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Parallelism and convergence in anuran fangs

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The anuran lower jaw is composed of three pairs of bones: dentaries, angulosplenials and mentomeckelians. Although the lower jaw is toothless, except in Gastrotheca guentheri, enlarged fangs or odontoids have evolved at least four times independently in some myobatrachids, hylids, ranids and leptodactylids through both parallel and convergent evolutionary events. Fangs seem to represent the single best design solution to enable an anuran to inflict a bite-like wound, but the biological role of biting varies among species. Fangs are projections of the dentaries in ranids, but in the hylid frog Hemiphractus and in ceratophryine leptodactylids, they form a sinosteotic unit with the dentaries and mentomeckelians. Comparisons of morphology, behaviour and diet among frog taxa with enlarged fangs reveal that the fangs may be the result of either sexual or natural selection. Those fangs that evolved in response to sexual selection seem to be relatively larger than those that resulted of natural selection.
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J. Zool., Lond. (2003) 260,41–51 C
2003 The Zoological Society of London Printed in the United Kingdom DOI:10.1017/S0952836903003479
Parallelism and convergence in anuran fangs
Marissa Fabrezi1*and Sharon B. Emerson2
1CONICET, Museo de Ciencias Naturales, Universidad Nacional de Salta, Mendoza 2, 4400-Salta, Argentina.
2Department of Biology, University of Utah Salt Lake City, UT 84112 U.S.A.
(Accepted 2 September 2002)
Abstract
The anuran lower jaw is composed of three pairs of bones: dentaries, angulosplenials and mentomeckelians.
Although the lower jaw is toothless, except in Gastrotheca guentheri,enlarged fangs or odontoids have evolved
at least four times independently in some myobatrachids, hylids, ranids and leptodactylids through both parallel
and convergent evolutionary events. Fangs seem to represent the single best design solution to enable an anuran
to inflict a bite-like wound, but the biological role of biting varies among species. Fangs are projections of the
dentaries in ranids, but in the hylid frog Hemiphractus and in ceratophryine leptodactylids, they form a sinosteotic
unit with the dentaries and mentomeckelians. Comparisons of morphology, behaviour and diet among frog taxa
with enlarged fangs reveal that the fangs may be the result of either sexual or natural selection. Those fangs that
evolved in response to sexual selection seem to be relatively larger than those that resulted of natural selection.
Key words:Anura, odontoid, convergence, parallelism, evolution
INTRODUCTION
Interesting, but little-studied, morphological features of
some anuran amphibians are fang-like outgrowths of
the lower jaw, usually referred to as odontoids (Fig. 1).
Traditionally, the term odontoid has been applied to
rigid structures superficially similar but not equivalent
to true teeth (Trueb, 1973). Although rare, odontoids
have evolved independently in species belonging to four
families of frogs: ranids, myobatrachids, leptodactylids
and hylids (Noble, 1931; Duellman & Trueb, 1986; Ford
&Cannatella, 1993) (Fig. 2). Furthermore, they seem to
have arisen more than once within the subfamily Raninae
(Bossuyt & Milinkovitch, 2000) and within the family
Hylidae (Sheil et al., 2001). Although the biological role
of fangs (sensu Bock & Von Wahlert, 1965) has not been
examined in most species, their functional significance is
clear. The structures inflict a bite-like wound when the
frog closes its jaws on an object.
Frog odontoids provide an excellent opportunity to
learn more about the repeated, independent evolution
of similar structures, an evolutionary phenomenon that
is often cited as evidence of the strong influence of
selection in the evolution of effective functional design
(Dawkins, 1987). Frog odontoids have evolved in a suf-
ficient number of different taxa to allow phylogenetic
*All correspondence to: Marissa Fabrezi.
E-mail: museo@unsa.edu.ar
comparison of both the ontogenetic pathways and evol-
utionary processes producing the fangs. Herein, we
(1) describe the interspecific similarities and differences
in the developmental pathways and adult phenotypic
structure of frog odontoids; (2) determine the biological
role(s) of fangs in species that possess them; (3) discuss
our findings in the context of other recent work on
parallelism and convergence (e.g. Hodin, 2000).
MATERIALS AND METHODS
The odontoids of species belonging to the Ranidae,
Hylidae and Leptodactylidae were examined. Dimorpho-
gnathus (subfamily Petropedetinae, family Ranidae) was
the only genus known to have species with odontoids
that was not part of the study. Species included
were Aubria subsigillata,Ceratobatrachus guentheri,
Conraua alleni,Conraua crassipes,Conraua goliath,
Hoplobatrachus occipitalis,Nyctibatrachus major,Occi-
dozyga laevis,Platymantis guyypi,Platymantis vitiensis,
Ptychadena anchietae,Ptychadena mascareniensis,
Ptychadena mossambicus,Pyxicephalus adspersus,Rana
cancrivora,Rana corrugata,Rana cyanophlyctis,
Rana hexadactyla,Rana limnocharis,Rana rugulosa,
Rana tigrina,Sphaerotheca pluvialis and Sphaerotheca
cryptotis (Ranidae); Hemiphractus fasciatus,Hemiphrac-
tus proboscideus and Phyllodytes auratus (Hylidae);
Ceratophrys cranwelli,Chacophrys pierotti,Lepidobat-
rachus asper,Lepidobatrachus laevis,Lepidobatrachus
42 M. FABREZI AND S. B. EMERSON
Mandibular
symphysis
Dentary
Meckel’s
cartilage
Mentomeckelian
Angulosplenial
Fig. 1. Elements of a typical anuran mandible. Rectangle delimits
the portion in which the odontoids usually are present.
Neobatrachia
Microhylidae
Ranoidea
Allophryne ruthveni
Brachycephalidae
Bufonidae
Heleophryne
‘Leptodactylidae’*
Limnodynastinae
Pseudidae
Centrolenidae
Sooglossidae
Scaphiophryninae
Scoptanura
Myobatrachinae*
Rhinoderma
Hylidae*
Dendrobatidae
Arthroleptidae
Hemisus
‘Ranidae’*
Hyperoliidae
Rhacophoridae
Fig. 2. Phylogenetic hypothesis of relationships among neo-
batrachian taxa (Ford & Cannatella, 1993) in which families
containing species with odontoids are marked with an asterisk.
llanensis,Leptodactylus chaquensis,Leptodactylus
labyrinthicus and Leptodactylus laticeps (Leptodactyl-
idae). Information on Adelotus brevis was taken from the
literature. Examined specimens are catalogued in the
Fig. 3. Internal views of the anterior portion of frog lower jaws: (a) right mandible of Aubria subsigillata (RFL 212) with an odontoid
projection from the dentary; (b) right mandible of Hoplobatrachus occipitalis (RFL 348) with a laminar odontoid from the dentary;
(c) right mandible of Conraua crassipes (RFL 246); (d) pseudo-odontoid of Leptodactylus laticeps (FML 3982), a mound of connective
tissue at the mandibular symphysis protrudes between the two mentomeckelian bones; (e) paired odontoids of Chacophrys pierotti (FML
1019), immediately lateral to the mandibular symphysis; (f) right mandible of Ceratophrys cranwelli (FML 5471); (g) paired odontoids of
juvenile Lepidobatrachus asper (FML 5479), vestiges of Meckel’s cartilages are still present; (h) right mandible of adult Lepidobatrachus
asper (FML 549); (i) right mandible of Lepidobatrachus laevis (FML 620); (j) right mandible of Lepidobatrachus llanensis (FML 420).
