~oologicalJournalof the Linnean Society (1988), 94: 1-38. With 13 figures
Evolution of pipoid frogs: intergeneric
relationships of the aquatic frog family
Pipidae (Anura)
DAVID C. CANNATELLA* AND LINDA TRUEB
Museum of JVatural History, and Department of Systematics and Ecology,
The University of Kansas, Lawrence, KS 66045-2454, U.S.A.
Received April 1987, accepted for publication September 1987
The 27 species of the aquatic frog family Pipidae are currently arranged in four genera: Xenopus (15
species), Hymenochirus (four species), and the poorly known genus Pseudhymenochirus (one species)
occur in Africa; Pipa (seven species) is found in South America and lower Central America. Despite
extensive work on the biology of Xenopus from various disciplines, the evolutionary relationships of
Xenopus to other pipids have not been resolved. Phylogenetic analyis of morphological features of
pipid frogs indicates that, contrary to earlier opinions, Hymenochirus and Pipa are closest relatives
(sister-groups); these genera are placed in the subfamily Pipinae. Also, the currently recognized
species of Xenopus do not form a natural group; the species tropicalis and epitropicalis are more closely
related to Hymenochirus
Pip, than to the remaining species of Xenopus. The two discordant species
are transferred to the genus Silurana, which is relegated to the new subfamily Siluraninae; it is the
sister-group of the Pipinae. The remaining species of Xenopus constitute a monophyletic group that
is placed in the subfamily Xenopodinae as the sister-group of the other genera of pipids.
+
KEY WORDS :-Anura-Pipidae-phylogeny-Pipa-Hymenochirus-Xenopus-Sna.
CONTENTS
Introduction . . . . .
Historical overview
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Material and methods . . .
Results
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Analysis of characters . . .
General shape of the skull .
Nasal region . . . .
Frontoparietal
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Parasphenoid . . . .
Pterygoid. . . . .
Squamosal and middle ear
Eustachian tubes . . .
Maxillary arch
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Lowerjaw
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Neurocranium
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Hyolaryngeal apparatus .
Vertebral column . . .
Pectoral girdle
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*Present address: Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803, U.S.A.
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0024-4082/88/090001+ 38 $03.00/0
0 1 9 8 8 The Linnean Society of London
2
D. C. CANNATELLA AND L. TRUEB
Forelimb . . . .
Pelvic girdle . . .
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Hind limb
Integument . . .
Miscellaneous. . .
Reproduction and larvae
Discussion. . . . .
P i p a . .
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Hyrnenochirus . . .
Silurana . . . .
Pipidae . . . .
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Relationships.
Classification. . .
Xenopus and other f r o p
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Acknowledgements
References.
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Appendix I
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Appendix 2 . . . .
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37
INTRODUCTION
The pipid frog Xenopus laezis (Daudin) has become one of the most commonly
used laboratory animals. I t is the mainstay of a wide variety of research in
developmental and molecular biology (e.g. Roe, Ma, Wilson & Wong, 1985;
Gerhart & Keller, 1986). Polyploidy in anurans is relatively rare, yet there are
diploid, tetraploid, octoploid and dodecaploid species of Xenopus (Tymowska,
1977; Burki & Fischberg, 1985) a t least one species has been demonstrated to be
an allopolyploid (Carr, Brothers & Wilson, 1987). Important contributions have
been made toward an appreciation of the evolution of the several polyploid
species through investigations of comparative immunology, parasites, and
mitochondria1 DNA (Bisbee et al., 1977; Kobel, 1981; Tinsley, 1981; Carr et al.,
1987). Yet, the relationships of the genus Xenopus to other pipid frogs are not
clear, and indeed the relationships among the genera of pipid frogs are not
agreed upon.
A second, related problem exists. Is X . laeuis a ‘typical’ frog? In other words,
to what degree can conclusions drawn from the study of X . laevis be applied to
other frogs? Xenopus (and pipids) is generally regarded as a very specialized, yet
primitive, frog. Can one distinguish, then, whether a particular characteristic of
interest is a truly primitive. feature or the result of adaptive specialization?
Without some understanding of the relationships of Xenopus to other pipids and
frogs in general, the evolutionary significance of characteristics observed in
Xenopus is unclear; that is, are these particular features associated with the
species Xenopus laevis, the genus Xenopus, the family Pipidae, or other frogs at a
more inclusive level? This question is particularly relevant in that much of the
evidence from developmental biology that bears on the question of origin of
Recent amphibians is derived from Xenopus, and characteristics of the Xenopus
system have been extrapolated to be typical of all frogs (Hanken, 1986).
I n this paper, we present the results of a morphological survey of several taxa
of the family Pipidae in order to (1) summarize the evolutionary novelties that
characterize the family Pipidae, (2) ascertain phylogenetic relationships among
the taxa of pipids, (3) propose a classification that summarizes those
relationships, (4)provide a framework for discussion (in a companion paper in
EVOLUTION OF PIPOID FROGS
3
preparation) of the developmental and evolutionary morphology of this bizarre
group of frogs.
HISTORICAL OVERVIEW
The anuran family Pipidae includes 27 living species. Given that the family
represents less than 1% of the total species of anurans (3438), it has received a
disproportionate amount of attention since its recognition early in the 1800s.
Doubtless, this primarily is a result of the bizarre appearance of pipids, which
are fully aquatic anurans that rarely venture onto land. Pipids are
dorsoventrally depressed frogs that hold their limbs in a laterally sprawled
position, and have fully webbed feet and tiny, dorsally placed eyes. Most pipids
lack eyelids, and all adults retain the larval lateral line system. Several other
morphological features associated with their aquatic mode of life distinguish
pipids from other frogs; for example, they possess a single midline opening for
the Eustachian tube into the pharynx, and lack a tongue. Modifications of the
hyoid apparatus reflect changes in the throat and tongue musculature; the
range of hyobranchial alterations in pipids exceeds that of all other frogs. Their
aquatic adaptations also extend to such behavioural features as a unique mode
of feeding in anurans and an intricate system of acrobatic manoeuvres
performed during courtship and egg-laying.
Currently, four Recent genera are included in the family. The 15 species of
Xenopus (Frost, 1985; Loumont, 1986) apparently are among the least
specialized of the pipids; these frogs are small to moderate-sized, and inhabit
most of sub-Saharan Africa. Hymenochirus includes four species of small frogs,
which are distinguished from Xenopus by having webbed fingers.
Pseudhymenochirus is a poorly known, monotypic genus; both Hymenochirus and
Pseudhymenochirus occur in equatorial Africa. T h e fourth genus, Pipa (seven
species), is exclusively Neotropical, and is distinguished from the other three
pipid genera by its fingertips, which bear a variety of lobed, sensory structures.
The females of the species of Pipa brood the developing embryos on their backs;
development is either indirect (i.e. free-swimming tadpoles hatch) or direct (i.e.
froglet hatches directly from egg).
Pipids are unusual in that their fossil record is among the most extensive and
complete in frogs. Estes (1975a, b, reported Xenopus from the Paleocene of Brazil,
about 60 my. There are five other exclusively fossil genera of pipids, the oldest
being from the Lower Cretaceous of Israel. Relationships among the fossil
genera were discussed by Baez (1981).
The many unusual features of the Pipidae have placed them in a distinctive
position in terms of their relationships to other frogs, and much of their early
taxonomic history reflects attempts to reconcile this morphological distinctiveness. Wagler (1830) considered pipids to be the most primitive of the
anurans because of their aquatic habits and lack of a tongue; consequently, he
divided anurans into two suborders, the Aglossa for the Pipidae, and the
Phaneroglossa for all other frogs. Boulenger (1882) recognized the same
suborders, and further distinguished the two families placed in the Aglossa
(Dactylethridae and Pipidae) on the basis of presence or absence of teeth. Cope
(1865), like Wagler, distinguished pipids as the Aglossa. However, Cope
suggested that the two families (the edentate Pipidae for Pipa, and dentate
4
D. C. CANNAI‘ELLA A N D L. TRUEB
Dactylethridae for Xenopus) had arisen from the different suborders (the
edentate Bufoniformia and the dentate Arcifera, respectively); thus, their
aquatic habits were the result of convergence. Cope concluded that pipids and
dactylethrids probably are not closely related.
However, most other workers (e.g. Beddard, 1895a, b; Ridewood, 1897) who
examined the anatomy of Ripa and Xenopus decided that their similarities
reflected a close relationship. This view was reinforced subsequent to
Boulenger’s (1896) description of the genus Hymenochirus. In his discussion of the
morphology of Hymenochirus, Boulenger (1899) noted that the species seemed to
represent a morphological intermediate between Pipa and Xenopus, which at that
time were placed in separate families. Since Boulenger’s work no one has
questioned seriously the integrity of the Pipidae; however, the question of its
relationship to other anurans is unresolved to date.
T o our knowledge, Noble c1922) was the first worker to place all pipids in a
single family, the Pipidae. Nicholls ( 1916) had included the opisthocoelous
Pipidae in the Aglossa, apart from all other tongued anurans. Because Noble
(1922, 1931) did not accord the tongueless condition much significance, he
included the Pipidae with the Discoglossidae in his suborder Opisthocoela.
Two interpretations of intergeneric relationships within the Pipidae have been
promulgated. In the first, Xenopus and Hymenochirus are considered to be closest
relatives, whereas, in the second, Pipa and Hymenochirus are closest relatives.
Noble (1931) subscribed to the former because he divided the Pipidae into two
subfamilies-the Xenopinae for the African genera (Xenopus, Hymenochirus, and
Pseudhymenochirus), and the Pipinae for the Neotropical Pipa (including
Protopipa). Dunn (1948) also supported the first alternative. He listed several
features that distinguish the African and American genera, and concluded that
the American species formed a natural group. Unlike Noble (1931), Dunn did
not believe that any subfamilial recognition was needed.
Opinion among more recent workers remains divided. For example, Sokol
(1977) assessed relationships among Xenopus, P;Pa and Hymenochirus by means of
a detailed analysis of larval features, and concluded that Xenopus and
Hymenochirus formed a monophyletic group. Goin, Goin & Zug (1978) also
recognized an African Xenopinae and American Pipinae. Estes, Spinar & Nevo
(1978) pointed out that Hymenochirus and Pipa share some derived features to the
exclusion of Xenopus, and Baez (1981) provided a cladistic analysis of
osteological features of fossil and Recent genera of pipids which indicates that
Hymenochirus and P;Pa are closest relatives. Dubois (1983, 1984) followed Noble
(1931 ) and recognized two subfamilies, the Pipinae and Dactylethrinae, for the
Neotropical and African forms, respectively. Frost ( 1985) followed a similar
arrangement, but presented arguments for the validity of the name
Xenopodinae as opposed to the Dactylethrinae.
No detailed treatments for the monophyly of either Xenopus or Hymenochirus
have been presented. Bisbee et al. (1977) analysed relationships among Xenopus
using microcomplement fixation techniques for serum albumin. They
distinguished two lineages for Xenopus, one for X.tropicalis and another for other
species of Xenopus, and estimated their time of divergence at a little more than
30 my. Carr et al. (1987) investigated the phylogeny of Xenopus species using
mitochondria1 DNA, but did not include the species tropicalis in the analysis.
Trueb & Cannatella (1986) provided a cladistic analysis of the species of Pipa,
EVOLUTION OF PIPOID FROGS
5
but did not comment extensively on the monophyly of the genus or its
relationships to other genera. The status of the poorly known Pseudhymenochirus
merlini Chabanaud is open to question, and we will not treat it here.
MATERIAL AND METHODS
Many of the characters surveyed were osteological features of the cranium.
