Title: The Ancestry of Modern Amphibia: A Review of the Evidence
Author: Eaton, Theodore H. (Theodore Hildreth), 1907-1981
Language: English
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    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

    [Illustration]

    27-8362



[Transcriber's Notes: Several typos have been regulated.

One typo of "ancester" for "ancestor" was corrected.

One instance of "salamanderlike" corrected to "salamaner-like".]



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


[Illustration: 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.

[Illustration: 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


[Illustration: 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 arch)
   b'oc.--basioccipital
   ce._{1-4}--centrale_{1-4}
   ch.--ceratohyal
   clav.--clavicle
   clei.--cleithrum
   cor.--coracoid
   d.c._{1-4}--distal carpal_{1-4}
   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.

[Illustration: 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.

[Illustration: 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.

[Illustration: 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.

[Illustration: 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.

[Illustration: 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.

[Illustration: 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.

[Illustration: 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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_Transmitted April 7, 1959._





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