JOURNAL OF MORPHOLOGY 272:149–168 (2011)
The Evolution of Jumping in Frogs: Morphological
Evidence for the Basal Anuran Locomotor Condition
and the Radiation of Locomotor Systems in Crown
Group Anurans
Stephen M. Reilly* and Michael E. Jorgensen
Department of Biological Sciences and Center for Ecology and Evolutionary Studies, Ohio University,
Athens, Ohio 45701
ABSTRACT Our understanding of the evolution of frog
locomotion follows from the work of Emerson in which
anurans are proposed to possess one of three different iliosacral configurations: 1) a lateral-bending system found
in walking and hopping frogs; 2) a fore-aft sliding mechanism found in several locomotor modes; and 3) a sagittalhinge-type pelvis posited to be related to long-distance
jumping performance. The most basal living (Ascaphus)
and fossil (Prosalirus) frogs are described as sagittalhinge pelvic types, and it has been proposed that long-distance jumping with a sagittal-hinge pelvis arose early in
frog evolution. We revisited osteological traits of the pelvic
region to conduct a phylogenetic analysis of the relationships between pelvic systems and locomotor modes in
frogs. Using two of Emerson’s diagnostic traits from the
sacrum and ilium and two new traits from the urostyle,
we resampled the taxa originally studied by Emerson and
key paleotaxa and conducted an analysis of ancestralcharacter state evolution in relation to locomotor mode.
We present a new pattern for the evolution of pelvic systems and locomotor modes in frogs. Character analysis
shows that the lateral-bender, walker/hopper condition is
both basal and generally conserved across the Anura.
Long-distance jumping frogs do not appear until well
within the Neobatrachia. The sagittal-hinge morphology
is correlated with long-distance jumping in terrestrial
frogs; however, it evolved convergently multiple times in
crown group anurans with the same four pelvic traits
described herein. Arboreal jumping has appeared in multiple crown lineages as well, but with divergent patterns
of evolution involving each of the three pelvic types. The
fore-aft slider morph appears independently in three different locomotor modes and, thus, is a more complex system than previously thought. Finally, it appears that the
advent of a bicondylar sacro-urostylic articulation was
originally related to providing axial rigidity to lateralbending behaviors rather than sagittal bending.
J. Morphol. 272:149–168, 2011. Ó 2010 Wiley-Liss, Inc.
about it from the jumping frogs of Calaveras County
(Twain, 1867) to the etymology of the oldest known
anuran named Prosalirus bitis, meaning ‘‘to leap
forward, high over it’’ (Shubin and Jenkins, 1995).
The naming of this early frog appears to reflect two
kinds of ‘‘leap’’ in the transition to frogs. First, it
reflects the apparent design leap from the generalized tetrapod body plan to the set of traits that distinguish the frog morphotype: fewer presacral vertebrae, longer hindlimbs, and long ilia between which
lies a shortened, fused tail called the urostyle. The
early Triassic amphibian Triadobatrachus has the
antecedents of the anuran body plan (moderately
longer ilia, fewer trunk, and caudal vertebrae) but
was built for lateral undulatory walking (Rage and
Roček, 1986, 1989; Sanchiz, 1986). The earliest
known frog, Prosalirus and its well-known sister
taxon Notobatrachus, made the transition to longer
ilia and caudal vertebrae fused into the urostyle
(Báez and Nicoli, 2004). Both are morphologically
intermediate between Triadobatrachus and modern
anurans (Jenkins and Shubin, 1998).
The second ‘‘leap’’ reflects the behavioral leap to
specialization for bilateral limb extension in terrestrial locomotion that appears to have arisen with
the new body plan. The current hypothesis for the
evolution of locomotion in frogs follows from the
work of Emerson (1979, 1982) in which anurans
are proposed to possess three different iliosacral
configurations that are correlated with locomotor
mode (burrowing, walking, hopping, and jumping)
KEY WORDS: frog evolution; jumping; sacrum; urostyle; bicondylar
*Correspondence to: Stephen M. Reilly, Department of Biological
Sciences, Ohio University, Athens, OH 45701.
E-mail: [email protected]
INTRODUCTION
Received 10 May 2010; Revised 10 June 2010;
Accepted 19 June 2010
The advent of frog jumping is one of the most
enigmatic and paradoxical evolutionary transitions
in vertebrate evolution. Much has been written
Published online 8 November 2010 in
Wiley Online Library (wileyonlinelibrary.com)
DOI: 10.1002/jmor.10902
Ó 2010 WILEY-LISS, INC.
Additional Supporting Information may be found in the online
version of this article.
150
S.M. REILLY AND M.E. JORGENSEN
Fig. 1. Three basic pelvic designs in frogs (Emerson 1979, 1982) based on the shape of the sacral diapophyses, the presence/absence of iliac ridges (CT images), and the nature of the dorsal iliosacral ligaments (bottom, modified from Emerson, 1982). A: Emerson’s fore-aft slider morph with expanded flat-sided sacral diapophyses (flat sides either bony or cartilaginous) and a large ilio-ilial
ligament. B: The lateral-bender morph with expanded but rounded diapophyses (with rounded cartilaginous caps, not shown) and
long dorsal iliosacral ligaments. C: The sagittal-hinge morph with rod-like elevated (white arrows) diapophyses, iliac ridges, and
short dorsal iliosacral ligaments.
and ecological (terrestrial and arboreal) groups.
One configuration (with greatly expanded flatsided sacral diapophyses) is proposed to be a predominantly fore-aft-sliding system in derived
aquatic forms but is also scored for some climbing
and burrowing forms. Another configuration (with
bowtie-like sacra and narrow to moderately
expanded sacral diapophyses) is mostly a lateralbending system in walker/hoppers and some burrowers. The third (with rod-like, nonexpanded diapophyses) is hypothesized to function as a sagittalhinge system, limiting the iliosacral movement to
vertical rotation in long-distance jumping forms.
Journal of Morphology
These pelvic functions are based on limited functional studies of a few model species (movement or
cineradiography of anesthetized specimens: Whiting, 1961; Emerson, 1979; one EMG study: Emerson and De Jongh, 1980; and cineradiographic
frames of three sagittal-hinge jumps: Jenkins and
Shubin, 1998) and are illustrated in videos in the
Supporting Information S1–S5.
The ‘‘high over it’’ connotation of P. bitis’ etymology reflects the current hypothesis that long-distance jumping with the sagittal-hinge (as observed
in ranid frogs) is the ancestral state for Anura
(Fig. 1C; Shubin and Jenkins, 1995; Jenkins and
THE EVOLUTION OF LOCOMOTION IN FROGS
Shubin, 1998). This hypothesis has not been proposed from any formal phylogenetic analysis but is
based entirely on interpretations of iliosacral traits
in the most basal fossil (Prosalirus) and living
(Ascaphus) frog taxa as evidence that the sagittalhinge-type pelvis appeared in the first frogs. The
extinct Prosalirus was interpreted as having the
sagittal-hinge morph and ranid-like jumping ability based on two partial ilia and one partial sacrum among the remains of about four individuals
(Shubin and Jenkins, 1995; Jenkins and Shubin,
1998). Although Emerson did not comment on the
basal anuran sacral condition, she did score the
basal living frog family (Leiopelmatidae) as possessing her sagittal-hinge iliosacral traits based on
dissection of one specimen of Ascaphus truei
(Emerson, 1979).