Characters also were taken from the cephalic musculature, skeleton and
musculature of the hyolaryngeal apparatus, pectoral girdle, forelimb (especially
the carpal elements), vertebral column, pelvic girdle and hindlimb (with some
emphasis on musculature of the thigh, and miscellaneous features relating to
mode of reproduction, larval types, and superficial morphology of sense organs
eyes, nostrils, etc).
The following species of pipids were examined: Pipa arrabali Izecksohn, P.
carualhoi (Miranda-Ribeiro), P. myersi Trueb, P. parua Ruthven and Gaige, P.
p$a (Linnaeus), P. snethlageae Muller, Hymenochirus curtipes Noble, Xenopus borealis
Parker, X . epitropicalis Fischberg et al., X . laeuis, X . muelleri (Peters), and X .
tropicalis (Gray). The specimens examined are listed in Appendix 1.
Osteological data were taken from dried skeletons and alizarin-red and
alizarin-red-alcian-blue stained skeletons (Dingerkus & Uhler, 1977). Muscle
dissections were stained using the method of Bock & Shear (1972). Drawings
were made on a Wild M-8 stereoscopic dissecting microscope with camera
lucida attachment.
Evolutionary direction (polarity) of the character-states was determined by
outgroup comparison. Selection of the appropriate outgroups for a phylogenetic
analysis of the Pipidae was done as follows. It is well accepted that the Pipoidea
is a monophyletic group composed of the families Pipidae and the monotypic
Rhinophrynidae. Thus, the Rhinophrynidae (Rhinophrynus) is appropriate as the
first outgroup for this analysis.
A choice of the second outgroup requires some justification. Recent workers
(Lynch, 1973; Duellman & Trueb, 1986) considered the pelobatoids neobatrachians (advanced frogs) to be the sister-group to the pipoids. Pelobatoids
often have been considered to be a plesiomorphic, transitional group between
the most primitive anurans and the neobatrachians. Alternatively, Cannatella
(1988) provided synapomorphies that suggest that the pelobatoids are the
sister-group to the pipoids. Thus, from either view, the choice of the
Pelobatoidea as the second outgroup is justifiable. In the character discussion
below, the term ‘outgroup’ refers to the pelobatoids (megophryines, pelobatines
and Pelodytidae) and Rhinophrynus; if the state in Rhinophrynus is discussed along
with that of the pipids, then ‘outgroup’ refers only to pelobatoids.
When appropriate to the discussion, the distribution of states within the
‘discoglossoid’ frogs (i.e. Ascaphus, Leiopelma, Alytes, Barbourula, Bombina and
Discoglossus) is presented. These genera have been included by some (e.g.
Duellman, 1975) in a superfamily, the Discoglossoidea. Sokol (1977) considered
this group to be monophyletic, whereas others (e.g. Lynch, 1973) treat it as a
primitive grade. In any event, the ‘discoglossoids’are the most plesiomorphic of
the Anura, but they are appropriate as an outgroup only after the states in
R h i n o p h ~ nand
~ the pelobatoids have been considered. The specimens examined
for the outgroups are listed in Appendix 1.
+
6
D. C. CANNATELLA AND L. TRUEB
Figure 1. Cladogram of relationships of pipid taxa. "Characters are reversed within the cladogram.
The occurrence of convergences is indicated with an asterisk. Characters that support the empty
node between Nodes G and I are given in Trueb & Cannatella (1986). Node A: 7 , 9 , 14, 15, 17, 18,
20, 21, 23, 26, 27, 28, 29, 31, 32, 53, 38, 39, 47, 50, 53, 57. 59, 61, 63, 68, 69, 70, 71, 72, 77, 80, 82,
86, 90, 91. Node B: 3, 4, 6, 46, 76, 78. Node C: 5, 10, 43, 54, 55, 56, 75, 83, 93. Node D: 22, 52.
Node E: 1, 2, 8, 12, 20", 24, 25, 34, 41, 44, 45, 48, 58, 60, 64, 65, 72", 73, 74, 7 7 O , 79, 82", 84, 89,
94. Node F: 30*, 85*. Node G: 9", 11, 19, 36, 37, 40, 42, 49, 51, 54", 55", 57", 62, 67, 81, 87, 88, 92.
Node H: 30*, 35, 66,85*. Node I: 13, 16.
I n the following analysis, each numbered character has been defined to have
only two states, primitive and derived; no multistate characters are used. That
state found in the outgroup is considered primitive, and that state found in the
Pipidae or subset of the Pipidae is derived. A matrix of character-states and
pipid taxa is given in Appendix 2. Equally parsimonious alternatives for the
evolution of the character-states are treated in the Discussion,
RESULTS
We present the results of the analysis of evolutionary relationships here in
order to facilitate discussion of the characters. Most branches of the cladogram
(Fig. 1) are well supported by derived character-states. T h e few instances of
parallelism or reversal (honioplasy) are pointed out in the discussion of the
individual characters.
We have found abundant evidence that the family Pipidae is a well-defined
lineage; the 36 synapomorphies render the monophyly of this group the best
corroborated among all of the families of frogs. As was concluded earlier (Trueb
& Cannatella, 1986), the genus Pipa is monophyletic, and additional shared
derived features of the genus have been discovered. Furthermore, synapomorphies that strengthen the lineages within the genus Pipa, especially the P;Pa
parva group (Trueb & Cannatella, 1986), have been added to the tree. Because
only H. curtipes was examined, we cannot comment on the monophyly of
Hymenochirus. Characters that are unique to Hyrnenochirus were not included in
the analysis, even though they may prove to be synapomorphies of the genus
EVOLUTION OF PIPOID FROGS
7
when other species are examined. T h e poorly known, monotypic genus
Pseudhymenochirus is currently under study. This present analysis shows that
Hymenochirus and P;Pa form a well-supported monophyletic group, and these two
genera are placed in the subfamily Pipinae. This departs from previous usage, in
which Pipa alone was in the Pipinae.
The most significant result of this study is that the genus Xenopus, as generally
understood, was found to consist of two independent lineages, one for the species
epitropicalis and tropicalis, and another for other species of Xenopus. These
conclusions differ from those of Bisbee et al. (1977), who considered the two
lineages of Xenopus to be closest relatives. O u r results suggest that X . tropicalis
and epitropicalis are more closely related to Hymenochirus and Pipa, rather than to
other Xenopus. I n order to render Xenopus monophyletic, we have removed the
species tropicalis and epitropicalis from Xenopus and resurrected the name Silurana
for these two species. All other species are retained in Xenopus.
Silurana (formerly Xenopus tropicalis and X . epitropicalis) is the sister-group of the
Pipinae, and we herein erect a new subfamily, the Siluraninae, to accommodate
that genus. Xenopus (sensu stricto) is placed in its own subfamily, the
Xenopodinae, which is the sister-group to Siluraninae Pipinae. T h e rationale
for the designation of subfamilies is given in the Discussion.
+
ANALYSIS OF CHARACTERS
General shape of the skull
(1) I n Xenopus, and Silurana and the outgroups, the general shape of the skull
is rounded and domed in lateral profile (Fig. 2C, F). I n Hymenochirus and P;Pa
the skull is wedge-shaped (Fig. 3C, F); further flattening and expansion of this
wedge shape were used by Trueb & Cannatella (1986) to define groups within
the genus Pipa.
Nasal region
(2) The nasals of the outgroups (Fig. 4) are separate sickle-shaped bones, with
concave anterior margins that partially surround the external nares. T h e nasals
also have well-developed, anteriorly directed processes that extend forward
along the midline (Fig. 4A, C, D). I n Hymenochirus (Fig. 3A) and Pipa (Fig. 3D),
the nasals are large with convex anterior margins. T h e nasals conceal most of
the septomaxillae; this is a derived state.
(3) I n Hymenochirus, Silurana, Pipa and the outgroups, the nasals are
unfused, or only partly fused, to each other. A derived state is found in Xenopus
(sensu stricto) in which the nasals are fused along their entire medial margins
(Figs ZA, 4D). Examination of developmental series of larvae of X . laeuis and X .
muelleri indicates that this fusion is an ontogenetic phenomenon that is not
intraspecifically variable in adults.
(4) I n all species of Xenopus (sensu stricto), the bodies of the nasals are shallow,
resulting in a crescent-shaped bone (Figs 2A, 4D). In other pipids and the
outgroups, the corpus of the nasal is deeper and more robust (Figs l D , 3, 4).
D. C. CANNATELLA AND L. TRUEB
8
5 rnrn
C
E
Figure 2. Skulls of Xenopus and Silurana.A-C, Xenopus rnuelleri (KU 156043, female, 74.9 mm svL) in
dorsal (A), ventral (B) and lateral (C) views. D-F, Silurana epztropicalis in dorsal (D) and ventral (E)
views ( K U 195660, female, 61.1 rnrn); lateral aspect (F) of KU 195661. Missing structures
reconstructed with dashed lines. Cartilage indicated by stipple pattern.
F
Figure 3. Skulls of Hymenochirus and Pipa. A-C, Hymenochirus curlipes (KU 204127, female,
3 2 . 9 m m s v ~ in
) dorsal (A), ventral (B) and lateral (C) aspects. D-F, Pipa parva (USNM 115775,
female, 35.0 mm SVL) in dorsal (D), ventral (E), and lateral (F) aspects. Dashed lines indicate
probable margin of pterygoid. Cartilage shown in stipple pattern.
10
D. C. CANNATELLA AND L. TRUEB
Figure 4. Semidiagrammatic representations of dorsal rostra1 regions o f pipoids. A, Rhinophrynus
dorsalis. B, P$a myersi. C , Silurana d pi tropical is. D , Xenopus muelleri. Nasal bones are stippled.
(5) In the outgroups, the vomers (prevomers auctorum) primitively are paired
palatal bones that underlie the nasal capsules and usually border the medial
margins of the internal nares. The vomers are present in the outgroups, but
absent in Silurana (Fig. 2E), Hymenochirus (Fig. 3B) and Pipa (Fig. 3E).
( 6 ) When present, the vomers are either paired or azygous. They are paired
in taxa of the outgroup, but azygous (the derived condition) in the genus
Xenopus (Fig. 2B).
( 7 ) In the pelobatoids and Rhinophrynus (outgroups), the septomaxillae
primitively are tiny and tri-radiate or U-shaped bones (Fig. 4A). In the Pipidae
the septomaxillae are large, elongate, and flattened, and lie parallel to the arc of
the maxillae along the lateral margins of the nasals (Fig. 4B-D).
(8) The septum nasi is usually cartilaginous in the outgroup. In Hymenochirus
(Fig. 3B) and primitively in Pipa, the septum is bony throughout its length, a
derived feature. Two species of Pipa (Pipa snethlageae and P . pipa) exhibit
secondary reduction of the septum (Trueb & Cannatella, 1986), but this feature
is not coded separately here.
(9) The orbitonasal foramen lies in the anterolateral portion of the
sphenethmoid and allows passage of a branch of the ramus ophthalmicus of the
trigeminal nerve. In Xenopus, Silurana (Fig. 2 ) , and Hymenochirus (Fig. 3A-C) the
lateral expansion of the sphenethmoid is reduced, with the result that the
foramen is only partially, or not, surrounded by bone. In the outgroups, the
orbitonasal foramen is completely enclosed by bone. Therefore, the absence of
the completely bony orbitonasal foramen is most parsimoniously interpreted as a
derived feature uniting the Pipidae, and the presence of the bony foramen in
Pipa a reversal to the plesiomorphic state of the outgroups.