ang, angulosplenial; den, dentary; Mc, Meckel’s cartilage; mmk, mentomeckelian; o, odontoid; po, pseudo-odontoid. Scale bars =1mm.
herpetological collections of Instituto de Herpetolog´
ıa,
Fundaci´
on Miguel Lillo (FML), in Tucum´
an (Argentina),
Museo de Ciencias Naturales (MCN and RFL),
Universidad Nacional de Salta, in Salta (Argentina); The
Field Museum of Natural History (FMNH) in Chicago;
The American Museum of Natural History (AMNH) New
Yo rk City, and The Museum of Comparative Zoology
(MCZ) in Cambridge (see Appendix).
The morphology of the odontoids was studied in both
dry skeletons and alcohol-preserved specimens. For some
species, whole mounts of larvae and adults were cleared
and differentially stained for cartilage and bone using
alcian blue and alizarin red (Wassersug, 1976; Hanken
&Wassersug, 1981). The normal table of Gosner (1960)
was used for staging larvae. Illustrations were prepared
with the aid of a stereo microscope with camera lucida
and/or photographed.
Intra- and interspecific quantitative differences in
odontoids were studied by measuring snout–vent lengths
(SVL) and fang lengths in preserved specimens. Fang
length is defined as the perpendicular distance between the
ventral border of the mandible and the tip of the odontoid
process (after Emerson, 1994). It was necessary to include
jaw depth, as well as odontoid length because preliminary
studies indicated that measurements of fang length alone
lacked repeatability. All measurements were converted to
log base10 and then graphed as a series of bivariate plots to
examine whether or not there is sexual dimorphism in the
sizes of the odontoids. Regression equations describing
the quantitative relationship between log fang length and
log SVL were calculated using JMP 3.1. ANCOVA was
used to test for significant effects of size and sex on fang
length. For interspecific comparisons, mean fang length
and mean SVL for males are used to represent each
species.
Aphylogeny for the fanged frogs and relatives in
the subfamily Raninae was constructed from molecular
data of the 12S and 16S portions of the mitochondrial
genome (sequences from GenBank) using PAUP
4.0b8*. Taxa included in the analysis were Aubria
subsigillata,Ceratobatrachus guentheri,Hoplobatrachus
occipitalis,Limnonectes kuhlii,Limnonectes leporina,
Nyctibatrachus major,Occidozyga laevis,Platymantis
vitiensis,Pyxicephalus adspersus,Rana cancrivora,
Rana corrugata,Rana limnocharis,Rana temporaria
and Sphaerotheca pluvialis.ForAubria subsigillata,
Ceratobatrachus guentheri,Platymantis vitiensis and
Pyxicephalus adspersus only 16S data were available. In
these taxa the 12S portion of the genome was scored as
Parallelism and convergence in anuran fangs 43
(a)
den
o
ang
mmk (b)
den
o
ang
mmk
(c)
den
o
ang
mmk (d)
den
po
ang
mmk
(e)
den
o
ang
mmk
(f)
den
o
ang
mmk
(g)
den o
ang
mmk
(h)
den
o
ang
mmk
(i)
den
o
ang
mmk
(j)
den
o
ang
mmk
Mc
Mc
Fig. 3. For caption see facing page.
44 M. FABREZI AND S. B. EMERSON
(a)
o
mp
(b)
o
(c)
o
den
Mc
(d)
den
ir
mmk
(e) (f)
mmk
(g)
cm
o
ang
ir
(h)
den
o
den
den
oo
mmkmmk
Mc
Mc
ang
ir
den
ms
o
se
ang
Fig. 4. For caption see facing page.
Parallelism and convergence in anuran fangs 45
missing. Nesomantis thomasseti (Sooglossidae) was used
as the outgroup in the analysis (Ford & Cannatella, 1993).
Transitions and transversions were weighted equally.
Sequences were analysed using the heuristic search option
and 10 replicate searches with random addition of taxa
were performed. Non-parametric bootstrap analyses with
100 replicates were run to evaluate the strength of
the groupings. Fang characters were mapped on this
phylogenetic hypothesis using MacClade (Maddison &
Maddison, 1992).
RESULTS
Qualitative variation in odontoid morphology
The anuran lower jaw consists of four elements on each
side: a symphyseal bone (=mentomeckelian), and the
dermal dentary and angulosplenial that invest Meckel’s
cartilage (Fig. 1) (Trueb, 1973). The fang-like outgrowths
of the lower jaw found among frog species vary
considerably in their ontogenies, adult shapes and relative
sizes (Figs 3–5).
Some species of ranines (Brown, 1952; Bossuyt &
Milinkovitch, 2000; Emerson, Inger & Iskandar, 2000 and
references therein) have a pair of odontoids in the lower
jaw (Fig. 3). The sizes of odontoids vary interspecifically
(described below), but in all ranines examined each
odontoid develops as a laminar projection from the
dentary, somewhat lateral to the mandibular symphysis.
In A. subsigillata (Fig. 3a), C. guentheri,C. crassipes
(Fig. 3c), H. occipitalis (Fig. 3b), Limnonectes spp. (sensu
Emerson et al., 2000), P. adspersus and R. corrugata,only
the upper or dorsal edge of the dentary contributes to the
formation of the odontoids. Ontogenetically, the odontoid
processes differentiate post-metamorphically. When the
mouth is closed, each odontoid abuts the lingual surface
of the upper mandible at the level of the premaxillary–
maxillary articulation. In species of Limnonectes,
A. subsigillata,H. occipitalis and P. adspersus,the ex-
treme anterior portion of the pars palatina of the
maxilla is concave and delimits a space where the lateral
odontoids fit when the jaws are closed (Clarke, 1981).
In addition to the presence of lateral odontoids, some
fanged ranines also posses a well-developed mound of
connective tissue between the mentomeckelian bones
Fig. 4. Internal views of odontoid development in ceratophryine leptodactylids: (a) Lepidobatrachus llanensis larval stage 42 (MCN 567):
odontoid germs have differentiated on both sides of the medial process of the infrarostral cartilage; (b) Lepidobatrachus llanensis larval stage
43 (FML 4678): odontoid germs are larger and the medial process of infrarostral is beginning to reabsorb; (c) Lepidobatrachus llanensis
larval stage 45 (MCN 667): odontoid is fused with the dentary and the mentomeckelian ossification is progressing; (d) Lepidobatrachus
llanensis sub-adult (MCN 668): odontoid, dentary, and mentomeckelian form a single complex but individual elements still can be
recognized; (e) Ceratophrys cranwelli larval stage 43 (MCN 669): odontoid germs are amorphous, appearing as the medial process of
the infrarostral begins to reabsorb; (f) Ceratophrys cranwelli larval stage 44 (MCN 669): dentary and mentomeckelian ossifications have
differentiated and the odontoid is fused with the dentary; (g) Ceratophrys cranwelli larval stage 45 (MCN 669): amorphous odontoid is
fused with the mentomeckelian; (h) Ceratophrys cranwelli,recently metamorphosed specimen (MCN 005): ossification of lower jaw is
strong, limits of the odontoid, dentary, and mentomeckelian are not clear. ir, infrarostral; mp, medial process of infrarostral; se, dentary
serration; others as Fig. 3. Scale bars =1mm.