With the ‘‘sagittal-hinge jumping is primitive’’
hypothesis in mind, we were perplexed by the
question of how ranid-like jumping evolved so rapidly in the first frogs. A gradual transition seems
more plausible, one changing from a lateral-bending mode (posited in Triadobatrachus) to a walker/
hopper mode of other basal living frogs (such as
Rhinophrynus and Bombina) to dorsoventral bending during locomotion posited for phylogenetically
derived jumping frogs. We also questioned the parsimony of resulting inferences from the ‘‘sagittalhinge jumping is primitive’’ hypothesis that many
basal and crown taxa subsequently and repeatedly
‘‘abandoned’’ the hinge joint to evolve the other
horizontal-moving iliosacral configurations for
swimming, walking, hopping, and burrowing
(Shubin and Jenkins, 1995; Přikryl et al., 2009).
The purpose of this study was to reexamine the
anatomy of the pelvic region in frogs to better
understand historical patterns and correspondence
of iliosacral traits in relation to Emerson’s pelvic
functional complexes and basic behavioral locomotor modes. We studied two bony characters Emerson used that are well defined and easily scorable.
Emerson (1979, 1982) defined the sagittal-hinge
type as having two bony features: 1) narrow
(termed cylindrical, nonexpanded) sacral diapophyses extending posterolaterally and 2) large raised
dorsal ridges on the ilia (Fig. 1). In contrast,
Emerson’s lateral-bender and fore-aft slider
morphs have slightly to moderately expanded or
greatly expanded flat-sided sacral diapophyses,
respectively, and lack iliac ridges (Fig. 1). We
examined the traits that defined Emerson’s (1982)
three iliosacral functional units in three samples.
First, we studied larger sample sizes of the same
(or closely related) species Emerson used. Second,
we included a larger taxonomic sample of the most
basal living frogs (Leiopelmatidae), which are considered to be very similar to the last common
ancestor of living frogs (Roelants and Bossuyt,
2005). Finally, we added extinct taxa (including
Prosalirus) for which pelvic traits could be scored
151
and their phylogenetic placement is known. We
scored taxa using literature descriptions, new dissections, cleared and double-stained preparations,
and micro-CT and radiographic imagery. In addition, we scored two new traits related to pelvic
function: the form of the sacro-urostylic articulation and nature of the dorsal ridge on the urostyle.
Basic locomotor states were taken from the locomotor modes scored for the study taxa by Emerson
(1979, 1982), and data on jumping performance in
relation to body length were used to provide a
quantitative distinction for hopping versus jumping following Zug (1978) and Emerson (1979,
1982).
MATERIALS AND METHODS
We sampled pelvic characters in 75 species representing five
paleotaxa and a resampling of 54 taxa used by Emerson (1979,
1982) in her description of the iliosacral functional complexes of
frogs (Table 1). Thirty-six were the same species, 13 were different species of the same genus, two were different genera in the
same family, and 18 were new species we added. Three taxa
were omitted (where Emerson sampled two closely related species within families). We also sampled the two species of Ascaphus currently recognized, one species of Leiopelma (n 5 3) and
five extinct basal taxa (Table 1) for which phylogenetic relationships have been proposed (Gao and Wang, 2001). The phylogeny
of the extant taxa primarily follows Frost et al. (2006) with topology of the microhylid subfamilies following Van der Meijden
et al. (2007), and we recognized the family status of the Eleutherodactylidae following Hedges et al. (2008). Emerson’s original sampling now covers a broader array of higher anuran taxa
because of advances in our understanding of anuran phylogeny
(Frost et al., 2006). Taxonomic changes in generic names are
indicated with the new usage in parentheses in the middle
column of Table 1. Museum specimen numbers are listed in
Appendix.
Characters were studied and scored from dorsal X-ray images
(n 5 except where noted in Table 1) from each of the extant
taxa and verified where needed by dissection, from cleared and
double-stained specimens (bone and cartilage), from whole-body
micro-CT images of 36 taxa (asterisks in Table 1), and using
illustrations and/or descriptions in the literature for extant
(Stephenson, 1952; Ritland, 1955; Estes and Reig, 1973; Duellman and Trueb, 1994; Evans and Borsuk-Bialynicka, 1998;
Brown and Crespo, 2000; Pugener, 2002; Přikryl et al., 2009;
Pugener and Maglia, 2009) and extinct taxa (Rage and Roček,
1986, 1989; Sanchiz, 1986; Roček and Nessov, 1993; Báez and
Basso, 1996; Jenkins and Shubin, 1998; Gao and Wang, 2001;
Pugener, 2002; Gao and Chen, 2004; Roček, 2008; Pugener and
Maglia, 2009). Micro-CT images were scanned at the Ohio University Micro-CT facility using a GE eXplore Locus small animal scanner at a slice thickness of 45 or 90 lm. Data were output as DICOM images, and 3D reconstructions were produced
in the program MeVisLab (version 2.0).
Ancestral Character State Reconstruction
Ancestral character states of crown group taxa were reconstructed for each of our four pelvic characters (sacral diapophyseal expansion, dorsal iliac ridge, sacro-urostylic articulation,
and urostyle dorsal ridge) using maximum likelihood (ML) in
Mesquite (version 2.72; Maddison and Maddison, 2009). The
Mk1 model of evolution was used in the ML analysis because
this treats changes between all character states as equally
likely (Schluter et al., 1997). Character probability trees were
used to visualize patterns of evolution in individual traits.