EVOLUTION OF PIPOID FROGS
11
Frontoparietal
(10) All pipoids have azygous frontoparietals. Among the pipoids,
anterolateral processes are present in Pipa, Hymenochirus and Silurana along the
posterior margins of the nasals (Figs 2D-F, 3). Xenopus (Fig. 2A-C) and taxa in
the outgroups lack anterolateral processes.
Parasphenoid
(11) In the genus Pipa, the body of the parasphenoid is wide and has
anterolateral wings (Fig. 3E) that replace part of the planum antorbitale
(cartilaginous posterior wall of the nasal cavity). These alae are absent in the
out group.
(12) In Rhinophrynus, Xenopus, and Silurana, the end of the parasphenoid is
expanded posteromedially between the otic capsules (Fig. 2B, E) . These lateral
expansions are not homologous to the lateral alae of the parasphenoid that
underlie the otic capsules in non-pipoids. Instead, the otic capsules flank the
constriction of the parasphenoid, and are bounded by the corpus of the
parasphenoid anteriorly and the aforementioned lateral expansions posteriorly.
The presence of these lateral expansions is a synapomorphy of pipoids, and is
therefore primitive for the Pipidae. In Hymenochirus and Pipa, the lateral
expansions are absent and the parasphenoid is posteriorly acuminate (Fig. 3);
this is a derived feature.
( 13) Within Pipa, the species arrabali, pipa, and snethlageae bear a small process
on the posterolateral margin of the parasphenoid (Trueb & Cannatella, 1986:
figs 3, 5 ) . The process barely contacts the expanded medial ramus of the
pterygoid. This derived feature is absent in all other pipoids and the outgroups.
Pterygo id
(14) In Xenopus, Silurana, and Pipa, there is a prominent, ventrally directed
flange on the anterior ramus of the pterygoid (Figs 2, 3). The flange is absent in
the outgroups; therefore, this feature is a derived state for pipids. Because
Hymenochirus lacks an anterior ramus of the pterygoid, it is not logically possible
for the flange to be present.
(15) In the pelobatoids, the medial ramus of the pterygoid is not expanded
and articulates with the anteroventral wall of the otic capsule; the Eustachian
tube canal is not concealed by the pterygoid. The medial ramus of the pterygoid
is absent in Rhinophrynus. The posterior and medial arms of the pterygoid are
expanded into a broad plate that invests the otic capsule ventrally and forms at
least part of the floor of the Eustachian tube canal in pipids. This derived state
is found in Xenopus (Fig. 2B), Silurana (Fig. 2E), Hymenochirus (Fig. 3B), and
primitively in the genus Pipa (Fig. 3E)--P. carvalhoi, myersi and parua (Trueb &
Cannatella, 1986).
(16) In Pipa arrabali, P. pipa and P . snethlageae, the medial ramus of the
pterygoid is elongated transversely, and with the posterior ramus invests the
quadrate and the anteroventral surface of the otic capsule (Trueb & Cannatella,
1986: figs 3, 5 ) . The pterygoid basically is tri-radiate in these taxa, and represents
a state derived from the apomorphic condition described above (cf. No. 15).
12
D. C . CANNATELLA AND L. TRUEB
( 1 7) When present, the anterior ramus of the pterygoid usually articulates
medial to the facial flange of the maxilla, in the angle between the pars palatina
and pars facialis. It laterally invests a cartilaginous rod, the posterior maxillary
process, which is continuous anteriorly with the cartilages that support the nasal
capsules, and confluent posteriorly with the pterygoid process of the quadrate.
This condition is found in the pelobatoids and in Rhinophrynus.
In the Pipidae (except Hymenochirus, which lacks an anterior pterygoid
ramus), the anterior arm of the pterygoid invests the maxilla and the posterior
maxillary process of the chondrocranium dorsally instead of laterally (Figs. 2,
3). This is the derived condition.
Squamosal and middle ear
(18) In anurans, the squamosal is generally a tri-radiate (i.e. T-shaped) bone
with an otic ramus (or process) that articulates with the crista parotica, a
zygomatic ramus that forms part of the posterior margin of the orbit, and a
ventral ramus that is applied to the quadrate. In the Pipidae, the squamosal is
uniquely modified into a funnel-shaped structure that houses the columella (Figs
ZC, F, 3C, F), and is derived from fusion of the tympanic annulus and the
squamosal (Trueb & Cannatella, 1986).
(19) Among pipoids, the zygomatic process of the squamosal is present in
Xenopus, Silurana and Hymenochirus, and absent in Rhinophrynus and Pipa (Figs 2,
3). The zygomatic process is present in the pelobatoids. The absence of the
zygomatic ramus is most parsimoniously interpreted as being independently
derived in Pipa and Rhinophrynus.
(20) In the outgroups, the zygomatic process (when present) is usually short
and lacks an articulation anteriorly. Xenopus and Silurana (Fig. 2C, F) are
unique among the taxa studied in having an elongate zygomatic process that
articulates with the anterior ramus of the pterygoid, dorsal to and separate
from the maxilla. We interpret this character to be a synapomorphy of pipids
that is reversed in Node E (Hymenochirus and Pipa). Alternatively, it can be
interpreted as independently derived in Xenopus and Silurana.
(21) Contrary to Lynch (1973), the columella (=stapes) is present in all
pipids, and is derived because it is elongate, and extends anterolaterally around
the sides of the otic capsule to lie within the funnel-shaped squamosal (Figs 2,
3 ) . The columella is absent in Rhinophrynus (an independently derived trait) and
present, but not elongate, in the pelobatoids.
(22) When present, the tympanic annulus is round in the outgroups and in
pipids, except in Silurana in which it is distinctly elliptical.
Eustachian tubes
When Eustachian canals are present in anurans, their openings into the
pharynx usually are located at the posterior corners of the roof of the mouth;
this is the condition in non-pipoid taxa that possess Eustachian tubes. All pipids
have Eustachian tubes; however, pipids exhibit a unique condition among
anurans, because the two Eustachian canals open into the pharynx through a
single, median aperture in the roof of the pharynx. The concomitant
osteological modifications are unusual. First, the medial and posterior rami of
the pterygoid, which are usually slender, are greatly expanded and flattened
EVOLUTION OF PIPOID FROGS
13
into an otic plate that forms at least part, if not all, of the ventral floor of the
Eustachian tube. Second, the ventral surface of the prootic-exoccipital complex
(otoccipital auctorum) bears a transverse furrow to accommodate the Eustachian
tubes (Figs 2B, E, 3B, E). Variation within this derived morphology is
summarized in Characters 23 and 24 below.
(23) In all pipids, the canal for the Eustachian tube is floored at least
partially by the otic plate of the pterygoid. This condition is not present in
Rhinophrynus (which lacks Eustachian tubes) or the pelobatoids.
(24) In Hymenochirus (Fig. 3B) and primitively in Pipa (carvalhoi, parva, pipa
and myersi) (Fig. 3E), the canal is covered completely by the pterygoid, but the
Eustachian tube opening is surrounded only by the mucosa of the pharynx. A
further derivation of this condition occurs in P. snethlageae and P. arrabali (Trueb
& Cannatella, 1986), but this is not included here.
Maxillary arch
The maxillary arch includes paired premaxillae, maxillae and quadratojugals; the latter may be absent. The maxillae and premaxillae usually are
dentate, and generally possess three flanges (when viewed in cross section)
radiating from the corpus: the pars facialis, pars palatina and pars dentalis. The
pars facialis is oriented dorsomedially; the premaxilla bear a distinct alary
process that projects dorsally. The partes palatinae of the maxilla and
premaxilla lie in the horizontal plane and are directed lingually. The third
flange, the pars dentalis, is directed ventrally. Teeth, when present, are located
on the lingual side of the pars dentalis, resulting in a pleurodont condition.
(25) The alary process of the premaxilla usually is oriented more or less
vertically and is distinct from the pars facialis of the premaxilla in the
outgroups, Xenopus (Fig. ZB), and Silurana (Fig. 2E); this is the plesiomorphic
state. Hymenochirus and Pipa differ from all other taxa examined in that there is
no demarcation of the alary process from the body of the pars facialis (Fig. 3).
(26) The pars facialis of the maxilla extends most of the length of the bone. It
is well developed in the outgroups, but greatly reduced (derived trait) in the
Pipidae (Figs 2C, F, 3C, F).
(27) The pars dentalis of the maxilla is present in the outgroups and absent in
the Pipidae. The absence of the pars dentalis in the dentate pipids (Xenopus,
Silurana, P. carvalhoi and P. arrabali) yields an acrodont dentition in these taxa
(Fig. 2B, E).
(28) In the outgroups, the pars facialis of the maxilla does not overlap the
premaxilla; the two are juxtaposed or separated by a slight gap. In all pipids,
the pars facialis of the maxilla overlaps at least slightly that of the premaxilla
(Figs 2B, E, 3B, E).
(29) The quadratojugal connects the maxilla to the articular region of the
quadrate, and generally is a small, slender bone. It is present in the outgroups,
but absent in all pipids (Figs 2, 3).
(30) Teeth are present in the pelobatoids; among the pipoids, Rhinophrynus,
Hymenochirus and several species of Pipa (myersi, parva, pipa, and snethlageae) are
edentate. The most economical explanation for the distribution of this character
is that teeth are primitively present in pipids and were lost independently in
Hymenochirus, the myersi-parva clade (Node H), and the snethlageae-pipa clade.
D. C. CANNATELLA AND L. TRUEB
14
-
-
5 mm
Pipa parva
IOmm
Xenopus muelleri
u
2 mm
Hymenochirus curtipes
Figure 5. Pipid mandibles and hyoids in ventral view. A, Pzpa parua (USNM 115771, female,
35.0 m m s v ~ ) .B, Hymenochirus curtipes (KU 204126, female, 32.5 mm SVL) C , Xenopus muellen
( K U 196043, female, 74.9 mm S V L ) . Cartilage shown in uniform stipple pattern. Irregular stippled
pattern indicates calcified cartilage.
(3 1 ) Primitively, teeth are pedicellate in anurans (and salamanders and
caecilians), as well as short, blunt and bicuspid. Pedicellate teeth are present in
the outgroups. In those pipids that are dentate (Xenopus, Silurana, P. carvalhoi,
and P. arrabali), the teeth are fanglike, monocuspid, and lack the joint between
crown and pedicel.
Lower j a w
(32) I n the outgroups, and in anurans in general, the coronoid process
generally is poorly developed. It is well developed and expanded into a blade-like
flange in all of the Pipidae (Fig. 5) except for P. pipa and P. snethlageae, in which
the flange is reduced to a weak process (Trueb & Cannatella, 1986: fig. 9B); this
secondary absence is not considered in the cladogram.
(33) Among primitive frogs, including the outgroups, the depressor
mandibulae muscle is simple and undivided. A synapomorphy of the Pipidae is
the division of the depressor mandibulae into two discrete parts, here called the
pars interna and pars externa (Fig. 6A, B). These portions are a t least partly
separated by the insertion of the cucullaris on the otic capsule. The pars externa
originates from the upper posterior part of the otic capsule, and the pars interna
from a site that is slightly ventral and lateral to the insertion of the cucullaris
muscle on the otic capsule.
Because of the medial displacement of the jaw articulation relative to the
tympanic annulus, the muscles pass down and forward to wrap around the
posterior face of the otic capsule to reach their points of insertion. Among the
primitive frogs, this feature is unique to the pipids.
EVOLUTION OF PIPOID FROGS
m. dorsalis scapulae
A
m. cucullaris
3mm
1
1
B
15
m. dorsalis scapulae
m. cucullaris
1
v p a r s interna (m.depressor mandibulae)J
pars externa (m. depressor mandibulae)
1
,
,
,
I
3 mm
Figure 6. Jaw muscles. A, Hymenochirus boettgeri (KU 154210). B, Pip. myersi (KU 113664).