1.0
0.8
0.6
0.4
0.2
0.0
0.2
0.4
Log fang length
1.3 1.4 1.5 1.6 1.7 1.8 1.9 2.0 2.1 2.2
Log snout–vent length
Fig. 5. Relationships between log fang length and log snout–vent
length in species of male ranine frogs. Stars without labels are
species of Limnonectes.Non-capitalized names are species of the
genus Rana.Three groups delineating three sizes of relative fang
length are shown by black lines.
that sometimes stains with alcian blue. Some authors
have referred to this structure as an additional fang
(e.g. Stewart, 1967; Passmore & Carruthers, 1979;
Poynton & Broadlley, 1985). Structurally, this pseudo-
odontoid represents hypertrophied connective tissue of
the mandibular symphysis and does not include any
mandibular bone. A similar pseudo-odontoid also occurs
in species of Leptodactylus (Leptodactylidae) (Fig. 3d)
and some bufonids (M. Fabrezi, pers. obs.).
Ceratophryine leptodactylids have a pair of pointed,
robust and fully ossified odontoids, with the fangs flanking
each side of the mandibular symphysis (Fig. 3e–h).
Because the mandibular bones of these taxa are strongly
fused, it is difficult to determine the limits of each element.
It seems, however, that each odontoid is synostotically
united to dentary and mentomeckelian. When the mouth
is closed, the odontoid abuts the superficial lingual part of
the alar process of the premaxilla; the palatal shelf of the
premaxilla is absent in Ceratophryinae (Lynch, 1971).
46 M. FABREZI AND S. B. EMERSON
Tab l e 1 . Intraspecific patterns of relationships between fang length and snout–vent length (SVL)
Regression equation 95% CI
Ceratobatrachus guentheri Log fang =−1.57 + 1.04 log SVL 0.71–1.38
Pyxicephalus adspersus Log fang =−1.50 + 1.14 log SVL 0.64–1.63
Aubria subsigillata Log fang =−1.55 + 1.05 log SVL 0.87–1.22
Conraua crassipes
Male Log fang =−1.79 + 1.25 log SVL 0.10–2.4
Female Logfang=−1.49 + 1.02 log SVL 0.57–1.47
Hemiphractus fasciatus Log fang =−0.63 + 0.59 log SVL 0.33–0.86
Ceratophrys cranwelli Log fang =−1.11 + 0.92 log SVL 0.54–1.29
Lepidobatrachus llanensis Log fang =−0.22 + 0.51 log SVL 0.34–0.68
Lepidobatrachus laevis Log fang =−0.32 + 0.58 log SVL 0.21–0.92
Morphological and molecular data indicate that Cerato-
phrys,Chacophrys and Lepidobatrachus are a mono-
phyletic group (Lynch, 1971; Maxon & Ruibal, 1988).
Ontogenetically, the development of their odontoids is
similar, although there is some variation in the timing
of emergence, the shape and size of the initial odontoid
condensations, and the relationship between odontoid
size and body size at the end of metamorphosis. In
L. llanensis,they flank each side of the medial projection
of the infrarostral cartilage by larval Stage 41 (Fig. 4a).
These condensations stain positive with alizarin red.
Each odontoid lengthens and becomes sharper during
development (Fig. 4b). Differentiating dentary tissue
fuses with the odontoid condensation as it ossifies
(Fig. 4c). By the end of metamorphosis, the dentary and
the mentomeckelian ossifications are fused completely.
In contrast, the odontoid is not fully incorporated into the
angulosplenial until later in ontogeny in the juvenile stages
(Fig. 4d).
In Ceratophrys cranwelli,the odontoid condensations
are present and stain positive for bone in larval Stage 43
(Fig. 4e). They remain as amorphous ossifications that
grow slowly while dentary ossification proceeds (Fig. 4f–
g). By the end of metamorphosis, the odontoid and dentary
are fused. After metamorphosis, the odontoid fuses with
the mentomeckelian, but a suture is visible (Fig. 4h).
In A. brevis (family Myobatrachidae) the odontoid is
derived from both the mentomeckelian and the dentary
(L. Trueb, pers. comm.). There is a diastema in the
maxillary tooth row; presumably this accommodates the
odontoid when the jaws are closed (Lynch, 1971).
In species of Hemiphractus (family Hylidae), the odon-
toid is derived from the dentary and is located adjacent to
the mandibular symphysis (Trueb, 1974; Shaw, 1989) in a
position similar to that of the odontoids of ceratophryine
leptodactylids. In contrast to the latter, however, only
the odontoids and the dentary of Hemiphractus are
synostotically united (Shaw, 1989) as Hemiphractus
lacks mentomeckelians (Trueb, 1974). There is a medial
diastema in the premaxillary teeth where the odontoids
fit when the jaws are closed. In Phyllodytes (family
Hylidae), the fang is located immediately lateral to
the mandibular symphysis (Miranda-Ribeiro, 1926) as
well, but apparently it is derived entirely from the
mentomeckelian (L. Trueb, pers. comm.).
Quantitative variation in the morphology
of the odontoids
Intraspecific plots of fang length against SVL for
the various species reveal interesting and different
patterns. In two species of ceratophryine leptodactylids,
Lepidobatrachus laevis and Leptobatrachus llanensis,and
in the hylid Hemiphractus fasciatus,fang length scales
with a significant negative allometry with respect to
SVL (Table 1). Females are larger than males in these
species, but both sexes are described by a single regression
equation. As a result of the negative allometry in the
fang length to SVL relationship in these species, recently
metamorphosed and juvenile frogs have relatively larger
fangs than older, larger adults. In C. cranwelli,fang length
scales isometrically with SVL. The males and females are
described by a single regression equation and there is no
difference in relative fang length between juveniles and
adults (Table 1).
In the myobatrachid A. brevis,fang size scales with a
strong positive allometry with SVL in males (Katsikaros
&Shine, 1997). In contrast, the females have almost no
fangs (Katsikaros & Shine, 1997). Males are larger than
females and therefore have relatively and absolutely larger
fangs than females.
Among the ranine species, there are different intra-
specific patterns of relationship between fang length
and SVL. In A. subsigillata,C. guentheri,P. adspersus
and H. occipitalis,there are isometric relationships
between fang size and snout–vent size (Table 1;
Emerson, 1994). Females are larger than males in Aubria,
Hoplobatrachus and Ceratobatrachus,butthere is no
significant difference between sexes in relative fang length
at the same SVL. Males and females are described by a
single regression equation (Table 1; Emerson, 1994). In
P. adspersus,males are larger than females, but, again,
the sexes do not differ significantly in relative fang
length at the same SVL (Table 1) and males and
females are described by a single regression equation.