Journal of Morphology
152
S.M. REILLY AND M.E. JORGENSEN
TABLE 1. Species sampled in order of taxa listed on phylogenetic trees
Sampled taxa
yTriadobatrachus
yProsalirus
yNotobatrachus
yMesophryne
Leiopelmatidae
Rhinophrynidae
yPalaeobatrachus
Pipidae
Emerson’s (1979, 1982) study species
Ascaphus truei
Rhinophrynus dorsalis
Xenopus laevis
Pipa pipa
Alytidae
Discoglossus pictus
Bombinatoridae
Bombina orientalis
Scaphiopodidae
Pelobatidae
Megophryidae
Scaphiopus couchii
Pelobates fuscus
Megophrys monticola
Myobatrachidae
Pseudophryne occidentalis
Limnodynastidae
Eleutherodactylidae
Hylidae:
Pelodryadinae
Phyllomedusinae
Notaden bennetti
Eleutherodactylus punctariolis
Litoria rubella
Agalychnis callidryas
Pachymedusa dacnicolor
Hylinae
Hyla cinerea
Hyla gratiosa
Smilisca phaeota
Phrynohyas (Trachycephalus) venulosa
Hylinae
Pseudacris triseriata
Hyla (Pseudacris) regilla
Leptodactylus pentadactylus
Leptodactylidae
Ceratophryidae
Cycloramphidae
Leiuperidae
Bufonidae
Telmatobius marmoratus
Rhinoderma darwinii
Physalaemus (Engystomops) pustulosus
Bufo (Rhinella) marinus
Bufo (Anaxyrus) boreas
Bufo (Anaxyrus) americanus
Bufo (Rhaebo) blombergi
Bufo (Epidalea) calamita
Melanophryniscus stelzneri
Atelopus zeteki
Dendrobatidae
Dendrobates tinctorius
Hemisotidae
Arthroleptidae
Hemisus marmoratus
Leptopelis bocagii
Leptopelis aubryi
Kassina senegalensis
Hyperolius marmoratus
Hyperoliidae
Microhylidae:
Kalophryninae
incertae cedis
Gastrophryninae
Phyrnomerinae
Microhylinae
Journal of Morphology
Kalophrynus pleurostigma
Myersiella subnigra
Gastrophryne carolinensis
Hypopachus variolosus
Dasypops shirchi
Phrynomerus (Phrynomantis) annectens
Microhyla rubra
Kaloula pulchra
Glyphoglossus molossus
Species in this study
1, 2 (see Fig. 6)
3 (see Figs. 2 and 3)
4, 5 (see Figs. 2 and 3)
6
Same species*, 7
Ascaphus montanus* (n 5 3)
Leiopelma hochstetteri* (n 5 3), 8
Same species*
6
Same species (x 5 4)
Same species
Pseudhymenochirus merlini*
Same species*
Alytes obstetricans*
Same species* (n 5 3)
Bombina maxima
Scaphiopus hammondii*
Pelobates cultripes (n 5 4)
Megophrys nasuta
Ophryophryne microstoma*
Scutiger boulengeri*
Pseudophryne bibronii
Myobatrachus gouldii*
Same species
Eleutherodactylus coqui
Litoria nasuta*
Same species
Same species*
Phyllomedusa sauvagii* (n 5 1)
Same species (n 5 4)
Hyla versicolor (n 5 3)
Smilisca baudinii
Trachycephalus jordani
Triprion petasatus*
Same species
Same species
Leptodactylus gracilis*
Paratelmatobius lutzii* (n 5 4)
Telmatobius brevipes
Same species*
Same species
Same species
Same species* (n 5 3)
Rhaebo haematiticus
Same species (n 5 4)
Same species
Atelopus spumarius*
Pedostibes hosii*
Dendrobates auratus
Oophaga pumilio*
Same species*
Cardioglossa leucomystax
Same species
Hyperolius lateralis
Same species*
Same species* (n 5 1)
Same species
Same species
Same species*
Phrynomantis bifasciatus*
Microhyla berdmorei
Same species
Same species*
Chaperina fusca*
THE EVOLUTION OF LOCOMOTION IN FROGS
153
TABLE 1. (Continued)
Sampled taxa
Emerson’s (1979, 1982) study species
Asterophryninae
Cophixalus riparius
Ptychadenidae
Hildebrandia ornata
Rhacophoridae
Rhacophorus leucomystax
Rhacophorus colletti
Chiromantis rufescens
Rana (Lithobates) catesbeiana
Rana(Lithobates) pipiens
Ranidae
Species in this study
Cophixalus cheesmanae
Cophixalus oxyrhinus
Same species (n 5 4)
Ptychadena anchietae*
Rhacophorus viridis
Rhacophorus chenfui*
Chiromantis xerampelina*
Same species (n 5 3)
Same species*
Amolops hosii* (n 5 3)
Meristogenys jerboa*
The 54 species used by Emerson (1979, 1982) in her description of the pelvic functional complex in
frogs (middle column) are currently assigned to the 34 higher listed taxa in column 1. We resampled
Emerson’s taxa (n 5 5–8 per species (Appendix) or as noted, column 3) with some substitutions and
added 18 species within these families as well as extinct taxa (y) of known phylogenetic placement for
which traits could be scored from literature accounts. Micro-CT material is marked with asterisks.
Three species were omitted in families represented by two species. Sources for paleotaxa and additional leiopelmatids are indicated with numbers in column 3.
1, Rage and Roček, 1989; 2, Roček, 2008; 3, Jenkins and Shubin, 1998; 4, Pugener, 2002; 5, Báez and
Nicoli, 2004; 6, Gao and Wang, 2001; 7, Ritland, 1955; 8, Stephenson, 1952.
Unique character states (indicated by square symbols) were
not included in the ML reconstructions. Patterns of trait correspondence across all four traits were then used to identify
pelvic systems and compare them to locomotor modes (burrowing, walking, hopper, terrestrial jumping, and arboreal
jumping) of Zug (1978), Emerson (1979), and Brown and
Crespo (2000). We follow the convention of Zug (1978) and
Emerson (1979) who used an eight body-lengths threshold to
distinguish short from long-distance leaping and termed them
hoppers and jumpers, respectively. Although the hopper/
jumper distinction is a relatively quantitative one, the other
general locomotor modes used describe the most common
types of locomotion used by each species and are the best comparative data available in the literature. Clearly, there are
exceptions to these patterns in some taxa, but the simplification of locomotor states is necessary to begin to understand
patterns of evolution in anuran locomotor anatomy. The work
was conducted from 2008 to 2010 at Ohio University under
approved animal care and use protocols.
RESULTS
Emerson’s Skeletal Sacral Traits
Sacral shape. Micro-CT images illustrating
Emerson’s three basic types of frog pelvic systems
are shown in Figure 1, and pelvic movements associated with these types are presented in movies in
the Supporting Information S1–S6. Sacral diapophyseal expansion was the most obvious skeletal
character to score in dorsal view, and it has three
states (Emerson, 1982). The fore-aft-slider morph
possesses longitudinally expanded and flat-sided
butterfly-like diapophyses (Fig. 1A). We will call
this the flat-sided morph. These sacra are either
completely bony (e.g., Pseudhymenochirus) or have
rounded sacral diapophyses upon which large
extended cartilaginous edges make up the flat
sides that articulate with the ilia (e.g., Triprion
and Litoria). Here, a large ilio-ilial ligament
extends from the ventrolateral and anterior half of
one iliac shaft, dorsally over the back to the other
iliac shaft, forming a tunnel in which the sacrum
slides over the ilia (Fig. 1A, bottom). Manipulations of this pelvic type show that the ilia appear
to be limited to bilateral fore-aft sliding because
lateral movements of the pelvis translate through
the sacrum to cause bending in the presacral vertebral column (Supporting Information S1).
The lateral-bender morph has a bowtie-like sacrum ranging from narrow to widely expanded diapophyses (Fig. 1B). The diapophyses are dorsoventrally flattened with curved bony margins covered
with curved cartilaginous caps. The cartilaginous
caps extend the lateral edges of the sacrum to produce a larger curved articular surface than the
underlying bone and may extend beyond the bony
tip anteriorly and posteriorly as well (Fig. 4C,D).