(34) In Hymenochirus and P$a (Fig. 6A, B), the pars externa has a bony origin
from hypertrophied crests of the otic capsule. In Xenopus, Silurana, and the
outgroups, the muscle originates from the fascia1 connective tissue covering the
crista parotica.
(35) A uniquely derived condition of the depressor mandibulae is found only
in P. parva and P. myersi (Fig. 6B), in which the pars externa is absent and the
pars interna retains the primitive configuration found in other pipids.
Neurocranium
(36) In the outgroups and most pipids, the articular surfaces of the occipital
condyles are located on the posteromedial aspects of the condyles; in ventral
view the faces of the articular surfaces are oriented posteromedially. In Pipa the
planes of the articular facets are oriented posterolaterally (Fig. 3D, E).
(37) Additionally, Pipa seems to be unique among frogs in that the articular
surfaces of the occipital condyles are flat and subcircular (Fig. 3D, E ) . Other
anurans bear condyles that have rounded, reniform articular facets.
(38) Primitively in anurans, the optic foramen is bound by a cartilaginous
margin that separates it from the oculomotor, trochlear, and the prootic
foramina. In all pipids, the optic foramen is bound in bone; this is a derived
feature. Rhinophrynus has an autapomorphic condition in which Cranial Nerves
11-VII exit through a common bony foramen (Trueb & Cannatella, 1982).
Hyolaryngeal apparatus
(39) In the Pipidae a small hyoglossal fenestra is present in the hyoid plate; it
is formed by the fusion of the medial portions of the hyale, and is a derived
feature (Fig. 5). The greatly reduced hyoglossus muscle passes through this
fenestra. The hyoglossal fenestra is absent in the outgroups.
(40) In the genus Pipa, a large portion of the hyalia has disappeared, but the
hyoglossal fenestra persists, bounded by the proximal remnants of the hyalia.
The hyalia persist in Xenopus, Silurana and Hymenochirus (Fig. 5), although they
are ossified in Hymenochirus.
D. C. CANNATELLA AND L. TRUEB
16
Figure 7. Dorsal and ventral views of pipoid atlases. A-B, Rhinophrynus dorsalis (KU 84883) in dorsal
( A ) and vencral [B) aspects. C-D, Pipa myersi (KU 113663) in dorsal ( C ) and ventral (D) views.
Vertebral column
(41) Most anurans exhibit the primitive condition in which the anterior
margin of the lamina of the atlas is indented or slightly notched, thus exposing
the spinal cord in dorsal view (Fig. 7A). Within the pipids, the laminar margin
is more or less straight in Hymenochirus and Pipa (Fig. 7C), and thus the spinal
cord is not visible dorsally between the occiput and the atlas.
(42) I n the outgroups and in all pipids (except Pipa), there is a slight notch
between the cotyles of the atlas (Fig. 7A, B). I n Pipa, the notch in the
intercotylar region is absent, and the margin is straight or bears a process
(Fig. 7C, D).
(43) The first and second vertebrae are separate in the outgroups. Within the
pipoids, the first two vertebrae are fused in Hymenochirus, Pipa and Silurana; they
are separate in Rhinophrynus and Xenopus.
(44)I n Hymenochirus and Pipa, the spinal foramen between the fused atlas and
axis is greatly reduced in size. T h e foramen is much larger in the outgroups,
Xenopus and Silurana; the first two vertebrae also are fused in the latter genus.
(45) Among anurans, overlap between the neural arches of successive
vertebrae may occur. Usually, the neural arches of the vertebrae bear a single,
posteriorly directed spinous process that overlaps the succeeding vertebra. The
prominent neural arches in Hymenochirus and Pipa seem to inhibit the posteriad
B
A
F=-l
L
A
5 mm
Figure 8. Dorsal views of anterior presacral vertebrae. A, Silurana epitropicalis ( K U 195660, female,
61.1 m m s v ~ )B,
. Xenopus wiltei (KU 195673, female, 55.6rnmsv~).Cartilage indicated by stipple
pattern.
EVOLUTION OF PIPOID FROGS
17
development of the spinous process of the preceding vertebrae. However,
posterior expansion of the neural arches in the parasagittal regions is not
inhibited, and thus the parasagittal processes are produced.
Hymenochirus and P;Pa have paired parasagittal processes, which may be broad
and blunt, or narrow (Fig. 7C). Variation among the species of Pipa is discussed
in Trueb & Cannatella (1986).
(46) The transverse processes of the fourth vertebra are relatively straight in
the outgroups and most pipids (Fig. 8A). In Xenopus, the ends of the processes
are obviously curved posteriorly (Fig. 8B).
(47) In all pipids, the coccyx (urostyle) is fused to the sacrum. It is not fused
in Rhinophrynus. In many of the pelobatoids, the articulation also is fused, a
convergent derivation.
(48) A spinous process on the sacrum is present in all species of P;Pa (except
snethlageae) and in Hymenochirus, but is absent in Xenopus, Silurana and the
outgroups. We consider the absence of the crest in P. snethlageae to be an
autapomorphic loss of that feature (Trueb & Cannatella, 1986); consequently, it
is not included in the cladogram.
Pectoral girdle
(49) In pipoids there is no true prezonal element (omosternum) as described
for such anurans as Rana. However, in the genus Pipa the anterior termini of the
procoracoid cartilage extend anteriorly to the medial tips of the clavicles,
forming a cartilaginous promontory (Fig. 9D). This does not occur in any of the
other taxa studied.
(50) In the outgroups, the epicoracoid cartilages are crescent-shaped; their
posterior ends taper to a point at the sternal end of the coracoids. In the
Pipidae, the epicoracoids are not crescentic (Fig. 9A-D). The posterior ends of
the epicoracoids are expanded, and extend posterolateral to the coracoids to
occupy much of the space between the sternum and the coracoids. Functionally,
the posterolateral epicoracoids seem to be integrated with the sternum.
(51) The posterior ends of the epicoracoids are expanded the most broadly in
the genus Pipa; they extend laterally beyond the lateral margin of the sternum
(Fig. 9D). This is a derived feature, and is not present in other pipids or the
outgroups.
(52) In Silurana, the posterior epicoracoid horns are in contact not only with
the sternal end of the coracoid, but also with the lateral, distal aspect of the
coracoid (Fig. 9B). This condition is not present in any other pipids or the
outgroup.
(53) In the outgroups, the epicoracoid cartilages broadly overlap throughout
most of their lengths. In all pipids, the anterior portion of the epicoracoids abut,
rather than overlap, one another (fused in Hyrnenochirus) (Fig. 9C).
(54) In Silurana, the epicoracoids abut throughout their lengths, with no
overlap (Fig. 9B); this feature is derived relative to the preceding character. In
Hymenochirus, the epicoracoid cartilages are fused to each other (Fig. 9C). We
assume that this fusion is derived from a condition in which the cartilages are
abutted as seen in Silurana; thus, completely abutting epicoracoid cartilages are
a shared derived feature of Hymenochirus and Silurana. However, it is also possible
that fused cartilages of Hymenochirus may have been derived independently from
'
p,
Figurc 9. Pipid pectoral girdlrs in vcntral view. A, Xenopus muellerz ( K U 196043, fcmalr, 7 4 . 9 m m s v ~ ) .B, Silurana epilropica1i.c ( K U 195660, female, 61.1 mmsvL).
C, Hymenochirus curtipes ( K U 204126, female, 32.5 mmsvL). D, Pzpa parna (USNM 115775, female). Cartilage shown in unirorm stipple pattern; irregular stippling
indicates calcification.
5 rnm
Hymenochirus curtipes
1
1
1
1
1
1
C
u
5 rnm
Xenopus muelleri
a
p
EVOLUTION OF PIPOID FROGS
19
partially overlapping cartilages as found in Xenopus. Were this the case, then the
abutting epicoracoids of Silurana would be a synapomorphy only for that genus.
The evolution of this feature has two equally parsimonious interpretations.
Either the completely abutting cartilages arose independently in Hymenochirus
and Silurana, or it is a synapomorphy of Silurana Pipinae that is reversed in
P$a. We have accepted the latter option.
(55) Among the taxa under study, the epicoracoid cartilages are fused
indistinguishably to the sternum in Silurana and Hymenochirus (Fig. 9C, D). In all
other pipoids and in the outgroup, the epicoracoids are not fused to the
sternum. As in the preceding character, the distribution of this character has
two equally parsimonious interpretations. Either it arose independently in
Silurana and Hymenochirus, or it is a synapomorphy of Silurana and the Pipinae
that is reversed in Pipa.
(56) In Xenopus and the outgroups, the sternum is relatively small, its width
being much less than the distance between the glenoid cavities of the pectoral
girdle. The'loss of the sternum in Rhinophrynus is an autapomorphy. In the
derived condition of Silurana, Hymenochirus, and Pipa the sternum is large-i.e. as
wide as the interglenoid distance (Fig. 9B-D).
(57) The clavicle and scapula are separate elements in the Rhinophrynus, Pipa
.(Fig. 9D) and all of the outgroups. In Silurana, Xenopus and Hymenochirus, the
clavicle and pars acromialis of the scapula are fused (Fig. 9A-C). The most
parsimonious arrangement is that this derived feature is a synapomorphy of the
Pipidae, and is reversed in Pipa.
(58) In Xenopus, Silurana, and the outgroups, the sternal end of the coracoid
bears a slight expansion where it joins the epicoracoid cartilage. In Pipa and
Hymenochirus the sternal end is expanded both anterior and posterior to its
longitudinal axis to form a large fan-shaped plate (Fig. 9C, D).
(59) The anterior angle formed between the long axis of the coracoid and the
longitudinal midline of the body is about 55" or less in all pipids, whereas it is
relatively large (62-80") in Rhinophrynus and the outgroups. The smaller angle
represents the derived condition.
(60) In Hymenochirus and P$a (Fig. 9C, D) the angle of the coracoid to the
long axis of the body is reduced further to 33-48". This is a state derived from
that seen in the preceding character. This gradual reduction in the
coracoid-midline angle correlates with an increase in longitudinal length of the
epicoracoid cartilages.
(61) Within the non-pipoids, the scapula is short and stocky in the
discoglossoids (most primitive frogs): Ascaphus, Leiopelma, Bombina, Alytes and
Discoglossus. In the pelobatoids (except Pelodytes) and Rhinophrynus, the scapula is
about two to three times as long as it is wide. All pipids have short scapulae
(Fig. 9). Although the short scapula is primitive for anurans in general, the long
scapula of the pelobatoids and Rhinophynus (outgroups of the Pipidae) indicates
that the reduced scapula of pipids is a reversal and therefore, a derived feature.
(62) The proximal end of the scapula usually bears a notch that separates the
pars acromialis from the pars glenoidalis; this condition is referred to as a
bicapitate or cleft scapula. Whereas all species of the genus Pipa lack the notch,
other pipids and the outgroup possess a cleft scapula. Procter (1921) incorrectly
reported the scapula as lacking a notch in Xenopus and Hymenochirus, and her
mistake has persisted in the literature.
+
D. C. CANNATELLA AND L. TRUEB
20
-
Silurana epifropicatis
Leiopelma hochsfelferi
1 mm
D
PIP0 parva
'
1mm
'
Pipa carvalhai
'
Imm
'
Figure 10. Carpal elements in dorsal view. A, Leiofelm hochstetten', right manus (UMMZ 146852).
B, Szlurana epztroficalis, left manus (KU 195660). C, P+aparva, right manus (USNM 115775). D,
Pipa carualhoi, left manus (KU 128761).
