarium. The implication is that the Urodele condition is primitive, but it cannot now be supposed that Urodela are ancestral to any other group, and the rib-bearer is most probably a specialization limited to salamanders. This does not, of course, invalidate the first part of his interpretation.

(2) Remane (1938), noting that rib insertions of early Amphibia are essentially as in Amniota, argued that the rib-bearer is not from the basiventral but is a neomorph which originates directly from the neural arch and grows ventrally. This he inferred mainly from Gamble's (1922) observation on Necturus, but his assumption that Necturus is more primitive than other salamanders (such as the Salamandridae), where the pattern differs from this, is not necessarily correct. Rather, the perennibranchs are distinguished mainly by their neotenous features, and their development is likely to show simplifications which are not necessarily primitive. The suggestion of a "neomorph" ought not to be made except as a last resort, for it is simply an acknowledgment that the author does not recognize homology with any structure already known; sometimes further information will make such recognition possible.

(3) Gray (1930), using Molge taeniatus, concluded that the normal capitulum of the rib was lost, but that the tuberculum bifurcated to make the two heads seen in Urodela, thus accounting for the failure of the costal foramen to coincide with that of the vertebral artery. This answer, too, seems to entail an unprovable assumption which should not be made without explicit evidence.

(4) Finally, Emelianov (1936) regarded the rib-bearer as a rudimentary ventral rib, on account of its relationship to the vertebral artery, and considered the actual rib to be a neomorph in the dorsal position characteristic of tetrapod ribs in general. This argument would fit the ontogenetic picture satisfactorily, provided that (a) there were some evidence of ventral, rather than dorsal, ribs in early Amphibia, and (b) we accept the invention of another neomorph in modern Amphibia as an unavoidable necessity. Emelianov's conclusion (p. 258) should be quoted here (translation): "The ribs of Urodela are shown to be upper ribs, yet we find besides these in Urodela rudimentary lower ribs fused with the vertebral column. The ribs of Apoda are lower ribs. In Anura ribs fail to develop fully, but as rare exceptions rudiments of upper ribs appear."

Of these various interpretations, that of Naef seems to involve the minimum of novelty, namely, that the rib-bearer is the basiventral, expanded and external to the vertebral artery. It is not necessary to take this modification as the ancestral condition in tetrapods, of course. The basiventral (=intercentrum) would merely have expanded sufficiently to provide a diapophysis for the tuberculum as well as the (primitive) facet for the capitulum. No neomorph appears under this hypothesis, which has the distinct advantage of simplicity.

Figures of early stages in vertebral development by the authors mentioned show that the basidorsals chondrify first, as neural arches, while a separate mass of mesenchyme lies externally and ventrally from these. This mesenchyme may chondrify either in one piece (on each side) or in two; in Molge the part adjacent to the centrum is ossified in the 20-mm. larva, and subsequently unites with the more dorsal and lateral cartilaginous part, while the rib, appearing farther out, grows inward to meet this composite "rib-bearer." In Necturus the mesenchyme below the neural arch differentiates into a cartilage below the vertebral artery (position proper to a basiventral), a bridge between this and the neural arch, and a rib, the latter two chondrifying later than the "basiventral" proper. In the "axolotl" (presumably Ambystoma tigrinum) the rib-bearer grows downward from its first center of chondrification at the side of the neural arch (Emelianov, 1936).

Thus it appears that the simplest hypothesis to account for the rib-bearer is that (a) it is the basiventral, (b) it is recognizable just before chondrification as a mass of mesenchyme in contact with both the notochordal sheath and the basidorsal cartilage, (c) it may chondrify or ossify first in its ventral portion or in its dorsal portion, the two then joining before it fuses with the rest of the vertebra, (d) the enclosure of the vertebral artery is a consequence of the extension of the basiventral beyond the position occupied by it in primitive Amphibia, and (e) there is no indication that this took place in other orders than the Urodela.

It seems that the vertebrae in Urodela have at least the following components: perichordal centra, separate basidorsal cartilages, and basiventrals, which are somewhat specialized in their manner of development. The vertebrae of Anura develop in the fashion just described except that basiventrals are lacking. It would seem no more difficult to accept the derivation of salamander vertebrae from the temnospondylous type than it is in the case of frogs, if other evidence points to such an ancestry.