This morph has a dorsal iliosacral ligament with a
wide attachment on the anterolateral ilium
(slightly narrower than the width of the distal diapophysis) that extends medially over the diapophysis and narrows to its attachment on the medial
half of the dorsal aspect of the diapophysis (Fig.
1B, bottom). Each iliac shaft can move fore and aft
several millimeters to the extent that the ligament
allows. Thus, the ilia can slide fore and aft together (Supporting Information S2) or in opposite
directions during lateral bending (Fig. 4B; Supporting Information S3).
The sagittal-hinge morph has rod-like diapophyses that extend posterolaterally and are usually
elevated above the horizontal plane that runs
along the tips of the vertebral neural arches (Fig.
1C). In these sacra, the ilia are tightly bound to
the diapophyses by short, dorsal iliosacral ligaments incorporated into a capsule by a binding of
fascia. In this pelvic type, there is little movement
Journal of Morphology
154
S.M. REILLY AND M.E. JORGENSEN
around these ligaments except for hinge-like bending as the ilia rotate under the rod-like diapophyses (Supporting Information S4). Here, lateralbending movements translate through the tightly
bound iliosacral articulation to bend the presacral
vertebral column (Supporting Information S5).
Emerson’s iliac ridge trait. Emerson’s second
bony trait was the presence of a large dorsal ridge
on each iliac shaft that she described as diagnostic
of the sagittal-hinge morph (1979, 1982). Our
resurvey reveals that, when present, this dorsal
ridge is a large to very large ‘‘fin’’ that arises on
the dorsal aspect of the ilia just posterior to where
the ilia articulate with the sacral diapophyses and
extends posteriorly to the ischium (Fig. 2B). The
iliac ridge exists in striking contrast to the smooth
ilia seen in other pelvic types (Fig. 2A). In the
smooth ilia, the ilial cross section has a round or
oval shape and looks much like the cortical cross
section of a long bone (Fig. 2). In ilia with a dorsal
ridge, the ridge extends well above the diameter of
the iliac shaft, generally curves medially on its
dorsal aspect, and it often increases in height posteriorly (Fig. 2B). The pipids are aquatic and have
laterally directed ridges that we scored as unique
(&); we did not include these in the character
reconstruction.
Reinterpreting Emerson’s Traits in
Prosalirus and Ascaphus
Sacral shapes of fossil and living basal anurans
are illustrated in Figure 3A–F. The most basal
frogs are represented by the sister taxa Notobatrachus and Prosalirus (Gao and Wang, 2001). Notobatrachus is the best-known Jurassic frog with
over 100 specimens, many from the same site with
exceptional preservation (Báez and Nicoli, 2004).
The sacral diapophyses of Notobatrachus are dorsoventrally flattened (Fig. 3A, from Pugener,
2002), and the well-preserved series of sacra illustrates the range of intraspecific variation in diapophyseal expansion in this species (Fig. 3B, from
Báez and Nicoli, 2004). The sacrum of Prosalirus
(Fig. 3C) is drawn from one partial fossil found in
a group of four disarticulated specimens (Jenkins
and Shubin, 1998). The single known Prosalirus
diapophysis (Fig. 3C) was described as approximately triangular in cross section but widest in
the anteroposterior direction. Although it lacks a
key sagittal-hinge trait (iliac ridges), Shubin and
Jenkins (1995) interpreted Prosalirus to have a
sagittal-hinge pelvis apparently because of the
general morphological similarity of its sacrum to a
ranid sacrum. Others consider Prosalirus to be
most similar to Notobatrachus on the basis of sacral morphology and several other osteological
traits (Báez and Nicoli, 2004; Pugener and Maglia,
2009). As shown in Figure 3, the Prosalirus sacJournal of Morphology
rum is similar to those of other basal anuran taxa,
and the fossil reconstruction falls well within the
range of phenotypic variation known in both its
sister taxon Notobatrachus (Fig. 3B) and the most
basal living frog Ascaphus (Fig. 3D). In addition,
shading in the reconstruction indicates that the
Prosalirus diapophyses are not elevated above the
horizontal plane as in sagittal-hinge sacra (Fig.
1C). We follow Pugener and Maglia (2009) in scoring the Prosalirus sacrum as the expanded type,
and thus, a lateral-bender morph.
Our reexamination of the sacra of the most basal
living taxa confirms that Ascaphus and Leiopelma
also have dorsoventrally flattened diapophyses
(Duellman and Trueb, 1994; Gao and Wang, 2001;
Pugener, 2002; Fig. 3E,F). Ritland (1955) illustrated the variability in diapophyseal expansion in
Ascaphus (Fig. 3D) similar to that in Notobatrachus (Fig. 3B). Ascaphus possesses expanded cartilaginous flanges on the diapophyses illustrating
the larger extent of sacral expansion often not
revealed by ossified portions of frog sacra (Fig.
4C,D). Leiopelma has flattened diapophyses, as
well, but possesses a unique sacrum among frogs
in that it is proximally ‘‘Y’’ shaped diapophyses
articulate on the midline (Stephenson, 1952; Fig.
3F). Each diapophysis can be moved independently
anteroposteriorly relative to the sacral centrum.
Both Ascaphus and Leiopelma lack the iliac ridges
diagnostic of Emerson’s sagittal-hinge morph (Fig.
3E,F). It is unclear why Emerson scored Ascaphus
as having a rod-like diapophysis unless she examined a specimen with an extremely narrow diapophysis or a juvenile. Emerson also based her
scoring on the size of the dorsal iliosacral ligament. In our dissections of Ascaphus, we found a
long dorsal iliosacral ligament essentially identical
to that of other lateral-bender sacra (Fig. 4A right,
B) with a broad attachment along the ilium and a
sacral attachment extending to the proximal end
of the diapophysis (Fig. 4C). In addition, there is a
large articular surface on the dorsal face of the
ilium where the sacrum slides in the horizontal
plane (Fig. 4C, right ilium) unlike any sagittalhinge sacrum. Finally, manipulations of the Ascaphus pelvis (Fig. 4D) show a great deal of fore-aft
play in the iliosacral joints, with the dorsal iliosacral ligament limiting the extent of forward and
backward motion (bilaterally and unilaterally) in
the same way it does in other lateral-bender
morphs (compare Fig. 4B–D or Supporting Information S3–S6). It is clear that Ascaphus has the
lateral-bender morphology on the basis of expanded sacral diapophyses, smooth ilia, long dorsal
iliosacral ligaments, and the horizontal plane of
pelvic mobility. The leiopelmatids also have a fundamentally different swimming (Abourachid and
Green, 1999; Nauwelaerts and Aerts, 2002) and
leaping (Essner et al., 2010) behavior than other
frogs.