Only six individuals of R. corrugata were available for
measurement; for these males and females of the same
SVL, males had significantly larger fangs than females
(P<0.02). In C. crassipes,ANCOVA indicates a
significant effect of both size and sex on fang length
(SVL, F-ratio =3.57, P<0.0001; sex, F-ratio =23.01,
Parallelism and convergence in anuran fangs 47
Nesomantis thomasseti
Nyctibatrachus major
Rana temporaria
Rana limnocharis 2
Rana limnocharis 1
Rana cancrivora
Hoplobatrachus occipitalis
Limnonectes kuhlii
Occidozyga laevis
Pyxicephalus adspersus
Aubria subsigillata
Sphaerotheca pluvialis
Platymantis vitiensis
Ceratobatrachus guentheri
Limnonectes leporina
Rana corrugata
Nesomantis thomasseti
Nyctibatrachus major
Rana temporaria
Rana limnocharis 1
Rana limnocharis 2
Rana cancrivora
Hoplobatrachus occipitalis
Limnonectes kuhlii
Occidozyga laevis
Pyxicephalus adspersus
Aubria subsigillata
Sphaerotheca pluvialis
Platymantis vitiensis
Ceratobatrachus guentheri
Limnonectes leporina
Rana corrugata
Fig. 6. Tw oequally parsimonious hypotheses of phylogenetic relationships among selected species of ranine frogs. Numbers without
boxes are bootstrap values. Boxed numbers and grey shades represent fang character states: 0 (white), no fangs; 1 (light grey), small fangs;
2(medium grey), intermediate fang size; 3 (black), large fangs. Character state is ambiguous where hatching or multiple numbers appear
in a box. Relative fang size is defined in Fig. 5.
P<0.0004). In fanged species of Limnonectes,both males
and females have well-developed odontoids, but there
are marked differences between males and females in
relative fang size (Emerson, 1994). The males of most
species show a strong positive allometry to the relationship
between fang size and SVL (Emerson, 1994), whereas
the relationship between fang size and SVL tends to be
isometric in females (Emerson, 1994).
Interspecifically, the fang length of males in ranine
species varies across a wide range of body sizes. In
Fig. 5, at least three groups can be identified on the basis
of a species morphocline in relative fang length. The
male fanged frogs of P. adspersus,R. corrugata and the
genus Limnonectes have the largest relative fang lengths
(Group 3, Fig. 5). Aubria subsigillata,H. occipitalis,
R. rugulosa,N. major and C. crassipes have intermediate
relative fang lengths (Group 2, Fig. 5). Ceratobatrachus
guentheri,R. hexadactyla,R. tigrina,R. limnocharis,
R. cancrivora and R. cyanophlyctis have the smallest
relative fang lengths (Group 1, Fig. 5). In these latter
taxa, the bumps on the dentary often are so small that they
can be seen only in skeletal preparations of the mandible.
Occidozyga laevis,O. lima,P. anchietae,P. vitiensis,
P. guppyi and S. pluvialis lack fangs.
To understand the pattern of fang evolution in ranines,
the three categories of relative odontoid size (taken from
the log plot of fang size and SVL) were mapped on the
two equally parsimonious phylogenetic hypotheses of
ranine relationships generated from the molecular data set
(Fig. 6). Even with 332 parsimony-informative characters,
the phylogenetic relationships are not well resolved
(Fig. 6). As a consequence, these hypotheses must be
considered very preliminary. None the less, from the
mapping exercise, it seems that fangs evolved at least
three and possibly as many as five times in ranine frogs
(Fig. 6). Furthermore, it does not seem that the (relatively)
large-fanged species necessarily evolved from species that
had smaller fangs or bumps on the dentary.
DISCUSSION
Often parallelism and convergence are distinguished by
whether the same (parallelism) or different (convergence)
developmental pathways are involved in the independent
formation of the similar phenotypes (Wake, 1991; Hodin,
2000). Based on these definitions, independent evolution
of similar structures in more closely related species
may be more likely to be the result of parallelism than
convergence. More closely related species share a more
recent common ancestor and (presumably) would also be
more likely to have common developmental pathways
(Hodin, 2000 and references therein). In contrast,
similarity of structure in distantly related species would be
expected to be the result of convergence as presumably the
structures in these species would be more likely to have
arisen by different developmental pathways (Hodin, 2000
and references therein). Comparison of the ontogenetic
development of fangs in anurans supports this distinction.
The multiple, independent evolution of fangs within the
ranines always involves the same ontogenetic pathway. In
all ranines, the fangs develop through allometric growth of
aportion of the dentary after metamorphosis (Fig. 3). This
pattern is a classic example of parallelism. In contrast,
48 M. FABREZI AND S. B. EMERSON
Tab l e 2 . Comparisons of morphological and behavioural features, and diet across fanged frogs. Data were taken from Balinsky & Balinsky,
1954; Brown, 1952; Channing et al., 1994; Duellman, 1978; Fabrezi, 2001; Hanken, 1993; Hughes, 1979; Katsikaros & Shine, 1997;
Knoepffler, 1965; Lynch, 1971; Noble, 1924; Orlov, 1997; Perret, 1994; Reig & Limeses, 1963; Shaw, 1989; Sheil et al., 200l; Wild, 1999
Hyper- Aggressive
Relative fang ossification biting Male–male
Taxon Body size size skull behaviour combat Diet Teeth
Chacophrys Female >male ? Yes ? ? Relatively large Monocuspid/
vertebrate prey non-pedicellate
Ceratophrys Female >male Female =male Yes Yes No Relatively large Monocuspid/
vertebrate prey non-pedicellate
Lepidobatrachus Female >male Female =male Yes Yes No Relatively large Monocuspid/
vertebrate prey non-pedicellate
Hemiphractus Female >male Female =male Yes Yes ? Relatively large Monocuspid/
vertebrate prey pedicellate
Phyllodytes Fema le >male Male >female No No Yes ? ?
Adelotus Male >female Male >female No No Yes Occasional Bicuspid/
vertebrates pedicellate
Limnonectes Male >female Male >female No No Yes Occasional Bicuspid/
vertebrates pedicellate
Conraua Female >male Male >female No No ? Occasional Bicuspid/
vertebrates pedicellate
Hoplobatrachus Female >male Female =male No No ? Arthropods, frogs Bicuspid/
pedicellate
Aubria Fema le >male Female =male Yes Yes No Relatively large Monocuspid/
vertebrate prey pedicellate
Pyxicephalus Male >female Female =male Yes Yes Yes Relatively large Monocuspid/
vertebrate prey non-pedicellate
Rana corrugata Female >male Male >female No ? ? ? ?
Ceratobatrachus Female >male Female =male Yes ? ? ? ?
the evolution of fangs in species in different families
involves different ontogenetic pathways. In ceratophryine
leptodactylids, fangs develop from independent odontoid
tissue condensations that form and fuse to portions of
the mandibular bones near metamorphosis (Fig. 4). This
process differs from that observed in either ranine frogs
or the fanged hylid species of the genus Hemiphractus
(Shaw, 1989). Thus, the occurrence of fangs in different
anuran families is an example of convergent evolution.