(63) The suprascapular cartilage lies at the distal end of the scapula, and
dorsal to the vertebral column. Primitively in anurans and in the outgroups, the
suprascapula is moderately narrow; in the Pipidae it is greatly expanded and
fan-shaped (Fig. 9).
Forelimb
The primitive arrangement of carpal bones in anurans (Fig. 10A) is seven
elements that are arranged in three series. Immediately distal to the radio-ulna
there are two carpal elements, a medial radiale and lateral uinare. The second
series consists of the postaxial centrale, which is distal to the ulnare, and the
preaxial centrale, distal to the radiale. The third series is composed of three
smaller distal carpals, one each at the base of the first through third
metacarpals. Also, there are generally two or three prepollical elements; these
will not be considered further.
We have used Andersen's (1978) terminology, which is derived from that of
Howes & Ridewood (1888). Both works considered the four digits of the anuran
EVOLUTION OF PIPOID FROGS
21
C
Figure 11. Pipoid pelvic girdles. A-B, Rhznophrynw dorsalis (KU 186799) in lateral (A) and dorsal
(B) views. C-D, Pzpa arrabah (KU 167437) in lateral (C) and dorsal (D) aspects. E, Xenopw wzttez
(KU 195673) in ventral view. Cartilaginous epipubis is stippled.
manus to represent digits 2-5; thus, the ‘prepollex’ represents digit 1, according
to these authors. The three carpalia in primitive frogs are considered to be
carpals 2, 3 and 4.
(64) I n Hymenochirus and Pipa, the ulnare is fused to the postaxial centrale
(Fig. lOC, D); these elements are free in Xenopus, Siluruna, and the outgroups
(Fig. 10B).
(65) In Hymenochirus and Pipa distal carpal 2 is absent (Fig. lOC, D); it is
possible that it is fused to the preaxial centrale, but ontogenetic studies have not
been done to ascertain the ontogeny of the elements. In contrast to the condition
in the neobatrachians, distal carpal 4 remains free in the pipids. In all other
pipids and the outgroup, distal carpals 2 and 3 are free (Fig. IOA, B).
(66) A condition that appears to be unique in anurans is found in P. myersi
and P. parva; in these species the radiale and postaxial centralia ulnare are
fused, resulting in a broad element that traverses the carpus (Fig. 1OC). These
elements are free in all other frogs.
(67) In non-pipoids, Rhinophrynus, Xenopus, Silurana, and Hymenochirus, the tips
of the fingers are simple, and unlobed. In Pipa the fingertips are (primitively)
divided into four lobes. Variation of this character within Pipa has been
documented by Trueb & Cannatella (1986: fig 14).
+
Pelvic girdle
(68) Pipids have a prominent crest on the dorsolateral aspect of the shaft of
the ilium. Such a crest is lacking in Rhinophrynus and the outgroup (Fig. 11).
D. C. CANNATELLA AND L. TRUEB
22
sort -semitend
crur-
A
1
5mm
5 rnm
Ascopbus fruei
sort-semitend tend‘
‘
5mm
I
I
5mm
’
Pipa carvathoi
Etgure 12 Thigh muscles. A-B, Ascaphus h e 2 (KU uncatalogued) in superfic~al(A) and deep vlews
(B) C-D, Pzpa carualhot (KU92729) in superficlal (C) and deep (D) views
(69) I n the outgroups, the junction of the bodies of the ilia form a ‘V’ in
dorsal view (Fig. 1 1B). I n the Pipidae, the junction of the proximal ends of the
ilia form a ‘U’ in dorsal view; this is a derived feature (Fig. 1 lD, E).
(70) Primitively in anurans and in the outgroups, the dorsal prominence of
the ilium is poorly developed, i.e. broad and low (Fig. 11A). I t is well developed
in all pipids (Fig. 11C), but reduced in P. p$a and P. snethlugeae; the secondary
reduction in these two species was considered previously (Trueb & Cannatella,
1986), and is not included here.
(71) Among frogs, the pubis is primitively cartilaginous; it is ossified only in
the pipids. Examination of developmental material of Pipa myersi, H. curtipes, and
X . laevis demonstrates centers of ossification in the cartilage of the pubis.
(72) T h e epipubis is a flat cartilaginous plate located immediately anterior to
the preacetabular zone of the ilium (Fig. 11E). Among the pipids, the epipubis
is present in Xenopus and Silurana, but absent in Hymenochirus and Pipa. It is also
absent in Rhinophrynus and the outgroups; however, in Ascaphus and Leiopeha, an
EVOLUTION OF PIPOID FROGS
0
A
,-crur
23
semirnemb,
,add mog
,-semilend
crur-,
grac rnin-IJ
semitend
grac ma) 8 rnin
ext crur brevisJ
*
5 mm
'
Lplant long
5mm
'
Xenopus muelleri
semitend tend"
I
5mm
'
'
5mm
I
Stlurono epitropica/is
Figure 13. Thigh muscles. A-B, Xenopus muellen (KU 196042) in superficial (A) and deep (B) views.
C-D, Szlurunu epztroptcahs (KU 195663) in superficial (C) and deep (D) views.
epipubis is present, and it seems to be anatomically homologous with that in
Xenopus and Silurana.
The epipubis is a synapomorphy of pipids, but is lost in the ancestor of
Hymenochirus
P$a. The reported presence of an epipubis in Pseudhymenochirus
merlini (Sokol, 1977), a poorly known genus that shares some derived features
with Hymenochirus, suggests that the treatment of the epipubis as primitively
present in the Pipidae is correct.
+
Hind limb
(73) Hymenochirus and Pipa bear crests on the metatarsals, tibiale, and fibulare;
these appear to be ossified intermuscular septa. The crests are absent in Xenopus,
Silurana, Rhinophrynus and all non-pipoids.
24
D. C. CANNATELLA AND L. TRUEB
(74) Nussbaum (1982) described the presence of ossa sesamoidia tarsalia in
species of Pipa, some phrynobatrachine ranids, and the Sooglossidae, based on a
survey of 265 species of frogs. This tarsal sesamoid is an elongate, osseous
element found at the proximal plantar surface of the tarsus. We have observed
this element also in Hymenochirus and all species of Pipa; it is absent in Silurana,
Xenopus, Rhinophrynus and the outgroups.
(75) The pyriformis muscle is present in the outgroup (except Pelobates),
Rhinophrynus and Xenopus, but absent in Silurana, Hymenochirus and P$a.
( 7 6 ) The topographical relations of the distal tendons of the thigh musculature
were employecl by Noble (1922) as a major feature in the classification of higher
frogs. In the posterodorsal section of the thigh there are four superficial muscles
of interest: the sartorius, semitendinosus, gracilis major, and gracilis minor.
Among members of the outgroup (Fig. 12A, B) the tendon of the
semitendinosus (fused with that of the sartorius) passes ventral to that of the
gracilis, as in the bufonoid pattern of insertion (Lynch, 1973). I n Rhinophrynus
and the Pipidae, the insertion tendon of the semitendinosus passes dorsal to that
of the gracilis (Fig. 12C, D). Specifically, in Rhinophrynus, Silurana (Fig. 13C, D ) ,
Hymenochirus and P$a (Fig. 12C, D), the tendon of the semitendinosus pierces
that of the gracilis while passing dorsally to it; thus, this condition is primitive
for the Pipidae.
In Xenopus (Fig. 13A, B) a derived state exists in which the tendon of the
semitendinosus is dorsal to the tendon of the gracilis complex, but completely
free of it. It appears that within the pipoids one can see the evolutionary
‘migration’ of the semitendinosus tendon to a more dorsal position.
(77) In Rhinophrynus, Hymenochirus, Pipa (Fig. 12C, D) and the outgroup, the
tendon of the sartorius is fused with that of the semitendinosus. I n Xenopus and
Silurana (Fig. 13A-D) the bellies of the sartorius and semitendinosus are
partially fused, but the tendon of the sartorius has shifted to insert on the tendon
of the gracilis. This is a derived feature.
(78) Among the outgroups, Hymenochirus and Pipa, the sartorius and
semitendinosus are fused in their distal as well as much of the proximal portions
(Fig. 12C, D). Xenopus and Silurana (Fig. 13A-D) are apomorphic in that the
proximal parts of the muscles are fused, but the distal portions are separate (see
preceding character). In Silurana, the bellies of the sartorius and semitendinosus
are separated distally for only one fourth of the length of the muscles
(Fig. 13C, D ) ; in the species of Xenopus, the bellies are separated for three
fourths of their length (Fig. 12A, B). We consider the condition of slight
separation of the distal portions in Silurana to be primitive, and extensive
separation to be a synapomorphy of Xenopus.
Integument
(79) Among the primitive frogs, the integument is relatively smooth (or warty
in a few). In contrast, the skin of Hymenochirus and Pipa consists of regularly
placed tubercles that are spinose in some species.
(80) As adults, all species of the Pipidae retain the larval lateral line organs.
The lateral line organs are lost in adults of Rhinophrynus and the outgroup. In
EVOLUTION OF PIPOID FROGS
25
Hymenochirus, the lateral line system is not visible superficially, but its presence
was documented by Escher (1925).
(81) The skin a t the corner of the mouth is modified in Pipa into a small
pocket or larger fold. No modification is present in Hymenochirus, Silurana,
Xenopus, R h i n o p ~ r y n ~or
s the non-pipoids. See Trueb & Cannatella (1986) for
discussion of the variation within the genus Pipa.
(82) I n adult Silurana and Xenopus, there is a tentacle at the ventral margin of
the eye. Some workers have assumed this subocular tentacle to be sensory, but
Paterson (1939) pointed out that the terminal portion of the nasolacrimal duct
in X . laevis forms the lumen of the tentacle and exits at its free end. T h e tentacle
is absent in other pipids and the outgroup. I n Pipa and Hymenochirus the absence
of the tentacle is correlated with the absence of a nasolacrimal duct in these
genera. For this reason we interpret the absence of the tentacle in these latter
two genera as a loss, rather than a primitive feature as in the outgroups.
Therefore, the subocular tentacles are present primitively in pipids, but lost in
Hymenochirus and Pipa.
(83) Among the pipids, the palpebral membrane of the eye is well developed
in Xenopus and reduced or absent in Silurana, Hymenochirus, and Pipa; the reduced
condition is derived.
(84) A further derived condition of the palpebral membrane is found in
Hymenochirus and Pipa, in which the membrane is completely absent.
(85) The inner metatarsal tubercle is present in non-pipoids, Rhinophrynus,
Silurana, Xenopus, and all species of Pipa except for P. myersi and P. parva (Trueb
& Cannatella, 1986). I t is also absent in Hymenochirus. We consider its loss to be
convergent in Hymenochirus and the parva-myersi clade (Fig. 1: Node H) .
(86) Keratinous tips are found on the first toes of all pipids except for P. pipa
and P. snethlageae. These dermal modifications are absent in Rhinophrynus and the
outgroup, and thus, their presence is a synapomorphy for the Pipidae. Trueb &
Cannatella (1986) considered the absence of this trait in P. pipa and
P. snethlageae to be an instance of reversal, and it is not considered further here.
(87) I n Hymenochirus, Xenopus, and Silurana, the keratinous tips are black; in
Pipa they are brownish tan when present. We consider the brown tips in Pipa to
be a reduction of the pigment seen in Xenopus, and thus, a derived condition.
MiscellaneouJ
(88) I n Pipa, the nostrils are elongate slits, a derived trait. Other genera of
pipoids and the outgroups have round nostrils.