THE EVOLUTION OF LOCOMOTION IN FROGS
155
Fig. 2. Ilial and urostyle morphology in frogs. Frogs either have smooth ilia (A) or large dorsal ridges on them (B). The urostyle
of frogs is either smooth (A) or has large dorsal ridges extending along the anterior half or the full length of the bone (B). Some
frogs with smooth ilia retain some architectural remnant of the neural arch components in the form of raised lines of bone on the
dorsal surface (A). Line drawings illustrate the plesiomorphic ‘‘L’’ shaped sacral diapophyses and independent caudal vertebrae but
smooth anuran-like extended ilia of the immediate outgroup to Anura (Triadobatrachus, modified from Rage and Roček, 1986) and
the smooth urostyle and smooth ilium of the basal most anurans [the Notobatrachids Notobatrachus and Prosalirus (modified from
Pugener, 2002 and Jenkins and Shubin, 1998, respectively)].
Journal of Morphology
156
S.M. REILLY AND M.E. JORGENSEN
Fig. 3. Sacral shapes and intraspecific variation in the degree of expansion in basal lateralbender frogs. Line drawings are modified from A: Pugener, 2002; B: Báez and Nicoli, 2004; C:
Jenkins and Shubin, 1998; and D: Ritland, 1955.
Two New Pelvic System Traits on the
Urostyle
One of the diagnostic features of anurans is that
the adult caudal vertebrae are fused into a single
rod-like tail, the urostyle (Gaupp, 1896). In surveying taxa for this analysis, we were able to discern
and score two additional traits from the urostyle
that are relevant to the design of the pelvic girdle
in frogs because many of the muscles extending to
the sacrum and ilia arise from this fused remnant
of the tail. One is the nature of the urostyle’s articulation with the sacrum and the other concerns
the presence and extent of a dorsal ridge on the
urostyle.
Journal of Morphology
Sacro-urostylic articulation. Although Triadobatrachus possessed caudal vertebrae (Fig. 7,
&), the earliest frogs (e.g., Notobatrachus, Figs.
2A and 3A) retained only one unfused postsacral
vertebra between the sacrum and the urostyle.
The shapes of the centra in these taxa indicate
that normal intervertebral cartilaginous disks lie
on either side of the unfused postsacral vertebra.
In higher taxa, all of the vertebrae are fused into
the urostyle that articulates with the sacral centrum (Gaupp, 1896; Duellman and Trueb, 1994).
In basal frogs, the sacro-urostylic articulation
ranges from having a normal intervertebral disk
and large concave articular surfaces (Fig. 5A) to
THE EVOLUTION OF LOCOMOTION IN FROGS
157
Fig. 4. Lateral-bender morphology and pelvic movements in Ascaphus. The large dorsal iliosacral ligaments (A, right) that limit
the lateral-bending movements of the ilia on the sacrum are shown in the lateral-bender morph Rhinella marinus (B, Supporting
Information S3). Dorsal ligaments and a flat iliosacral articulation surface (C) and lateral-bending movements (D, Supporting Information S4) are present in Ascaphus revealing that Ascaphus is not a sagittal-hinge morph. Panel A is modified from Emerson
(1982).
Fig. 5. Sacro-urostylic articulations in frogs. Frogs have either a single articulation surface with a full range of axial movements
possible (A, monocondyly), a bicondylar articulation limiting lateral bending of the urostyle (B), or the urostyle is fused to the sacrum (Fig. 1: A, top and bottom panels; B, top panel). Line drawings, top to bottom, are modified from Jenkins and Shubin, 1998
and Pugener, 2002.
Journal of Morphology
158
S.M. REILLY AND M.E. JORGENSEN
centra forming a ball and socket (Fig. 5A, Barbourula). For the purposes of this study, we consider
all urostyles with single articular surfaces as
monocondylar (Fig. 5A). Many frogs have developed what has been called a bicondylar sacro-urostylic joint (Fig. 5B; Duellman and Trueb, 1994;
Pugener and Maglia, 2009). Here, instead of a single articular surface, the sacral centrum has two
side-by-side hemispherical condyles that articulate
with a matching pair of concave surfaces on the
anterior face of the urostyle. In a third and
derived form (discussed below), the urostyle is solidly fused to the sacrum (e.g., Fig. 1A: Pseudhymenochirus; 1B: Scaphiopus). Cases of urostylic
fusion that appear in several taxa across the phylogeny from both mono- and bicondylar ancestry
are discussed below. The details of variation in
monocondyly and the development of the bicondylar sacro-urostylic complex and the origin of the
fused condition have recently been described by
Pugener and Maglia (2009) but require a broader
sampling and comparative analysis.
Much has been said about the hypothesized
function of the urostyle in locomotion and the contrasting range of movements possible with a monoversus bicondylar urostyle (Green, 1931; Whiting,
1961; Emerson, 1979, 1982; Emerson and De
Jongh, 1980; Duellman and Trueb, 1994; Jenkins
and Shubin, 1998; Pugener and Maglia, 2009).
Currently, the function of the urostyle in different
modes of locomotion is not well understood as it
has only been examined in one comparative study
of three species (Emerson and De Jongh, 1980). In
tetrapods, muscles that control tail movement are
also widely used in moving the hindlimb. However,
in frogs with elongated ilia shifting the acetabula
posterior to the tail, the muscles of the tail (urostyle) have become involved in novel mechanisms
controlling movements of the pelvis relative to the
vertebral column during locomotion (Emerson,
1979, 1982). Functionally, there may be different
biomechanical implications for a monocondylar
joint with the freedom to move three dimensionally
compared to the bicondylar joint that appears to
be uniaxial with movement restricted to axial flexion-extension. Accordingly, the bicondylar joint has
been considered the best joint for jumping locomotion because it is hypothesized to be involved in
allowing the body to straighten out during take off
(Emerson, 1979, 1982; Emerson and De Jongh,
1980; Jenkins and Shubin, 1998; Kargo et al.,
2002; Pugener and Maglia, 2009). Although the
relationship between jumping and bicondyly (and
monocondyly and lateral bending) has been proposed, the relationship between the state of the
sacro-urostylic articulation and Emerson’s pelvic
morphs has not been quantified. Therefore, we
added a scoring of mono- versus bicondylar sacrourostylic articulation for comparison to the other
pelvic traits and variation across locomotor modes.
Journal of Morphology
Urostyle dorsal ridge. In all frogs, the body of
the urostyle is more or less cylindrical but differs in
the presence and nature of a ridge on its dorsal surface. In the survey of our sample taxa, we found
and scored three different types of urostyles. Some
frogs have smooth urostyles with full-length circular cross sections essentially like a limb bone (Fig.
2A). In some of these, a small increase in dorsal
thickness is observed as a single (Fig. 2: Bombina;
Fig. 3F, Leiopelma) or double (Fig. 2: Myobatrachus; Fig. 3E, Ascaphus) line of thicker bone anteriorly that extends about a third of the way posteriorly on the urostyle. When present on these otherwise smooth urostyles, this feature appears to be a
remnant of the neural arch components. The other
two types of urostyles we scored have a distinct,
elevated dorsal ridge several times thicker than the
cortical thickness of the shaft of the urostyle (Fig.