One of the most interesting aspects of the repeated,
independent evolution of frog fangs is that they seem to
be the result of more than one type of selection pressure.
Comparisons of morphology, behaviour and diet across
frog taxa with odontoids (Table 2) reveal broad patterns
which suggest that both sexual and natural selection may
have been involved in the evolution of fangs.
In some species, the presence of fangs seems to be
correlated with dietary specialization and to be the result
of natural selection. These species of fanged frogs eat
relatively large prey compared to their fangless relatives.
In H. occipitalis and A. subsigillata,frogs are a common
part of the diet (Noble, 1924; Hughes, 1979; Perret, 1994;
Table2). The ceratophryine leptodactylids, species of
Hemiphractus,and P. adspersus also specialize in eating
relatively large vertebrate prey including frogs, small
mammals, lizards and birds (Loveridge, 1950; Duellman,
1978; Cei, 1981; Hanken, 1993; Duellman & Lizana,
1994). These species are characterized by aggressive
biting behaviour, hyperossification of the cranium and
monocuspid teeth (Table 2). Additionally, P. adspersus
and the ceratophryine leptodactylids have non-pedicellate
teeth, a rare condition among anurans (Smirnov &
Vasil’eva, 1995; Fabrezi, 2001). (In these species, the
absence of pedicellate teeth is associated with a rapid,
intense calcification of the tooth germ that suppresses
the typical zone of weakness found in pedicellate teeth;
Smirnov & Vasil’eva, 1995; Fabrezi, 2001.)
In contrast, there is no significant effect of fang size
on relative prey size in the fanged species of Limnonectes
and A. brevis (Emerson & Voris, 1991; Emerson, 1994;
Katsikaros & Shine, 1997). These species do not seem
to specialize in eating large vertebrates, although they
do occur occasionally in their diet. Aggressive biting
behaviour and non-pedicellate teeth have not been
reported for any of these species.
Fanged frog species lacking a diet of relatively large
prey are generally sexually dimorphic in relative fang
sizes, suggesting that in these taxa, sexual selection
may have been important in odontoid evolution. In
P. adspersus,P. luteolus,A. brevis and species of
Limnonectes,males are larger than females and all taxa
except P. adspersus have marked sexual dimorphism
in relative fang sizes. Furthermore, in P. adspersus,
P. luteolus,A. brevis and species of Limnonectes,enlarged
fangs are used in male–male combat (Balinsky &
Balinsky, 1954; Weygoldt, 1981; Orlov, 1997; Katsikaros
&Shine, 1997; Tsuji & Kuang, 2000). In contrast, male
combat has not been reported for the fanged species
of Chacophrys,Ceratophrys or Lepidobatrachus that
specialize in relatively large prey. Furthermore, none of
Parallelism and convergence in anuran fangs 49
these species exhibits a sexual dimorphism in relative fang
sizes and males are smaller than females.
Pyxicephalus adspersus is unique among the taxa
with fangs in that it has both male–male combat and
aspecialized diet of relatively large vertebrate prey
(Channing, Perez & Passmore, 1994). Furthermore,
Pyxicephalus exhibits aggressive biting behaviour and
has hyperossified cranial bones. There is no significant
difference in relative fang sizes between males and
females at the same SVL but, commonly, males are larger
than females. Uniquely, the males of this species show
adaptive male parental care, which includes attacking
predators of their larvae including birds and other frogs
(Cook, Ferguson & Telford, 2001).
Pertinent details of breeding behaviour and/or diet are
not known for R. corrugata,N. major,C. crassipes and
C.guentheri,but some morphological data are available
(described in Results). Females are larger than males and
there is no sexual dimorphism in relative fang size in
species of Hemiphractus,N. major and C. guentheri;this
suggests that the presence of fangs in these species may be
related to diet specialization. In contrast, in C. crassipes
and R. corrugata,there is sexual dimorphism in fang size
with males having relatively larger fangs. These findings
suggest that fangs in these species may be related to
intrasexual competition.
Fangs in frogs seem to solve a common problem.
They are a means of handling relatively large, resistant
prey or foe. At the same time, fangs have not evolved
under a single selection regime. An interesting question
is whether natural and sexual selection left different
‘signatures’ on frog fang morphology. This might occur
because sexually dimorphic features are thought to be
under especially strong selection (West-Eberhard, 1983).
If this were true, one might predict that the fangs would
be relatively larger in species with male–male combat and
sexual selection than in species in which the fangs evolved
through natural selection to take relatively larger prey. In
fact, this seems to be the situation, whether the fangs are
the result of parallel or convergent evolution. Within the
ranine frogs, species of Limnonectes have the relatively
largest fang lengths (Fig. 4). This is a group characterized
by a history of sexual selection (Emerson, 1994; 2001).
Among families, the fangs of A. brevis,P. auratus and
the species of Limnonectes are relatively larger than those
of ceratophryine leptodactylids, species of Hemiphractus,
and C. guentheri (Emerson, 1994; Katsikaros & Shine,
1997; pers. obs). This first group of species are those
whose fangs seem to have evolved through sexual
selection. The presence of fangs, sexual dimorphism in
fang size and fang use in male–male competition are all
derived characters for the various taxa (Weygoldt, 1981;
Emerson, 1994; Katsikaros & Shine, 1997).
In conclusion, enlarged fangs have evolved indepen-
dently through both parallelism and convergence in anuran
amphibians. Depending on the species, these enlarged
odontoids can be the result of either sexual or natural
selection. Those fangs that evolved under sexual selection
seem to be relatively larger than those resulting from
natural selection.
Acknowledgements
The authors thank the various museums and their staff
for access to specimens. African specimens from the
personal collection of Dr R. F. Laurent were donated
to M. Fabrezi and deposited in the Museo de Ciencias
Naturales of Universidad Nacional de Salta. L. Trueb
contributed key observations on the osteology of Adelotus
and Phyllodytes and critical revision. Kurt Schwenk read
and made helpful comments on an earlier version of
the manuscript. Alfredo Albino drew the illustrations in
Fig. 3. This research has been supported in part by Consejo
Nacional de Investigaciones Cientificas y Tecnicas and the
Universidad Nacional de Salta (to MF) and the National
Science Foundation and the University of Utah (to SBE).
REFERENCES
Balinsky, B. & Balinsky, J. (1954). On the breeding habits of the
South African bullfrog, Pyxicephalus adspersus. S. Afr. J. Sci.
51:55–58.
Bock, W. & Von Wahlert, G. (1965). Adaptation and the form–
function complex. Evolution 19:269–299.
Bossuyt, F. & Milinkovitch, M. C. (2000). Convergent adaptive
radiation in Madagascan and Asian ranid frogs reveal covariation
between larval and adult traits. PNAS 97:6585–6590.
Brown, W. (1952). The amphibians of the Solomon Islands. Bull.
Mus. Comp. Zool. 107:1–64.