Fig. 7. Fig. 7. Vertebrae of Eusthenopteron (×1) and Ichthyostega (×2/3, after Jarvik, 1952), Trimerorhachis (×1-1/2, after Case), and Amphibamus (×10, after Watson, 1940) in lateral and end views; the two lower right-hand figures are from Watson (1940, as Miobatrachus); the lower left is from a cast of the "Miobatrachus" specimen in Chicago Natural History Museum, No. 2000, in the presacral region (original, ×10).

Fig. 7, lower right, is Watson's (1940) illustration of the anterior trunk vertebrae of Amphibamus (Miobatrachus), in which the intercentrum is shown as a single median piece. Fig. 7, lower left, shows two of the more posterior trunk vertebrae seen as impressions in a cast of the type of "Miobatrachus romeri;" evidently the inter-centra were paired at about the level of the 16th vertebra, and relatively large. Gregory's (1950) figure of the type specimen of "Mazonerpeton" (also equivalent to Amphibamus) shows the anterior trunk vertebrae in relation to the ribs essentially as they appear to me in the cast of Miobatrachus, and rather differently from Watson's figure of the latter. Gregory is probably right in considering the specimens to represent various degrees of immaturity. So far as present information goes, then, the vertebrae of salamanders and frogs show no clear evidence of derivation from those of any particular group among the early Amphibia, but their features are not inconsistent with a simplification of the pattern of Temnospondyli.

Fig. 8. Fig. 8. Pectoral girdles of Protobatrachus (after Piveteau, 1937), Notobatrachus (after Stipanicic and Reig, 1956), Ascaphus (after Ritland, 1955 a) and Rana (original); all ×2. For explanation of abbreviations see Fig. 3.

PECTORAL GIRDLE

Hecht and Ruibal (Copeia, 1928:242) make a strong point of the nature of the pectoral girdle in Notobatrachus, as described recently by Stipanicic and Reig (1955, 1956) from the Jurassic of Patagonia, and quite rightly recommend that the significance of the arciferal and firmisternal types of girdle be restudied. That of Notobatrachus is said to be firmisternal; in view of the arciferal condition in the supposedly primitive Leiopelma, Ascaphus, Bombinator, etc., this comes as a surprise. Is the firmisternal girdle, as seen in Rana, Bufo, and others, actually the ancestral type, and has the arciferal been derived from something like this?

In the figures given by Stipanicic and Reig the ossified parts of the girdle are figured in detail (Fig. 8) and Reig's discussion of it is thorough. The decision to call it firmisternal was taken with some hesitancy, for no median elements are indicated, and the position and shape of those seen is closely similar to the ossified parts in Ascaphus and Leiopelma; there is no bony sternum or omosternum. It is safe to suppose that some cartilage lay in the midline between the clavicles and coracoids, but there is no evidence as to its extent, rigidity, or degree of overlapping if any. Apparently, then, there is not sufficient reason to infer that this Jurassic frog had a pectoral girdle comparable with the modern firmisternal type.

Piveteau (1955:261) remarks that the only living Anuran that can be compared usefully with Protobatrachus (Triassic) with regard to its pectoral girdle is Ascaphus. Again, the extent of cartilage in Protobatrachus (Fig. 8) can only be inferred, and there are no median elements. The agreement with Ascaphus includes the presence, in both, of a separate coracoid ossification situated posterior to the ossified "scapulocoracoid" (actually scapula). This ossification is evidently that shown in Notobatrachus as "coracoid." Direct comparison of the three genera with one another suggests that if we use the term arciferal for any, we should use it for all.

In the remote predecessor of Anura, Amphibamus of the Pennsylvanian, the pectoral girdle was less substantial than in many of its contemporaries, but it contained the primitive median interclavicle in addition to the clavicle, cleithrum, and scapulocoracoid. (The figure of Watson, 1940, and that by Gregory, 1950, are of individuals of different ages, the latter being older.) It is clear that the paired elements of such a girdle were held rigid by their attachment to the interclavicle, via the clavicles. Subsequent elimination of the interclavicle in the Anuran line of descent, and decrease of ossification, left a girdle like that of Protobatrachus, Notobatrachus, Ascaphus and Leiopelma. But in several advanced families a more rigid median "sternum," of one or two bony pieces plus cartilage, is developed secondarily, possibly (as Cope, 1889: 247, suggested) in correlation with axillary amplexus.