2) and similar to the iliac ridges. These ridges are
larger anteriorly and generally expand into a dorsal
knob, which extends over the sacro-urostylic joint
(Fig. 2B). We distinguished two forms of urostyle
ridges by length, one with the ridge extending back
only along the anterior half of the urostyle (Fig. 2:
Triprion and Hemisus) and others with a fulllength urostyle ridge (Fig. 2: Lithobates). The
pipids have a short ‘‘T’’ shaped ridge on the urostyle
that we scored as unique (&) and did not include in
the character reconstruction.
The ridges on ilia have been proposed to function in providing larger muscle attachment surfaces (Přikryl et al., 2009). These would allow for
larger muscles of the ilia to control the movements
of the pelvis relative to the body and the limbs relative to the pelvis (Emerson and De Jongh, 1980;
Duellman and Trueb, 1994; Přikryl et al., 2009).
We propose that the ridges on the urostyle provide
the same function of providing larger muscle
attachment sites. Thus, the presence of ridges can
provide insights into the movements and function
of the urostyle in relation to the body and the
limbs. In addition, as discussed later, the correspondence of iliac and/or urostyle ridges with anatomical features allowing (monocondyly) or limiting urostylic movements (fusion, bicondyly) can
provide insights into the functional role of the
urostyle during locomotion in different frog pelvic
morphs.
Patterns of Pelvic Trait Evolution in Frogs
Evolutionary patterns of Emerson’s traits are
shown in Figure 6. With the corrected states for
Prosalirus and Ascaphus presented above, it
becomes clear that the basal condition for frogs is
expanded sacral diapophyses (Fig. 6, left) and
smooth iliac shafts (Fig. 6, right). This is not only
the basal condition but the general condition
across frogs based on high probabilities of
expanded diapophyses at the base of the Neobatra-
THE EVOLUTION OF LOCOMOTION IN FROGS
159
Fig. 6. Patterns of evolution in Emerson’s osteological pelvic traits. Maximum-likelihood ancestral character state reconstructions for the evolution of sacral expansion (left) and the presence of iliac ridges (right) are mapped on the phylogeny for our sample
taxa-based topology of Gao and Wang, 2001; Frost et al., 2006; Van der Meijden et al., 2007; and Hedges et al., 2008. Character
states scored for the terminal sample taxa are illustrated on the figure and in Figures 1–3. Pie diagram shading indicates the maximum likelihood of alternative character states at each ancestral node on the phylogeny. Probabilities of basal states are indicated
for key nodes showing the high likelihood of the retention of expanded sacra and smooth ilia well into the Neobatrachia. The Triadobatrachus illustration is modified from Rage and Roček, 1986.
chia (93%) and the bases of the Hyloides (90%)
and Ranoides (82%). Flat-sided diapophyses
appear independently in six terminal taxa, all
involving unique transitions from expanded sacral
diapophyses (Pipidae, Bombinatoridae, Megophryidae, Hylidae, and two microhylids). However, only
in the Pipidae, they are completely bony as
opposed to having flat-sided cartilaginous caps.
Rod-like diapophyses appear independently in four
different terminal taxa. Judging from the high
probabilities for expanded diapophyses at preceding ancestral nodes (90, 88, and 82% for Hyloides,
Arthroleptidae, and Natatanura, respectively),
each case exhibits a saltatorial shift to rod-like
sacral diapophyses.
Smooth iliac shafts are also basal and general
for the Anura. Iliac ridges appear in the Megophryidae and in several taxa within the Neobatrachia (Eleutherodactylidae, some Leptodactyliformes, some Afrobatrachia, and Natatanura, Fig.
Journal of Morphology
160
S.M. REILLY AND M.E. JORGENSEN
6, right). Within the Neobatrachia, iliac ridges
appear with rod-like sacral diapophyses in the
Eleutherodactylidae, Leptodactylidae, and Natatanura but appear to arise earlier than rod-like
sacra in the Afrobatrachia. The Hylidae and
Microhylidae retain smooth iliac shafts. Only in
the Megophryidae are flat-sided sacra associated
with iliac ridges. The presence of iliac ridges in
some taxa with flat-sided (Megophryidae) and
expanded sacra (Hemisotidae) shows that iliac
ridges are not always diagnostic of the sagittalhinge morph as proposed by Emerson (1979, 1982).
Evolutionary patterns of urostylic traits are presented in Figure 7. A monocondylar sacro-urostylic
articulation is basal for frogs, with a 62% or better
probability in basal nodes until the Neobatrachia.
Among terminal basal taxa, bicondyly appears in
two of the Xenoanura and in Alytidae. Basal pipids
are monocondylar (Nevo, 1968), suggesting that terminal pipids shifted to fusion from monocondyly.
Bicondyly appears at a high probability (96%) at the
base of the Neobatrachia (it is lost to fusion in a
few bufonids, breviceptids, and microhylids within
Gastrophryninae and Phrynomantinae; Pugener and
Maglia, 2009). Like the pipids, some of the Anomoceola (Scaphiopodidae and some pelobatids and
megophryids; Pugener and Maglia, 2009) develop
fused urostyles from monocondylar articulations.
Smooth urostyles are found in all basal frogs
except the Megophryidae. Urostyle ridges arise
repeatedly within the Neobatrachia. In the
Hyloides, except for the Cycloramphidae and Myobatrachidae, there appears to be a widespread
transition to possession of urostylic ridges, with
half-length ridges appearing in many taxa and the
two sagittal-hinge taxa independently developing
full ridges. In the Ranoides, there are three basic
groups: 1) the Afrobatrachia are dominated by
half-length ridges (with the one sagittal-hinge
morph developing a full ridge), 2) the microhylids
primarily retain smooth urostyles, and 3) full
ridges appear in the Natatanura.
DISCUSSION
A summary of the four pelvic traits used in this
analysis is presented on the sacral diapophysealshape character tree (Fig. 8). Sacro-urostylic articulation state is simply scored on a few branches,
as bicondyly only appears in three basal terminal
taxa (rhinophrynids, pipids, and alytids) and in
the Neobatrachia. Primary locomotor states for
each family are based on Zug’s (1978), Emerson’s
(1979), and Brown and Crespo’s (2000) scoring of
locomotor modes [dedicated AQuatic (Pipidae),
Burrowing habits, Walking, Hopping (less than
eight body lengths per leap), and Jumping (more
than eight body lengths per leap) with environment (Terrestrial and Arboreal)]. The scoring of
the locomotor mode of Ascaphus and Leiopelma as
Journal of Morphology
walker/hoppers is from Essner et al. (2010). The
paleotaxa are assumed to use the basal walker/
hopper mode evident in all extant basal taxa given
their widespread possession of lateral-bender pelvic traits. We have coded the jumping taxa in bold
and the letter F after the taxon names indicating
cases of taxa in which all (F) or some (f) members
have a fused urostyle (Fig. 8).