Cei, J. M. (1981). Amphibians of Argentina. Mon. Zool. Ital.
(Monogr.) (NS) 2:1–609.
Channing, A., Perez, L. & Passmore, N. (1994). Status, vocalization
and breeding biology of two species of African bullfrogs
(Ranidae: Pyxicephalus). J. Zool. (Lond.) 234:141–148.
Clarke, B. (1981). Comparative osteology and evolutionary
relationships in the African Raninae (Anura: Ranidae). Monitore
Zool. Ital. Suppl. (NS) 15:285–331.
Cook, C., Ferguson, J. & Telford, S. (2001). Adaptive parental care
in the giant bullfrog, Pyxicephalus adspersus. J. Herpetol. 35:
310–315.
Dawkins, R. (1987). The blind watchmaker. New York: W. W.
Norton.
Duellman, W. (1978). The biology of an equatorial herpetofauna in
Amazonian Ecuador. Univ. Kans. Mus. nat. Hist. Misc. Publ. 65:
1–352.
Duellman, W. & Lizana, M. (1994). Biology of a sit-and-
wait predator, the leptodactylid frog Ceratophrys cornuta.
Herpetologica 50:51–64.
Duellman, W. & Trueb, L. (1986). Biology of amphibians.
New York: McGraw-Hill.
Emerson, S. (1994). Testing pattern predictions of sexual selection:
a frog example. Am. Nat. 143:848–869.
Emerson, S. (2001). A macroevolutionary study of historical
contingency in the fanged frogs of Southeast Asia. Biol. J. Linn.
Soc. 73:139–151
Emerson, S., Inger, R. & Iskandar, D. (2000). Molecular systematics
and biogeography of the fanged frogs of Southeast Asia. Mol.
Phylogenet. Evol. 16:131–142.
Emerson, S. & Voris, H. (1991). Competing explanations for sexual
dimorphism in a voiceless Bornean frog. Funct. Ecol. 6:654–
660.
Fabrezi, M. (2001). Variaci´
on morfol´
ogica de la dentici´
on en
Anuros. Cuad. Herpetol. 15:17–28.
Ford, L. & Cannatella, D. (1993). The major clades of frogs.
Herpetol. Monogr. 7:94–117.
50 M. FABREZI AND S. B. EMERSON
Gosner, K. (1960). A simplified table for staging anuran embryos
and larvae with notes on identifiction. Herpetologica 16:183–
190.
Hanken, J. (1993). Model systems vs outgroups: alternative
approaches to the study of head development and evolution. Am.
Zool. 33:448–456.
Hanken, J. & Wassersug, R. (1981). The visible skeleton. Funct.
Photogr. 16:22–26.
Hodin, J. (2000). Plasticity and constraints in development and
evolution. J. exp. Zool. Mol. Dev. Evol. 288:1–20.
Hughes, B. (1979). Feeding habits of the frog Aubria subsigillata
in Ghana. Bull. Inst. Fondam. Afr. Noire Ser. A Sci. Nat. 41:
654–663.
Katsikaros, K. & Shine, R. (1997). Sexual dimorphism in the
tusked frog, Adelotus brevis (Anura: Myobatrachidae): the roles
of natural and sexual selection. Biol. J. Linn. Soc. 60:39–51.
Knoepffler, L.-Ph. (1965). Le comportement fouisseur de Conraua
crassipes (Amphibien anoure) et son mode de chasse. Biol.
Gabonica 1:239–245.
Loveridge, A. (1950). History and habits of the East African
bullfrog. J. Ea st Afr. Nat. Hist. Soc. 19:253–257.
Lynch, J. D. (1971). Evolutionary relationships, osteology, and
zoogeography of leptodactyloid frogs. Univ. Kans. Mus. nat. Hist.
Misc. Publ. 53:1–238.
Maddison, W. & Maddison, D. (1992). MacClade.Sunderland:
Sinauer.
Maxon, L. R. & Ruibal, R. (1988). Relationships of frogs in the
leptodactylid subfamily Ceratophryinae. J. Herpetol. 22:228–
231.
Miranda-Ribeiro, A. (1926). Notas para servirem ao estudo dos
Gymnobatrachios (Anura) Brasileiros. Arch. Mus. Nac. Rio de
Janeiro 27:1–227.
Noble, G. (1924). Contributions of the Belgian Congo based on the
collection of the American Museum Congo Expedition, 1909–
1915. Bull. Am. Mus. nat. Hist. 49:147–347.
Noble, G. (1931). The biology of the amphibia. New York; Dover.
Orlov, N. (1997). Breeding behaviour and nest construction in
aVietnam frog related to Rana blythii. Copeia 1997:464–
465.
Passmore, N. I. & Carruthers, V. C. (1979). South African frogs.
Johannesburg: Witwatersrand University Press.
Perret, J. (1994). Revision of the genus Aubria Boulenger 1917
(Amphibia Ranidae) with the description of a new species. Trop.
Zool. 7:255–269.
Poynton, J. C. & Broadley, D. G. (1985). Amphibia Zambesiaca 2.
Ranidae. Ann. Natal. Mus. 27:115–181.
Reig, O. A. & Limeses, C. E. (1963). Un nuevo g´
enero de anuros
ceratofr´
ınidos del distrito Chaque˜
no. Physyis 24:113–128.
Shaw, J. P. (1989). Observations on the polyphiodont dentition of
Hemiphractus proboscideus (Anura: Hylidae). J. Zool. (Lond.)
217:499–510.
Sheil, C. A., Mendelson, J. R. III & Da Silva, H. R. (2001).
Phylogenetic relationships of the species of neotropical horned
frogs, genus Hemiphractus (Anura: Hylidae, Hemiphractinae);
based on evidence from morphology. Herpetologica 57:203–
214.
Smirnov, S. V. & Vasil’eva, A. B. (1995). Anuran dentition:
development and evolution. Russian J. Herpetol. 2:120–128.
Stewart, M. M. (1967). Amphibians of Malawi. Albany: State
University of New York Press.
Trueb, L. (1973). Bones, frogs, and evolution. In Evolutionary
biology of the anurans: contemporary research on major
problems: 65–132. Vial, J. L. (Ed.). Columbia: University of
Missouri Press.
Trueb, L. (1974). Systematic relationships of Neotropical horned
frogs genus Hemiphractus (Anura: Hylidae). Occas. Pap. Mus.
nat. Hist. Univ. Kans. 29:1–60.
Tsuji, H. & Kuang, Y. (2000). The reproductive ecology of female
Rana (Limnonectes) kuhlii,afanged frog of Taiwan, with
particular emphasis on multiple clutches. Herpetologica 56:153–
165.
Wake,D.(1991). Homoplasy: the result of natural selection or
evidence of design limitations. Am. Nat. 138:543–567.
Wassersug, R. J. (1976). A procedure for differential staining of
cartilage and bone in whole formalin-fixed vertebrates. Stain
Technol. 51:131–134.
West-Eberhard, M. J. (1983). Sexual selection, social competition,
and speciation. Q. Rev. Biol. 58:155–183.