(89) I n Hymenochirus and Pipa, the nostrils are located at the terminus of the
flattened snout. In Xenopus, Silurana, Rhinophrynus and the outgroup, the nostrils
are placed more dorsal in location.
(90) T h e pupil is round in the Pipidae and vertically elliptical in Rhinophrynus
and the outgroup.
(91) The tongue is absent in pipids, although a small hyoglossal muscle
persists (Horton, 1982). Rhinophrynus and the outgroup have a tongue, but the
tongue of Rhinophrynus is highly modified (Trueb & Gans, 1983).
D. C. CANNATELLA AND L. TRUEB
26
Reproduction and larvae
8
(92) In the genus Pipa, the eggs are deposited on the dorsum of the female
(data unknown for P. myersi and P . aspera). In all other pipids and the outgroup,
the eggs are not carried on the female’s back.
(93) I n Hymenochirus (curtipes and boettgeri) and Pipa (carvalhoi, pipa and parua),
the males and females perform acrobatic turnovers during oviposition (Rabb &
Rabb, 1961, 1963a, b, 1969; Weygoldt, 1976). Swisher (1969) reported similar
behaviour in Xenopus (=Silurana) tropicalis; data are not available for the
recently described species Silurana epitropicalis. Species of Xenopus for which
reproductive behaviours are known (laevis, muelleri) do not share this derived
type of behaviour; this behaviour is not present in the outgroups.
(94) Larvae of Xenopus and Silurana bear a long sensory barbel at each corner
of the mouth. The larvae of Pipa and Hymenochirus lack barbels entirely, as do
the larvae of the pelobatoids. Rhinophrynus has several shorter, finger-shaped
projections around the mouth.
The larval barbels of Xenopus and Silurana are long, thin sensory structures
that are supported by a cartilaginous skeleton and are under muscular control,
much like the barbels in some siluriform catfish. The elongate (but blunter and
shorter) projections around the mouth of Rhinophrynus larvae have been
interpreted by some workers as homologous with the barbels of Xenopus, but
Thibaudeau & Altig (1986) suggested that the structures in Rhinophrynus are
simply modified labial papillae, such as occur around the mouth of most
tadpoles. We conclude that the structures called barbels in Rhinophrynus are not
homologous with the barbels of Xenopus and Silurana. Although the presence of
barbels is undoubtedly a derived feature, the distribution of this state on the
cladogram indicates that the barbels either evolved independently in Xenopus
and Silurana, or were primitively present in the Pipidae, and lost in the ancestor
of Hymenochirus Pipa. Ancillary data are helpful in deciding between these two
interpretations. Spinar (1972) reported long, thin barbels in the fossil larvae of
the Palaeobatrachidae. This extinct family is the sister-group of the Pipidae
(Cannatella, 1986), and the barbels of palaeobatrachids appear to be
homologues of those of Xenopus and Silurana. Therefore, the presence of larval
barbels seems to be a synapomorphy at a more inclusive level than the Pipidae,
and not interpretable as a synapomorphy of Xenopus and Silurana. Loss of the
barbels is therefore a derived features of the Pipinae.
+
DISCUSSION
A cladogram and list of synapomorphies of the pipid taxa treated in this
analysis are presented in Fig. 1. The first part of this discussion is devoted to an
explanation of this cladogram, beginning with the genus Pipa, and following
down the tree.
Pipa
Four characters (13, 16, 35, 66) occur uniquely within the genus Pipa. Two of
these ( 1 3, 16) are synapomorphies for Pipa arrabali, P. pipa, and P. snethlageae
(Node I, Fig. I ) . Character 13, the presence of a small process on the margin of
EVOLUTION OF PIPOID FROGS
21
the parasphenoid, was not included in the cladistic analysis of the species of P;Pa
by Trueb & Cannatella (1986); it is a unique feature among pipids that
strengthens Node I of the tree presented in this paper. Character 16, the
transversely elongate medial ramus of the pterygoid, is correlated with the slight
ventral exposure of the Eustachian tube by the medial ramus of the pterygoid
(character EUSTAPT of Trueb & Cannatella, 1986).
Characters 35 and 66 are unique to P. myersi and P.parva (Node H),and
were not used by Trueb & Cannatella (1986). These features, a distinctive
arrangement of the depressor mandibulae muscles (35), and a fusion of carpal
bones seen nowhere else in the Anura (66), provide compelling evidence for the
close relationship of these two species. As noted by Trueb & Cannatella (1986),
this branch of the Pipa cladogram was weakly supported previously.
Two other derived states occur within Pipa and also in Hymenochirus:
Characters 30 and 85. Both of these have alternative explanations. Teeth are
present primitively in the Pipidae and were lost (30) independently in
Hymenochirus (Node F), the P. myersi-parva (Node H), and the P. snethlageae-pipa
clade. Alternatively, teeth were lost at Node E and regained in the ancestor of
P. carvalhoi and Node I (unlabelled node). We view the independent loss of teeth
three times as more likely.
The loss of the inner metatarsal tubercle (Character 85) also has occurred
convergently in Hymenochirus and the P. myersi-parva clade. Alternatively, the
tubercle was lost at Node E and regained at the unlabelled node of the tree.
There are 14 unique synapomorphies for the genus Pipa (Node G), and two
reversals, the fusion of the clavicle and scapula (Character 57) and condition of
the orbitonasal foramen (Character 9) are synapomorphies for the Pipidae
(Node A) that are reversed for the genus P$a. The unique synapomorphies (no
homoplasy) include the following characters: presence of anterolateral wings of
the parasphenoid (1 l ) , absence of a zygomatic ramus of the squamosal (19),
shape and orientation of the occipital condyles (36, 37), conformation of the
margin of the intercotylar region of the atlas (42), absence of hyalia from the
hyoid apparatus (40), expanded procoracoid cartilage (49), laterally expanded
posterior horns of the epicoracoids (51), and uncleft scapula (62). Features of
the epidermis include the lobate fingertips (67), the pocket a t the corner of the
mouth (811, and brown keratin (rather than black) on the toe tips (87), and slitlike nostrils (88). Lastly, Pipa is the only pipid genus in which eggs are carried
on the dorsum of the female (92).
Two additional synapomorphies exist for Pipa,but the evolutionary history of
these features has two, equally parsimonious interpretations. Characters 54 and
55 describe the relation of the epicoracoid cartilages to each other and to the
sternum. The derived state of both characters occurs in Hymenochirus and
Silurana; thus, in both genera, the epicoracoid cartilages abut throughout their
entire lengths (with further autapomorphic fusion of the epicoracoids in
Hymenochirus), and the cartilages are fused indistinguishably to the sternum. I n
Xenopus and Pipa, the epicoracoids have a slight posterior overlap, and are not
fused to the sternum. Because there is overwhelming evidence (see below) that
Hymenochirus is the sister-group of Pipa, the distribution of the states of these two
characters can only be explained by homoplasy in the system. Either these two
characters have evolved independently in Hymenochirus and Silurana, or they
evolved in the ancestor of Silurana Pipinae (Node C) and are reversed in Pipa
+
D. C. CANNATELLA AND L. TRUEB
28
(Node G). We have chosen the latter interpretation, although we acknowledge
that an argument can be made for the alternative explanation.
Hymenochirus
In the present work we have studied H.curtipes primarily and, thus, we are
not prepared to comment on relationships among the four species of that genus;
however, a taxonomic and phylogenetic analysis of the species of Hymenochirus
and Pseudhymenochirus is underway (Cannatella & Trueb, in preparation).
Nevertheless, the sister-group relationship of Hymenochirus and P;Pa is extremely
well corroborated, and taxonomically, we consider the clade composed of
Hymenochirus Pipa to be the subfamily Pipinae (Node E). There are 21 shared
derived features uniting Hymenochirus and P$a, of which none undergoes
homoplasy: 1, 2, 8, 12, 24, 25, 34, 41, 44, 45, 48, 58, 60, 64, 65, 73, 74, 79, 84,
89 and 94. This suite includes features associated with the shape of the skull
(Character l ) , the nostrils, nasals and nasal septum (2, 8, and 89), parasphenoid
( 12), Eustachian canal (24), maxillary arch (25), depressor mandibulae
musculature (34), vertebral column (41, 44, 45, 48), pectoral girdle (58, 60),
carpal bones (64, 651, hind limb osteology (73, 74), integument (79), and
palpebral membrane (84). Additionally, the only trait that supports an
alternative arrangement is Character 9, the fusion of the clavicle and scapula;
this is shared by Xenopus, Silurana, and Hymenochirus. I n light of the large number
of synapomorphies shared by Hymenochirus and Pipa, the absence of fusion of
these elements in Pipa must be viewed as a reversal.
+
Silurana
The nine derived features (Node C) that unite Silurana with the Pipinae are
less numerous, but nonetheless convincing. Two of these, 54 and 55, exhibit
homoplasy in that they are reversed in Pipa, as discussed above. The other seven
are unique occurrences: the absence of vomers (5), the anterolateral processes of
the frontoparietal ( l o ) , fusion of the first two vertebrae (43), large sternum (56),
loss of pyriformis muscle (75), reduction of palpebral membrane (83), and
mating behaviour (93).
The derived features a t Node C demonstrate that the species tropicalis and
epitropicalis, generally placed in Xenopus, are related more closely to
Hymenochirus Pipa than to species of Xenopus; therefore, we have resurrected the
name Silurana Gray, 1864 to accommodate these two species. A third, unnamed
species (Reumer, 1985) probably is referrable to this genus.
The two species of Silurana are united by two unique synapomorphies:
Characters 22 (elliptical tympanic annulus) and 52 (conformation of the
posterior epicoracoid horns). Six synapomorphies support the monophyly of the
genus Xenopus: fusion and shape of the nasals (3, 4), azygous vomers (6), shape
of the transverse processes (46), and features of the semitendinosus muscle (76,
78).
There are four derived features that unambiguously support the monophyly
of Xenopus Silurana, and therefore, would potentially falsify the proposed
arrangement. These characters are: elongate zygomatic process of squamosal
(20), presence of an epipubis cartilage (72), partial fusion of the sartorius and
+
+
EVOLUTION OF PIPOID FROGS
29
semitendinosus tendons (77), and the presence of a subocular tentacle (82).
However, the hypothesis of Xenopus-Silurana monophyly is falsified by the nine
synapomorphies at Node C that ally Silurana to the Pipinae. It is possible to
interpret the features shared by Xenopus and Silurana either as convergences in
both taxa, or synapomorphies of the Pipidae (Node A) that are lost at Node E.
As discussed above (see Analysis of Characters), we have opted for the latter
alternative. Also, additional evidence for Character 72 (epipubic cartilage)
suggests that our initial assessment needs to be re-examined.
The epipubic cartilage (Character 72) has been reported to be present in
Pseudhymenochirus (Sokol, 1977) although we have not examined material of this
poorly known genus. From the limited morphological details of adult
Pseudhymenochirus, and the description of the larva (Sokol, 1977), it seems this
genus is most likely the sister-group of Hymenochirus. Thus, the broader
distribution of the epipubic cartilage among pipids requires its interpretation as
a primitive feature of pipids that is lost in Hymenochirus and Pipa, rather than a
potential shared derived feature of Silurana and Xenopus.
The subocular tentacle (Character 82) is another derived feature that at first
glance seems to ally Xenopus and Silurana. The function of the tentacle is relevant
to an evolutionary interpretation of its usefulness as a synapomorphy. The
tentacle is a conduit for the nasolacrimal duct, which terminates at the open end
of the tentacle. The nasolacrimal duct is present in most frogs, but absent in
Hymenochirus and Pipa. Therefore, the correlated lack of a tentacle in
Hymenochirus and Pipa can be interpreted as a loss, and the presence of the
tentacle as a synapomorphy of the Pipidae, rather than of Xenopus and Silurana.