Pelvic Designs in Relation to Locomotor
Mode in Basal Anurans
The walker/hopper mode is both basal and
general for the anura. Based on the four skeletal
characters, the early design of the frog pelvic region
is highly conserved in the basal Anura. Below the
neobatrachians, all six major frog lineages possess
expanded diapophyses, smooth ilia, and smooth
urostyles. In all terrestrial basal taxa, smooth ilia
are correlated with smooth urostyles (except in the
megophryids). In terms of locomotion, all basal taxa
use walking/hopping locomotion (except the aquatic
pipids). Thus, Emerson’s lateral-bender morph
(with monocondyly and smooth urostyles) and the
walker/hopper locomotor mode is clearly the basal
condition for the Anura. Walker/hopper-lateralbender morphs with expanded diapophyses and
smooth ilia and urostyles (***: Fig. 8) are also
widespread within the Neobatrachia (Myobatrachidae, Cycloramphidae, and two microhylids)
although they differ in that they are bicondylar.
The remaining neobatrachian walker/hoppers exhibit two other pelvic systems in which they retain
expanded sacral diapophyses, but add a half urostyle ridge (Limnodynastidae, Bufonidae, and Microhylidae: Microhylinae) or a half urostyle ridge and
iliac ridges (Ceratophryidae, Leiuperidae, Hemisotidae, and some hyperoliids).
Are bicondyly and sacro-urostylic fusion
innovations for burrowing? Patterns of sacrourostylic articulation provide a basis to hypothesize the function of the urostyle in lateral-bender
morphs and the relationship of urostyle movement
to burrowing. The most basal extant lineage (Leiopelmatidae) is monocondylar and is not known to
burrow in the soil. However, many of the burrowing taxa exhibit a strong tendency to develop ways
to limit the lateral movement of the urostyle, thus
directing muscle activity to moving the ilia and
limbs and not the urostyle. First, the xenoanuran,
alytid, and neobatrachian burrowers have bicondylar sacro-urostylic articulations. Second, the
Anomoceola (Scaphiopodidae and many pelobatids
and megophryids) have fused urostyles. Finally,
some bufonids and some microhylids (within Gastrophyninae and Phrynomantinae) add fusion to
bicondyly. Thus, in our taxonomic sample, all of
the 14 burrowing taxa have (or have some members with) limited urostylic mobility in the lateral
direction. This correlation appears to be evidence
THE EVOLUTION OF LOCOMOTION IN FROGS
161
Fig. 7. Patterns of evolution in two new osteological pelvic traits. Character states for the sacro-urostylic articulation (left) and
urostyle ridges (right) scored for the sample taxa are illustrated on the figure and in Figures 2 and 5. Maximum likelihood ancestral character state reconstructions (shading in nodes) indicate the probability of alternative states for each ancestral node on the
same phylogeny as Figure 6. Probabilities of basal states are indicated for key nodes showing shifts to bicondyly within the Xenoanura, the Alytidae, and the Neobatrachia and the high likelihood of the retention of smooth urostyles well into the Neobatrachia.
The Triadobatrachus illustration is modified from Rage and Roček, 1986.
that urostylic fusion or bicondyly (or both) may
provide an extended posterior axial anchor from
which the ilia can move relative to the body with
digging limb strokes. In addition, as mentioned
above, megophryids and many of the neobatrachian burrowers have added ridges on the ilia and/
or urostyle, which would provide additional surface area for muscles to produce larger and more
directly aligned lateral-bending movements in digging. We posit that laterally rigid urostyles may
facilitate independent and stronger lateral movements of the limbs relative to the axial column in
digging. From the wide ranging correspondence of
burrowing and traits that would limit lateral
movement of the urostyle, we propose that bicondyly may have first appeared as an adaptation to
burrowing/lateral-bending (and walking) locomotion. Thus, bicondyly may have been an exaptation
to sagittal-hinge jumping which does not appear
until well into the Neobatrachia.
Journal of Morphology
162
S.M. REILLY AND M.E. JORGENSEN
Fig. 8. Evolution of pelvic girdle designs in frogs in relation to locomotor modes. Patterns of sacral and pelvic traits (from Figs.
6 and 7) are summarized in relation to primary locomotor modes for each family from Emerson, 1979 and Zug, 1978. Bicondyly is
indicated with black bars. Locomotor modes are: AQ, dedicated aquatic (Pipidae); B, burrowing habits, W, walking, H, hopping
(less than eight body lengths per leap). Jumping forms (more than eight body lengths per leap) are divided by environment into
terrestrial jumpers (JT) and arboreal jumpers (J A). Note the generality of the basal walker/hopper traits across the phylogeny, the
convergence in traits in terrestrial jumpers (JT), and divergence in arboreal jumping systems (J A) in the Neobatrachia.
Radiation in Flat-Sided Morphs in the Anura:
Emerson’s Type 1 Sacrum Is Not One Type
There are several independent transitions to
flat-sided diapophyses (Emerson’s ‘‘Type I’’ sacra)
among frogs. The pipids are the most derived
group of frogs being dedicated aquatic swimmers
Journal of Morphology
and the only group with massive, flat, bony-sided
diapophyses fusing with a urostyle. Pipids have
many other osteological (e.g., unique lateral iliac
flanges: & in Figs. 6 and 8) and myological (e.g.,
shoulder muscles extending to the thighs) novelties associated with their fully aquatic habits and
THE EVOLUTION OF LOCOMOTION IN FROGS
extreme fore-aft sliding pelvic system (Whiting,
1961; Van Dijk, 2002).
The remaining flat-sided morphs are terrestrial
and have rounded bony diapophyses capped with
flat-sided cartilages (Fig. 1A). If not carefully evaluated, the flat shape of these cartilaginous caps
would be scored as ‘‘expanded’’ and thus lateralbender morphs. Among the taxa with cartilaginous
flat-sided sacra, there appear to be three basic
pelvic designs. First, three widely separated taxa
(Bombinatoridae and two microhylid lineages)
have cartilaginous flat-sided sacra but are basal in
that they lack iliac or urostylic ridges. Essentially,
these appear to be lateral-bender morphs with
their cartilaginous caps formed into flat sides.
Given their otherwise basic similarity to lateralbender morphs, it is not surprising that they are
walker/hoppers. Second, perhaps the most unique
pelvic design is among the basal frogs in the Megophryidae. From among its externally and ecologically similar lateral-bender-morph sister taxa in
the Anomoceola, the megophryids have shifted to
flat-sided sacra (similar to bombinatorids) with
half urostylic ridges and iliac ridges. Some are
burrowers (and have fused urostyles; Pugener and
Maglia, 2009) and the family is unique among
frogs in having intervertebral disks with ossified
centers (Frost et al., 2006). This family, like many
other taxa, uses forest floor and streamside habitats. However, it contains twice as many species
(140) as all of the rest of the extant lineages
below the Neobatrachia combined (70). It
remains to be seen why this speciose walker/hopper family is so derived in pelvic and axial design
and how its morphological novelties relate to its
great success in Southeast Asia. Finally, the last
flat-sided form is the family Hylidae, which are
climber/arboreal jumpers and have added urostylic
ridges to the system (discussed below with other
arboreal forms).