Weygoldt, P. (1981). Beobachtungen zur fortpflansungs biologie
von Phyllodytes luteolus (Wied, 1824) in terrarium. Salamandra
17:1–11.
Wild, E. R. (1999). Description of the chondrocranium and
osteogenesis of the chacoan burrowing frog, Chacophrys pierotti
(Anura: Leptodactylidae). J. Morphol. 242:229–246.
APPENDIX. SPECIMENS EXAMINED
Museum codes
ACZ: The Museum of Comparative Zoology, Cambridge.
AMNH: The American Museum of Natural History, New York City.
FML: Fundaci´
on Miguel Lillo, Tucum´
an, Argentina.
FMNH: The Field Museum of Natural History, Chicago.
MCN: Museo de Ciencias Naturales, Universidad Nacional de Salta,
Salta, Argentina.
RFL: Raymond Ferdinand Laurent, personal collection.
Ranidae
Aubria subsigillata: MCZ 21790–91, 557, 26944, 2963; AMNH
75121, 11905, 12922–26; FMNH 190815, 168848; FML 3154
(five specimens); RFL 212, 209 (two specimens).
Ceratobatrachus guentheri: FMNH 13717, 13743, 13745–46,
13855, 25897, 44528, 44786–87, 44789, 44791, 44794, 44799,
44912.
Conraua alleni: AMNH 140823, 140825–29, 83301–03.
Conraua crassipes: MCZ 5580–81, 3458, 13213–14, 23266,
23247–48; AMNH 11908–10, 23101, 23105, 63549–51; FML
3068 (five specimens); RFL 246 (two specimens).
Conraua goliath: FMNH 15980; MCZ 15738, 85228.
Hoplobatrachus occipitalis: FMNH 20830 (46 specimens),
22184, 160886, 160888–90, 160894, 160899; FML 1192 (10
specimens); RFL 348 (two specimens).
Nyctibatrachus major: FMNH 218202, 218204, 218206, 218209,
21815, 21819, 218223–24, 218226, 218228, 218231–32,
218234, 218237, 218766.
Occidozyga laevis: FMNH 24113, 234899–904, 234907–08,
234910, 234914–16, 234918–20.
Platymantis guppyi: FMNH 44584.
Platymantis vitiensis: FMNH 23000.
Ptychadena anchietae: MCZ 36241–44, 36246, 36248, 36250,
36252–53, 36257.
Ptychadena mascariensis: FMNH 175773.
Ptychadena mossambicus: MCZ 28622.
Pyxicephalus adspersus: FMNH 17153, 232743, 215535, 17148,
20745; MCZ 7265, 10368, 10788, 10826, 16483–84, 21359,
21362, 25374–75; FML 2050.
Rana cancrivora: FMNH 131485, 143433, 143436, 143439,
143451–52, 143457–59, 143462, 143468–69, 143497, 143500–
03, 143506, 143510, 143515–16, 143527, 143534, 200965,
200972–74, 200977, 200981.
Rana corrugata: FMNH 81229; AMNH 74244–45, 77474–78.
Parallelism and convergence in anuran fangs 51
Rana cyanophylyctis: FMNH 166716, 167178–79, 16790, 167207–
09, 167213–14, 167219–20, 167236, 167240, 167244, 167248,
167265, 167353, 167356–57, 167359, 167362, 167364, 167371–
72, 167323–24, 167333.
Rana hexadactyla: MCZ 31517–21.
Rana limnocharis: FMNH 196141, 1716, 50161, 50167–68, 50172,
50174–77, 50179, 50181, 50187, 50193, 50198, 50204–06,
50208, 51124, 51132, 51134, 51137, 51141, 51146–47, 51150,
51152, 51157, 51166–67, 51173, 51182.
Rana rugulosa: MCZ 13241–42; FMNH 196212, 8636, 7762,
24506, 21926, 13099, 176321.
Rana tigrina: MCZ 31548–49, 132420–21.
Sphaerotheca pluvialis: MCZ 412, 1275; FMNH 211889.
Sphaerotheca cryptotis: MCZ 24014–15, 107074.
Hylidae
Hemiphractus fasciatus: AMNH 124113–20, 92668, 98078, 98363,
107955–56, 108288.
Hemiphractus proboscideus: MCZ 90345, 90347, 91463, 92274,
97772, 17937.
Phyllodytes auratus: FMNH 218984, MCZ 15611–13, 80487–88.
Leptodactylidae
Ceratophrys cranwelli: FMNH 69164–66, 69075; FML 4573–4,
4534 (seven tadpoles between larval stages 40 and 46), 4777,
5471–2, 8961–70; MCN 005 (two specimens), 188, 260 (six
specimens), 669 (12 specimens between larval stages 40 and 46).
Chacophrys pierotti: FML 9046–49, 1094 (six specimens), 428
(two specimens), 1019 (four specimens), 9013.
Lepidobatrachus asper: FML 1386 (three specimens), 5669, 5470,
5479.
Lepidobatrachus laevis: FML 8102 4914 (three specimens), 1090,
620; MCN 109, 666, 695, 696 (three specimens), 663 (eight
tadpoles between larval stages 39 and 42).
Lepidobatrachus llanensis: FML 4856 (six specimens), 1016,
5220–21, 4678 (three tadpoles at larval stages 41, 42, 43);
MCN 667 (three specimens), 667, 081, 567 (12 tadpoles between
larval stages 38 and 42), 665 (six tadpoles at larval stages 41–
43).
Leptodactylus chaquensis: FML 4406; MCN 039 (two specimens),
082, 124, 142 (four specimens), 261 (two specimens), 449, 477.
Leptodactylus labyrinthicus: FML 0829 (four specimens).
Leptodactylus laticeps: FML 0269, 02181 (four specimens), 03645
(two specimens); MCN 104.
... There remains a need to verify that the mandibular dentition of G. guentheri is composed of true teeth. Alternatively, these structures may be bony odontoid serrations (i.e., pseudoteeth) as seen in some other anurans, such as the mandibular odontoids found in Cornufer guentheri and species of Hemiphractus (Shaw 1989;Fabrezi and Emerson 2003;Paluh et al. 2021), which would indicate that they do not represent a "re-evolved" trait. If true mandibular teeth are present, they may be degraded or simplified, such as through the loss of enamel or a bicuspid shape, due to deterioration of the odontogenic pathway. ...
... The shape, hyperossification, and articulation of the skull in G. guentheri are similar to other carnivorous frog species that specialize on eating large vertebrate prey, such as Ceratophrys, Pyxicephalus, Cornufer guentheri, and Hemiphractus (Paluh et al. 2020). These frogs are typically sit-and-wait predators that independently evolved bony odontoid fangs and serrations on the lower jaw that are thought to improve prey capture but are not true teeth (Fabrezi and Emerson 2003). Wiens (2011) speculated that the repeated evolution of odontoid fangs in these anurans suggests that selection can favor tooth-like structures on the mandible, but true teeth have not reevolved in any of these taxa due to an unspecified developmental constraint. ...