However, there is no simple explanation for the homoplasy of Characters
20 and 77. The greatly elongate zygomatic ramus of the squamosal (20) and the
insertion of the sartorius tendon on the tendon of the gracilis (77) are such
distinctive features that we postulate that they were lost in the ancestor of the
Pipinae (Node E), rather than evolved independently in Xenopus and Silurana.
Nonetheless, the generic separation of Xenopus and Silurana is justified. The
characters that separate Xenopus and Silurana are listed in Table 1.
Pipidae
There are 36 synapomorphies of the Pipidae. Five of these are characters that
are reversed in the ancestor leading to Hymenochirus and Pipa (Node E), and
were discussed above. Two additional characters, the condition of the
orbitonasal foramen (9) and the fusion of the clavicle and scapula (57), are
synapomorphies of the Pipidae that are reversed in the genus Pipa (Node G).
The 30 remaining synapomorphies are unique. These include the greatly
enlarged septomaxillae (7), reduced pars facialis (26), and absence of pars
dentalis (27) of the maxilla. When present, teeth are fang-like and nonpedicellate (31). The pars facialis of the maxilla at least partially overlaps that
of the premaxilla (28). Also, the quadratojugal is absent (29). The pterygoid is
modified in several ways; the anterior ramus invests the maxilla dorsally instead
of laterally (17). Also, the anterior ramus of the pterygoid bears a ventrally
directed flange (14) that is usually associated with the expanded coronoid process
of the mandible (32). Several synapomorphies are associated with the ear and
Eustachian tubes. The posterior and medial arms of the pterygoids are
30
D. C. CANNATELLA AND L. T R U E B
TABLE
1. Distinguishing features of Silurana and Xenopus
~
Feat u rr
Xenopus
Silurana
Sasals
Vomers
Anterolateral processes of frontoparietals
Palpebral membrane
Tympanic annulus
First and second presacral vertebrae
Transverse proressrs of fourth vertebra
Stcrnum
Posterior epicoracoid horns contact lateral aspect
of coracoid
Condition of epiroracoid cartilages along midline
Relation of epicoracoid cartilages and sternum
Pyriformis muscle
Position of semitendinosus tendon relative to
gracilis tendon
Separation of bellies of sartorius and semitrndinosus complex
Basic diploid number [Burki & Fischberp. 1985)
Globin polypeptide bands (Burki & Fischberg,
I985 )
Fused
Azygous
Absent
Normal
Round
Separate
Curved strongly
Small
Ah e n t
Separate
Absent
Present
Reduced
Elliptical
Fused
Curved weakly
Large
Present
Overlapping
Not fused
Present
Semitendinosus tendon
dorsal to that of gracilis
'rhrre-quarters of length
Abutting
Fused
Absent
Semitendinosus tendon
pierces that of grarilis
One-quarter of length
18
5 or more
4
20
expanded into a large plate (15) that forms part of the floor of the Eustachian
tube of pipids (23). The squamosal is modified into a conch-shaped structure
(18) that houses an elongate columella (21). The optic foramen is completely
surrounded by bone (38), and the depressor mandibulae is separated into two
discrete portions, separated by the insertion of the cucullaris muscle ( 3 3 ) .
The hyoid apparatus of pipids is perhaps the most variable among the
families of frogs (Fig. 5). Yet, all pipids share the reduced hyoglossal fenestra
(39) as a synapomorphy; this appears to be related to the fact that all pipids
lack tongues (9 1 ) . The pupils of pipids are round (90).
The pectoral girdle of all pipids is highly modified; the anterior portion of the
epicoracoid cartilages abut, rather than overlap (53), and the posteriormost
ends of the epicoracoids are greatly expanded (50). Also, the angle between the
long axis of the coracoid and the longitudinal midline axis of the body (59) is
about 55" or less in the Pipidae. In all pipids the scapula is very short (61) and
the suprascapula very large (63).
The sacrum and coccyx are fused in the Pipidae (Character 47); also, the
pelvic girdle is highly modified. Large crests are present on the shaft of the ilium
(68), as well as a large dorsal prominence on the body of the ilium (70). The
junctions of the proximal ends of the ilia form a 'U', and the pubis is ossified
(71) in all pipids.
The integument of pipids is also modified; lateral line organs are retained
from the larval stages (80), and the tips of the first three toes have keratinous
caps (86).
Relationships
As noted briefly in the preceding section (Results), we concluded the
following about the relationships of generic groups of pipids: (1) The genus Pipa
is monophyletic, and additional synapomorphies were discovered that
EVOLUTION OF PIPOID FROGS
31
strengthen the cladogram of the species of Pipa in Trueb & Cannatella (1986).
There is no evidence supporting the recognition of Hemipipa or Protopipa as
genera separate from Pipa. (2) Hymenochirus (as represented by the species
curtipes) is the sister-group of Pipa; this is in accord with the analysis of Baez
(1981). (3) The genus Xenopus, as traditionally understood (Frost, 1985), is
paraphyletic; that is, the species epitropicalis and tropicalis are more closely related
to Hymenochirus Pipa than to the other species of Xenopus. Accordingly, the
genus Silurana Gray, 1864, is resurrected for these species. (4)The three species of'
Xenopus that were examined form a monophyletic group. Currently, we are
engaged in a more detailed study of the morphology of the remaining species of
Xenopus, in order to allocate correctly the other species to either Silurana or
Xenopus.
A variety of cytological, electrophoretic, morphological and parasitological
data supports the separation of Silurana from Xenopus. However, because
comparisons generally have not been made with Hymenochirus and Pipa, it is not
possible to conclude whether these data support our hypothesis that Silurana is
the sister-group to Hymenochirus Pipa, rather than to Xenopus. Silurana tropicalis
and S. epitropicalis have 20 and 40 chromosomes, respectively (Tymowska &
Fischberg, 1982); the latter species is tetraploid. Most species of Xenopus are
tetraploids, with 36 chromosomes; three species (octoploids) have 72 and one
species (dodecaploid) has 108 (Burki & Fischberg, 1985). Thus, the basic
diploid number in Silurana is 20, and that of Xenopus is 18. Chromosome
numbers for other pipids were summarized by Duellman & Trueb (1986) as
follows: Hymenochirus boettgeri, 24; P. carvalhoi, 20; P. pipa, 22; and P. parva, 30.
Given the variation in diploid number in Hymenochirus and Pipa, it is difficult to
make statements about pipid relationships solely on the basis of chromosome
number.
Other lines of evidence support the divergence of Xenopus and Silurana. Burki
& Fischberg (1985) used electrophoretic analysis to determine that both species
of Silurana possess four distinct globin polypeptides, whereas all other species of
Xenopus have five or more. Also, all species of Xenopus (for which data are
known) are infected with the monogenean parasite Protopolystoma xenopodis
(Price), whereas S. tropicalis is not (Tinsley, 1981 ) . Loumont ( 1981) documented
that the morphology of the vocal apparatus of S. tropicalis differs substantially
from that of Xenopus; she did not comment on Pipa or Hymenochirus. Reumer
(1985) compared the cranial osteology of most of the species of Xenopus and
placed the species of Silurana in one group, and divided the other species of
Xenopus into three groups. His Group 1 (tropicalis and epitropicalis) differed from
the three other groups in having paired, rather than fused, nasals. We have
cited the fused nasal condition (Character 3) as a synapomorphy of the genus
Xenopus (sensu stricto).
Data from microcomplement fixation using serum albumin are also relevant.
Bisbee et al. (1977) demonstrated immunological distances of 51-61 units
between S. tropicalis ( = Xenopus in their paper) and the species of Xenopus tested
(borealis, clivii, fraseri, laevis and rnuelleri). The greatest distance between any two
species of Xenopus was 17 units. Also, a distance of 180 units was found between
X . laevis and Hymenochirus, and more than 200 units between X . laevis and
P. pipa. No direct comparisons were made between S. tropicalis and Hymenochirus
or Pipa; nonetheless, the work of Bisbee et al. (1977) suggests that Silurana is the
+
+
D. C. CANNATELLA AND L. TRUEB
32
+
sister-group of Xenopus, rather than of Hymenochirus Pipa, as we have suggested.
More generally, their evidence supports the formal separation of the species
tropicalis and epilropicalis from Xenopus.
Additionally, the distances of 180 units between Hymenochirus and Xenopus, and
>200 units between Pipa and Xenopus, suggest that Xenopus is more closely
related to Hvmenochirus than to Pipa, a conclusion again at odds with our
phylogeny, in which more than 20 synapomorphies ally Pipa and Hymenochirus
(Node E), and only two derived characters (9 and 57) are shared by Xenopus,
Silurana and Hymenochirus.
As discussed above, evidence from diverse sources has demonstrated that
Silurunu LropicaEis is highly divergent from Xenopus. However, demonstration that
this species was not the sister-group to Xenopus (as was generally assumed)
requires critical comparisons with Hymenochirus and Pipa, which were lacking
heretofore. We conclude from phylogenetic analysis of morphological evidence
that the species tropicalis and epitropicalis are more closely related to
Hvmenochirus Pip, than to Xenopus, although a few derived features support the
traditional idea that Silurana and Xenopus form a monophyletic group. The
challenge, then, is to adduce comparable nonmorphological data for
Hymenochirus and/or Pipa in order to corroborate or refute our claim that all
species formerly called Xenopus are not each others’ closest relatives.
+
Classlfication
The large number of characters and the relatively low amount of homoplasy
(convergences and reversals) involved justify a new proposal of infrafamilial
units for the Pipidae. We propose the following sequenced phylogenetic
classification. I n sequenced classifications (Wiley, 1979), the ordinal sequence of
taxa of equal rank defines a nested set of sister-group relations; therefore, the
Xenopodinae is the sister-group of Siluraninae Pipinae. Rationale for authors
and dates follows Frost (1985).
+
Pipidae Gray, 1825
Xenopodinae Fitzinger, 1843
Xenopus Wagler, 1827
Siluraninae new subfamily
Silurana Gray, 1864
Pipinae Gray, 1825
Pipa Laurenti, 1768
Hymenochirus Boulenger, 1896
Frost (1985), following the more traditional arrangement, placed Xenopus and
Hymenochirus in the Xenopodinae and Pipa in the Pipinae, but J. D. Lynch, in a
comment under the Xenopodinae account (Frost, 1985: 425), noted that “the
monophyly of this group has yet to be demonstrated”. Dubois (1983, 1984)
utilized the name Dactylethrinae in place of the Xenopodinae. We have
followed the arguments of Frost (1985) in regarding Xenopodinae as the correct
name.
EVOLUTION OF PIPOID FROGS
33
We introduce the new subfamily Siluraninae with some hesitation-not
because there is lack of evidence, but because of conventional taxonomic
practices. There is opposition to the proliferation of new and often redundant
taxa that a phylogenetic classification often promotes. (Siluraninae is redundant
in that the content of the subfamily is the same as that of the genus Silurana.) O n
the other hand, the 1985 Code of <oological Nomenclature does not require that
every genus be placed in a subfamily if subfamilies are recognized; however, this
is the custom in anuran taxonomy. An alternative classification that avoids
redundant categories is to recognize the subfamily Pipinae for Hymenochirus and
Pipa, and not to recognize subfamilies for either Xenopus or Silurana. We feel the
latter choice would be detrimental, because Xenopus and Silurana, by default,
would be placed in the Xenopodinae, thereby rendering that subfamily
paraphyletic.