Among Urodela no dermal bones occur in the pectoral girdle. There is usually a scapulocoracoid ossified as a single piece, from which a thin cartilaginous suprascapula extends dorsally and a broad cartilaginous coracoid plate extends medially, overlapping the one from the opposite side; a precoracoid lobe of this reaches forward on either side, and a median, posterior "sternum" of cartilage may make contact with the edges of the two coracoids. In Siren and Amphiuma two centers of ossification are found for each scapulocoracoid, and in Triton and Salamandra three. Probably the more dorsal and lateral of these represents the primitive scapula and the other one (or two) the primitive coracoid.

Comparing the girdle of a salamander with that of a frog, the closest similarity can be seen between Ascaphus and a salamander in which the scapula and coracoid ossify separately. Both have the median "sternum" in contact with the coracoid plates. The major difference, of course, is the lack of clavicle and cleithrum in the salamander.

CARPUS AND TARSUS

In Ascaphus (Ritland, 1955a; cleared and stained specimens of nearly grown males) distal carpals 1, 2, 3 and 4 are present and separate, increasing in size in the order given (Fig. 9). A prepollex rests against centrale 1; centralia 2 and 3 are fused; the radiale fuses with centrale 4, and the intermedium fuses with the ulnare; radius and ulna are fused with each other as in other frogs. The digits (and metacarpals) are considered by Ritland to be 1-4, in addition to the prepollex, rather than 2-5.

Fig. 9. Fig. 9. Skeleton of fore foot of Notobatrachus (after Stipanicic and Reig, 1956, terminology revised) and Ascaphus (after Ritland, 1955 a); all ×5. For explanation of abbreviations see Fig. 3.

In the Jurassic Notobatrachus Stipanicic and Reig (1956) have shown the carpus with surprising clarity (Fig. 9). If their nomenclature of the parts be revised, we obtain a fairly close resemblance to Ascaphus, except that centralia 2 and 3 are not fused, distal carpals 1 and 2 do not show (which would easily be understood if they were of the size of those in Ascaphus, or not ossified), and the intermedium remains separate from the ulnare.

In Salamandra (Francis, 1934; Nauck, 1938) distal carpals 1 and 2 are fused in both larva and adult, and 3 and 4 are separate; the radiale, intermedium and ulnare are separate in the larva but the latter two fuse in the adult; centrale 1 (labelled prepollical cartilage by Francis) and centrale 2 are separate. Francis considers the digits (and metacarpals) to be 1-4. Apparently the arrangement here indicated for the larva is characteristic of other larval salamanders, except where further reduced, and reduction below the number given for the adult is common in other terrestrial forms. The radius and ulna are, of course, separate.

The ossification of carpals is more likely to be complete in adult frogs than in salamanders, but some ossification of all parts named is found in several of the latter. A common ancestor of frogs and salamanders could be expected to have the following elements present and ossified in the adult: distal carpals 1-4 separate; 3 centralia; radiale, intermedium and ulnare separate. Comparison with fossils older than Notobatrachus is fruitless on these points, unless we go back to forms too distant to have any special value, such as Eryops. This is because of inadequate preservation and because the elements are not fully ossified in many immature specimens.

For the purpose of this review there is no special value in a comparison of the tarsi of frogs and salamanders, since the leaping adaptation of the former leaves very little common pattern between them. Even in Protobatrachus, where the legs were not yet conspicuously lengthened, the tibiale and fibulare ("astragalus" and "calcaneum" respectively) were already considerably elongated. The carpus and tarsus of Amphibamus are as yet undecipherable.

THE LARVA

Considering the postembryonic developmental stages of modern Amphibia, there can be no doubt that a gill-bearing, four-legged larva of a salamander, in which lateral line pores and a gular fold are present, represents much more closely the type of larva found in labyrinthodonts than does the limbless, plant-nibbling tadpole of the Anura. Salamander-like larvae of labyrinthodonts are well known, especially those formerly supposed to comprise the order Branchiosauria. Many, perhaps the majority of, labyrinthodonts show some features associated with aquatic life even when full-grown, as do the lepospondyls. These features may include impressions of sensory canals on the dermal bones of the skull, persistence of visceral arches, reduction in size of appendages, and failure of tarsal and carpal elements to ossify. In fact, it appears that very few of the Paleozoic Amphibia were successful in establishing themselves as terrestrial animals even as adults.

Nevertheless, in the ancestry of Anura, and that of at least the Hynobiid, Ambystomid, Salamandrid and Plethodontid salamanders, there must certainly have been a terrestrial adult, transforming from an aquatic larva. The leaping mechanism of Anura, shown in so many features of their anatomy, is perhaps to be explained as a device for sudden escape from land into the water, but it was not yet perfected in the Triassic Protobatrachus or the Jurassic Notobatrachus.