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... Barej et al. (2010a) and Gvoždík & Kopecký (2011) also interpreted these wounds and scars as the results of territorial behaviour. While biting is a known anuran behaviour, especially in fanged frogs (Balinsky & Balinsky 1954, Katiskaros & Shine 1997, Orlov 1997, Tsuji & Matsui 2002, Fabrezi & Emerson 2003, severe injuries are scarce (Wells 2007) even though they do occur. In several gladiator frogs (Boana spp.), severe injuries and even fatalities due to the usage of the sharp prepollical spines during fighting have been reported (Kluge 1981, Martins et al. 1998. ...
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... In fact, studies of stomach content and foraging habits of bufonids in natural environment have suggested that many species are myrmecophagous or ant specialists (Toft 1980;Flowers and Graves 1995;da Rosa et al. 2002;Isacch and Barg 2002;Ferreira and Teixeira 2009), with some of the larger species such as R. marina and Incilius alvarius expanding to a generalist diet that sometimes includes small vertebrates (Pizzatto et al. 2012). In expanding to a broader diet, Incilius alvarius has even evolved neopalatine odontoids to make up for the lack of teeth (Mendelson and Pramuk 1998), reminiscent of mandibular odontoids in nonbufonid frogs that prey on large prey items (Fabrezi and Emerson 2006). That said, it is interesting to note that even in a species as large as R. marina, ants and beetles dominate their diet in certain habitats that are undisturbed by humans (Zug and Zug 1979). ...
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Synopsis Extant anurans (frogs and toads) exhibit reduced dentition, ranging from a lack of mandibular teeth to complete edentulation, as observed in the true toads of the family Bufonidae. The evolutionary time line of these reductions remains vague due to a poor fossil record. Previous studies have demonstrated an association between the lack of teeth in edentulous vertebrates and the pseudogenization of the major tooth enamel gene amelogenin (AMEL) through accumulation of deleterious mutations and the disruption of its coding sequence. In this study, we have harnessed the pseudogenization of AMEL as a molecular dating tool to correlate loss of dentition with genomic mutation patterns during the rise of the family Bufonidae. Specifically, we have utilized AMEL pseudogenes in three members of the family as a tool to estimate the putative date of edentulation in true toads. Comparison of AMEL sequences from Rhinella marina, Bufo gargarizans and Bufo bufo, with nine extant, dentulous frogs, revealed mutations confirming AMEL inactivation in Bufonidae. AMEL pseudogenes in modern bufonids also exhibited remarkably high 86–93% sequence identity among each other, with only a slight increase in substitution rate and relaxation of selective pressure, in comparison with functional copies in other anurans. Moreover, using selection intensity estimates and synonymous substitution rates, analysis of functional and pseudogenized AMEL resulted in an estimated inactivation window of 46–60 million years ago in the lineage leading to modern true toads, a time line that coincides with the rise of the family Bufonidae.
... These taxa may have converged on a skull shape that enables them to withstand the high forces encountered when feeding on large, hard prey. Several of the hyperossified vertebrate predators with the most extreme skull shapes also possess odontoid fangs on the lower jaw [ Fig. 2C; and sometimes on the palate (47)], which are tooth-like structures that enable the infliction of a bite-like wound and are thought to evolve in species that specialize on large prey (48). Odontoid fangs have also evolved in frogs that use male−male combat (e.g., Adelotus, Limnonectes), but these taxa lack hyperossification and do not occupy the hyperossified vertebrate predator morphospace. ...
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Frogs (Anura) are one of the most diverse vertebrate orders, comprising more than 7,000 species with a worldwide distribution and extensive ecological diversity. In contrast to other tetrapods, frogs have a highly derived body plan and simplified skull. In many lineages of anurans, increased mineralization has led to hyperossified skulls, but the function of this trait and its relationship with other aspects of head morphology are largely unexplored. Using three-dimensional morphological data from 158 species representing all frog families, we assessed wide-scale patterns of shape variation across all major lineages, reconstructed the evolutionary history of cranial hyperossification across the anuran phylogeny, and tested for relationships between ecology, skull shape, and hyperossification. Although many frogs share a conserved skull shape, several extreme forms have repeatedly evolved that commonly are associated with hyperossification, which has evolved independently more than 25 times. Variation in cranial shape is not explained by phylogenetic relatedness but is correlated with shifts in body size and ecology. The species with highly divergent, hyperossified skulls often have a specialized diet or a unique predator defense mechanism. Thus, the evolution of hyperossification has repeatedly facilitated the expansion of the head into multiple new shapes and functions.
... Large orthopterans and small vertebrates are known to be important prey items in Ceratophrys cornuta, a frog species that is characterized as a sit-and-wait predator that often consumes large prey more than half of its snout-vent length (Duellman and Lizana, 1994). Other frog genera that feed on relatively large prey include Leptobatrachus, Chacophrys, Pyxicephalus, Aubria, and Hemiphractus (Fabrezi and Emerson, 2003). These predatory anurans have evolved odontoid fangs and serrations on the lower jaw that can improve prey capture, but none of these structures are true teeth. ...
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The South American frogs of the family Cer-atophryidae (three genera, twelve extant species) display unusual larval diversity and developmental variation despite rather similar adults. Many adult features of ceratophryids are associated with terrestrial/fossorial habits and resistance to desiccation; however, adults of the genus Lepidoba-trachus are aquatic. Morphological novelties have evolved in the ceratophryid feeding mechanism that makes them capable of feeding on exceptional large prey (i.e. megalophagy). Lepidobatrachus is unusual in having less ecomorphological differences between its larvae and adults than virtually all other anurans. Some unique features are differentiated in the tadpole and then exaggerated in the adult (e.g., a posterior displaced jaw artic-ulation) in a manner unseen in other anurans. Both the larvae and the frog are similarly able to capture large prey underwater.
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The South American frogs of the family Ceratophryidae (three genera, twelve extant species) display unusual larval diversity and developmental variation despite rather similar adults. Many adult features of ceratophryids are associated with terrestrial/fossorial habits and resistance to desiccation; however, adults of the genus Lepidobatrachus are aquatic. Morphological novelties have evolved in the ceratophryid feeding mechanism that makes them capable of feeding on exceptional large prey (i.e. megalophagy). Lepidobatrachus is unusual in having less ecomorphological differences between its larvae and adults than virtually all other anurans. Some unique features are differentiated in the tadpole and then exaggerated in the adult (e.g., a posterior displaced jaw articulation) in a manner unseen in other anurans. Both the larvae and the frog are similarly able to capture large prey underwater. The article reviews how shifts in developmental patterns have led to a novel way of life for both larval and adult Lepidobatrachus spp. Key Concepts • Derived features of ceratophryid larvae carry over metamorphosis to the adults and are central to the overall morphological evolution of Ceratophryidae. • Ceratophryidae shows how evolution can act upon development to produce organisms with novel structures and ecology. • Megalophagy is associated with a wealth of other specialisations that are products of shifts in development. • The origin of evolutionary novelties in Lepidobatrachus's ontogeny has produced a dramatic and unique larval ecomorphology. • Lepidobatrachus has broken metamorphic constraints to achieve common and shared larval and adult adaptations for megalophagy and feeding underwater.
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