Xenopus and other frogs
This analysis demonstrates that Xenopus (excluding tropicalis and epitropicalis) is
the sister-group to all other pipids, rather than the sister-group to Hymenochirus,
as present-day biogeography would suggest. More generally, how does Xenopus
compare with other groups of pipids? The number of derived states possessed by
a clade can be used as a rough measure of primitiveness or derivedness. There
are 37 shared derived features of the Pipidae; because these are common to all
pipids, they can be excluded from comparisons among the taxa. We have found
six synapomorphies for Xenopus, 11 for Silurana (sum of Nodes C and D), 34 for
the Pipinae (Nodes C and E) and 52 for Pipa (C, E and G). We have not
considered Hymenochirus separately because data were gathered from only one
species, and derived features unique to that species were not included in the
analysis. By this measure, Xenopus has the fewest derived features (and
conversely, the greatest number of primitive traits) of any of the genera of
pipids. In terms of the characters that we sampled, and relative to other pipids,
Xenopus has diverged little from the ancestor of the Pipidae (Node A ) , and could
be said to be a suitable representative of pipids as measured by morphological
features.
What can be concluded about the primitiveness of Xenopus (and other pipids)
in respect to other frogs? Minimally, all pipids share 37 derived features not
possessed by other frogs. This number far exceeds that of any of the other
‘primitive’ families of frogs (Cannatella, 1988). Thus, Xenopus (and other
pipids) has diverged radically in morphology from the most recent common
ancestor of living frogs; a companion paper to the present one will more
explicitly document the evolutionary trends in pipids.
The notion that pipids are primitive frogs persists. I t seems that this fallacy
stems from (1) a view that the larvae of pipids (and Rhinophrynus) are primitive
(Starrett, 1968, 1973) owing to the absence of keratinous beaks and denticles
found in most tadpoles, and (2) the extensive fossil record of pipids, as far back
as the Lower Cretaceous. The interpretation of the pipoid larva as being the
most primitive type of tadpole is now discredited; pipoid larvae are extremely
derived (Sokol, 1975, 1977). T h e presence of an excellent fossil record is not
evidence that a lineage is primitive; rather, it indicates that the pipid
morphotype may have been conserved over a long period, because the fossils are
easily identified as pipids owing to the numerous derived features present. The
34
D. C. CANNATELLA AND L. TRUEB
family Rhinophrynidae (the sister-group of pipids) must logically be as old as
the Pipidae, yet there are very few rhinophrynid fossils, and Rhinuphrynus is not
thought to be a primitive frog.
Among the genera of pipids, Xenupus has diverged least from the ancestor of
the Pipidae. .As a group, however, pipids are extremely dissimilar from other
frogs, and share many derived features that characterize a morphology atypical
of other frogs. Therefore, when making comparisons among major groups of
vertebrates, one should exercise caution in considering Xenopus to be
representative of other frogs; based on the present study, we would predict
Xenupus to be exceptional rather than typical. Some of the dissimilarity in
characteristics of developmental biology between Xenopus and salamanders, as
summarized by Hanken (1986), may be attributable to the highly derived
nature of pipid frogs.
ACKNOWLEDGEMENTS
We acknowledge the following persons and institutions for loan of specimens:
Pere Alberch and Josk Rosado, Museum of Comparative Zoology (MCZ),
Harvard University; Charles W. Myers, American Museum of Natural History
(AMNH); W. Ronald Heyer, George Zug, and Ronald I. Crombie, United
States National Museum (USNM); Arnold G. Kluge, University of Michigan
Museum of Zoology ( U M M Z ) ; Robert Drewes, California Academy of Sciences
(CAS); Robert F. Inger and Harold Voris, Field Museum of Natural History
(FMNH). William E. Duellman, The University of Kansas, Museum of Natural
History (KU:),criticized the manuscript and provided working space, and Ana
Maria Biez (Universidad de Buenos Aires), Richard Estes (San Diego State
University), and ZbynCk RoEek (Charles University, Prague) engaged in helpful
discussions about pipoid frogs. David Wake, Museum of Vertebrate Zoology
(MVZ), University of California, Berkeley, also provided laboratory space. We
are indebted to Felix Schutte (Museum Alexander Konig, Bonn), Richard
Tinsley (Queen Mary College, University of London), Jaime Pkfaur
(Universidad de 10s Andes, Mtrida, Venezuela), and M. Fischberg, J. Reumer,
and H.-R. Kobe1 (Station de Zoologie Expkrimentale, Universitk de GenZve)
for their continued cooperation and assistance in the provision of specimens and
ancillary data. Linda Ford provided technical laboratory assistance. This
research was supported in part by the Center for Biomedical Research of The
University of Kansas, and was funded by NSF grants BSR 82-07681 and 8508470 to Linda Trueb, and a University of Kansas Dissertation Fellowship to
David Cannatella.
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APPENDIX 1
SPECIMENS EXAMINED
XI1 specimens listed are skeletons; those marked with an asterisk are dry skeletons, and all others are
alizarin-alcian or alizarin preparations.
Hymenochirus rirr/ipe.i- KC‘ 204126, 204128. 204130-37.
,Yenopus borealis K U 192398, MCZ 15988*.
<Yenopuslaeazs K U 69842*, 129700-01*, 195934-35*, MCZ 2174-75*, 15989*, 26585*, 86798*.
.Yenopus mutlleri K U 97201-07, 129699*, 196043*, MCZ 14799*, 27851*, 51689*, 85213*.
.~ilzcranae/Jitropicalis -KU 195660-6 I .
Silurana tropicalis---KU 195667, MCZ 11866*.
f’zpa arrabalz-- AMNH 51 175*, K U 167437*, 167440, 167450, MCZ 85568*.
P i p carualhot--KC 92730*, K U 128761, MCZ 97277-79*.
Pzpa myprsi K U 113663*, UMMZ 132659.
Pipa panla C M M Z 57445, USNM 115775.
Pzpa pipa - 4 X S uncatalogued (two juvenile specimens), KU 129698*, U M M Z 132887*, 152283-84*, 152285,
16840% 09, USNM 39268*.
Pipa snethlagear MCZ 85571 -73*.
Khinophrynus dorsalis AMNH 6212-13, 6225, K U 62137*, 69084-85*, 70978, 84883-86*, 86648, 101952-53,
10 1956. 186799*, 187801-02.
EVOLUTION O F PIPOID FROGS
37
Leptobrachium hasseltii -FMNH 63491, KU 194712.
Megophrys aceras-MCZ 23436-37*.
Megophrys m o n t a n a ~ ~ - K U147205*, M C Z 22635*.
Pelobates cultripes-KU 144225, 148619.
Pelobates fuscus-KU 688 19, 129240*, MCZ 1012*, 10 13-C*.
Pelobates syriacus--KU 146856*.
Pelodytespunctatus-KU 153435*, M C Z 1616-B*, U M M Z 152533.
Scaphiopus holbrookii-KU 69008*, 69087*, 145413*.
Scaphiopus bombifrons- KU 351 I*, 5405.
Scaphiopus multipficatus-~ KU 59855*, 84887*.
APPENDIX 2
Data matrix of taxa and character-states in the present study; 0 =primitive state, I =derived state. Data for
the following groups of species are identical: Xenopus laeuis = muelleri = borealis; Silurana tropicalis = epitropicalis;
Pipa parua = myersi; Pipa pipa = snethlageae. A question mark indicates that it is logically impossible to assess the
state for that taxon.
Xenopus laeuis
Silurana tropicalis
Hymenochirus curtipes
Pipa parva
Pipa carvalhoi
P$a arrabali
Pipa pipa
5
2
3
4
0
0
1
0
0
1
1
0
0
1 0 1 1 0 1 0 0 0 0 1 1 0 1 1 0 1
0 1 ? 1 0 1 1 0 0 0 1 1 0 1 1 0 1
0 1 ? 1 1 1 1 0 1 0 ? 1 0 ? 1 0 0
1
1
1
1
1
1
1
1
0
0
0
0
0
0
0
0
1
1
1
1
6
7
8
9
1 1 1 1 1 1 1 1 1 1 2
0 1 2 3 4 5 6 7 8 9 0
I
?
?
?
1
1
1
1
1
1
0
0
0
1 1 1 0 1 1 0 1 1 1 0
1 1 1 0 1 1 0 1 1 1 0
1 1 1 1 1 1 1 1 1 1 0
?
1
1
0
1
1
1
1
1
1
1
1
1
1
0
2 2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 3 3 3 4
I 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0
Xenopus laevis
Silurana tropicalis
Hymenochirus curtipes
Pipa parva
P$a carvalhoi
Pipa arrabali
Pipa pipa
Xenopus laeuis
Silurana tropicalis
Hymenochirus curtipes
Pipa parua
Pipa carualhoi
Pipa arrabali
Pipa pipa
1
1
1
1
1
1
1
0
1
0
0
0
0
0
1
1
1
1
1
1
1
0
0
1
1
1
1
1
0
0
1
1
1
1
1
1 1 1 1 0 1 1 1 0
1 1 1 1 0 1 1 1 0
1 1 1 1 1 ? 1 1 1
1 1 1 1 1 ? 1 1 1
1 1 1 1 0 1 1 1 1
1 1 1 1 0 1 1 1 1
1 1 1 1 1 ? 1 1 1
0
0
0
1
0
0
0
0
0
0
1
1
1
1
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0
0
0
1
1
1
1
4
I
4
2
4
3
4
4
4
5
4
6
4
7
0 0 0 0 0 1 1
0 0 1 0 0 0 1
1 0 1 1 1 0 1
1 1 1 1 1 0 1
1 1 1 1 1 0 1
1 1 1 1 1 0 1
1 1 1 1 1 0 1
4
8
4
9
5
0
5
1
5
2
5
3
5
4
5
5
5
6
5
7
5
8
5
9
6
0
0
0
1
1
1
1
1
0
0
0
1
1
1
1
1
1
1
1
1
1
1
0
0
0
1
1
1
1
0
1
0
0
0
0
0
1
1
1
1
1
1
1
0
1
1
0
0
0
0
0
1
1
0
0
0
0
0
1
1
1
1
1
1
1
1
1
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
I
1
0
0
1
1
1
I
1
6 6 6 6 6 6 6 6 6 7 7 7 7 7 7 7 7 7 7 8
1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0
Xenopus laevis
Silurana tropicalis
Hymenochirus curtipes
Pipa parua
Pipa carualhoi
Pipa arrabali
Pipa pipa
1
1
1
1
0
0
0
1
1
1
1
1
0
0
1
1
0
0
1
1
0
0
0
1
0
0
0
1
1
1
1
1
1 1 1 1 0 0 0 1 1 1 0 1
1 1 1 1 0 0 1 0 1 0 0 1
1 1 1 0 1 1 1 0 0 0 1 1
1 1 1 0 1 1 1 0 0 0 1 1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0 1 1 1 0 0 0 1 1
0 1 1 1 0 0 0 1 1
0 1 1 1 0 0 0 1 1
38
D. C. CANNATELLA AND L. TRUEB
APPENDIX 2 continued
Xenopus laeuis
Silurana tropicalis
Hymenochirus curttpes
P;Pa parva
Pipa carualhoi
Pipa arrabali
Pipa pipa
8
1
8
2
8
3
8
4
8
5
8
6
8
7
8
8
8
9
9
0
9
1
9
2
9
3
9
4
0
0
0
1
1
1
1
1
1
0
0
0
0
0
0
1
1
1
1
1
1
0
0
1
1
1
1
1
0
0
1
1
0
0
0
1
1
1
1
1
1
1
0
0
0
1
1
1
1
0
0
0
1
1
1
1
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0
0
0
1
1
1
1
0
1
1
1
1
1
1
0
0
1
1
1
1
1