The middle ear, its sound-transmitting mechanism, and the tympanum, well developed in most Anura, are readily derived from those of early labyrinthodonts, and are presumably effective for hearing airborne sounds whether on land or while floating in the water. Reduction of these organs in Urodela may be correlated with their customary restriction to subsurface habitats and inability to maintain a floating position while in water.

Some light may be shed on the significance of the tadpole of Anura by considering the early stages of the ribbed frogs, Liopelmidae. Leiopelma and Ascaphus are so closely similar in the adult that there is no doubt that they belong in one family, primitive in some respects (including articulated ribs; pyriformis and caudalipuboischiotibialis muscles) but not in others (absence of tympanum and middle ear). In both genera the eggs are large, 5 mm. in Leiopelma, 4.5 mm. in Ascaphus, and unpigmented; but at this point the resemblance ends.

Fig. 10. Fig. 10. Leiopelma hochstetteri larva, lateral and ventral (after Stephenson, 1955), ×4.

Stephenson (1955) showed that embryos of L. hochstetteri develop equally well on land (in damp places) or in the water, and that embryos prematurely released from egg capsules develop successfully in the water. The larvae possess both pairs of legs (Fig. 10) and a broad gular fold similar to that of larval salamanders. In L. hochstetteri the fold grows back over the forelegs temporarily, but remains free from the body and presently the legs reappear, whereas in L. archeyi the forelegs are not covered at any time. No branchial chamber or spiracle is formed. Of course direct development, without a tadpole, occurs in several other groups of Anura, but in each case terrestrial adaptations are obvious. This is not true of Leiopelma, which Stephenson regards as more nearly comparable with Urodela in its development than with other Anura, and he sees in it a "primary and amphibious" mode instead of a terrestrial specialization.

The Ascaphus tadpole bears no outward resemblance to the larva of Leiopelma, but is a normal tadpole in form, although sluggish in activity. Its greatly expanded labial folds bear numerous rows of horny epidermal "teeth," which, with the lips, serve to anchor the tadpole to stones in the swift water of mountain brooks. Noble (1927) noticed that particles of food were taken in through the external nares, and that a current of water passed through these openings and out by way of the median spiracle. It appears that any action by the teeth and jaws in scraping algae from the rocks (which were bare in the stream where I have collected Ascaphus) would be quite incidental, and that the lips and teeth must be primarily a clinging mechanism. Certain other mountain brook tadpoles (for example, Borborocoetes) show similar devices, but these are developed independently, as specializations from the usual sort of tadpole.

May it not be that closure of the gill-chamber by the opercular (=gular) fold, retardation of limb development, expansion of the lips, growth of parallel rows of horny teeth, and other correlated features that make a tadpole, were brought about as an adaptation of the primitive Anuran larva to a swift-stream habitat, and that this "basic patent" then later served to admit the tadpoles of descendant types to an alga-scraping habit in quiet water as well? The tadpole, as a unique larval type among vertebrates, bears the hallmarks of an abrupt adaptive shift, such as might have occurred within the limits of a single family, and it seems difficult to imagine the enclosed branchial chamber, the tooth-rows, and lips of a familiar tadpole as having evolved without some kind of suctorial function along the way.

SUMMARY

The Anura probably originated among temnospondylous labyrinthodonts, through a line represented approximately by Eugyrinus, Amphibamus, and the Triassic frog Protobatrachus, as shown by Watson, Piveteau and others. The known Paleozoic lepospondyls do not show clear indications of a relationship with Urodela, but Lysorophus may well be on the ancestral stem of the Apoda.

Between Urodela and Anura there are numerous resemblances which seem to indicate direct relationship through a common stock: (1) a similar reduction of dermal bones of the skull and expansion of palatal vacuities; (2) movable basipterygoid articulation in primitive members of both orders; (3) an operculum formed in the otic capsule, with opercularis muscle; (4) many details of cranial development, cranial muscles, and thigh muscles, especially between Ascaphus and the Urodela, as shown by Pusey and Noble; (5) essentially similar manner of vertebral development, quite consistent with derivation of both orders from Temnospondyli; (6) presence in the larva of Leiopelma of a salamander-like gular fold, four limbs, and no suggestion of modification from a tadpole (Stephenson).

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