The Radiation of Jumping Locomotion in
the Neobatrachia
Figure 8 shows that a majority (14/25) of our
neobatrachian sample taxa represent a range of
different kinds of walker/hoppers with the basal
lateral-bender pelvis, some having a half urostyle
ridge. In terms of jumping frogs, there are clear
patterns of convergence in terrestrial jumpers and
divergence in pelvic traits in arboreal jumpers,
which appear well within the Neobatrachia.
Pelvic convergence in terrestrial jumpers.
One of the clearest patterns in this study is the
strong correspondence of one set of skeletal pelvic
traits with terrestrial jumping. All of the terrestrial jumpers have rod-like diapophyses and ridges
on the ilia and urostyle (Fig. 8, lll and JT).
This pattern independently appears twice in the
Hyloides (eleutherodactylids and leptodactylids)
163
and twice in the Ranoides (arthroleptids and Natatanura). All of these taxa (some previously
included together in the same taxa) resemble and
appear to jump like the ranid frogs most often
studied as the model sagittal-hinge jumping frog.
However, based on the patterns of trait change
and large shifts in probabilities on the individual
trait trees (Figs. 6 and 7), it is clear that each of
these distantly related taxa have independently
converged on the sagittal-hinge jumping system.
Although this suite of characters describes the sagittal-hinge morph and provides strong support for
the relationship between the sagittal-hinge morph
and jumping, it remains to be seen how similar
the four independently evolved terrestrial jumping
taxa are in the details of myology, motor pattern,
kinematics, and function. It seems probable that
tightly bound iliosacral joints and large dorsal
ridges (and muscles) on pelvic elements are related
to the increase in jumping ability in these frogs.
However, relative limb and body size appear to
play a role as well, as most of these taxa are large
frogs with relatively larger hindlimb muscles
(Emerson, 1978; Marsh, 1994; Choi and Park,
1996; Choi et al., 2003). Functionally, the relative
contributions to jumping of potential sagittal pelvic movements versus limb extension per se have
not been quantified in frogs. Nonetheless, we propose that the sagittal-hinge system may be an
adaptation to jumping in large terrestrial frogs.
Because mass increases as a cube, heavier frogs
may need the sagittal-hinge to raise the heavier
front end during take off and they may need a
good pelvic hinge to help fold up their longer hindlimbs for landing. However, comparisons of the
launch, aerial, and landing kinematic timing
patterns in Ascaphus, Bombina, and Lithobates
showed no difference in aerial duration despite the
fact that Lithobates jumped significantly farther
(Essner et al., 2010). Thus, the larger sagittalhinge frog must rotate its longer/heavier limb segments into landing position in the same amount of
time as the small frogs. Thus, we propose an alternative hypothesis that sagittal-hinge may actually
function in facilitating limb placement during
landing in relatively larger frogs.
One other family (Dendrobatidae) has members
converging on terrestrial jumping. The family
Dendrobatidae as we have sampled is based on
Emerson’s sample of the subfamily Dendrobatinae,
which have the basal pelvis (Fig. 8) and are
walker/hoppers (Zug, 1978). However, Zug (1978)
showed that the more basal dendrobatids (Colostethinae) are good jumpers, and our X-ray data (not
included in the present analysis) show them to
have rod-like sacra, iliac ridges, and a half urostyle ridge similar to terrestrial jumpers. Thus, the
basal dendrobatids (Colostethinae) appear to be a
fifth group to independently develop terrestrial
jumping traits and habits. Accordingly, the more
Journal of Morphology
164
S.M. REILLY AND M.E. JORGENSEN
derived poison-dart frogs (Dendrobatinae) have
reverted to basal walker/hoppers (in design and
performance) in concert with small body size, visually smaller hindlimbs, toxicity, and aposematic
coloration, all of which appear to relate to the loss
of the need for long-distance predatory escape.
Systematically, the Dendrobatidae is one of the
less resolved branches, having been historically
aligned with the Bufonidae, Ranidae, Leptodactylidae, and Arthroleptidae (Grant et al., 2006). The
presence of terrestrial jumping basally does not
support a close relationship of the Dendrobatidae
with the lateral-bender-morph Bufonidae.
Pelvic divergence in arboreal jumpers:
Four kinds of tree frogs. In contrast to the convergences seen in terrestrial jumpers, several pelvic types have moved into the trees. Three arboreal jumpers have arisen within the Ranoides, two
with expanded sacral diapophyses and one with
rod-like diapophyses. First, among the lateralbender morphs of the Microhylidae, members of
the subfamily Asterophryninae have become arboreal with the basal pelvic system traits (expanded
sacra, no iliac or urostyle ridges) except they are
bicondylar. This large radiation of small- to medium-sized Southeast Asian frogs has added intercalary cartilages and toe pads to the lateral-bender
morph and moved into the arboreal niche. Second,
the Hyperoliidae has a few walker/hopper taxa
(e.g., Kassina) but is dominated by small- to medium-sized reed and tree frogs. This family has
added iliac and half urostyle ridges to the
expanded sacrum. The third type of tree frog has
arisen from among the sagittal-hinge ancestry in
the Natatanura. The Rhacophoridae have developed intercalary cartilages and toe pads for climbing and appear to have taken the sagittal-hinge
system into the trees. The same pattern also
appears in another Natatanuran family not in our
study (Mantellidae) and in some eleutherodactylid
taxa, although they lack intercalary cartilages.
The fourth and dominant types of tree frogs are
in the Hylidae. This family, with toe pads and intercalary cartilages in the digits, is the most speciose frog family comprising nearly a sixth of all
known frogs. The hylids have the cartilaginous
flat-sided sacral diapophyses, and no iliac ridges,
but possess half ridges on the urostyle. As posited
above, the flat-sided cartilages may be a simple adaptation of the basal lateral-bender morph because
the bony diapophyses of hylids appear the same as
lateral-bender morphs and one has to look carefully for the flat-sided cartilaginous caps to score
them as a flat-sided morph. Interestingly, one
small group of hylids (Pseudacris and sister taxa)
has transitioned back to rounded cartilaginous diapophyseal caps and more terrestrial habits, but
they retain the urostyle ridge and jumping ability.
The discovery of four basic arboreal pelvic
designs has some general implications in relation
Journal of Morphology
to tree frog evolution. Although the sagittal-hinge
is tightly correlated to terrestrial jumping, the system works well in the trees as evidenced by the
huge radiation of rhacophorid tree frogs (300
sps). However, more basal pelvic designs are found
in the other three tree frog radiations that comprise a quarter of all frogs. The lateral-bender
morph (Microhylidae: Asterophryninae and Hyperoliidae) and flat-sided (Hylidae) tree frogs, in general, are smaller and have relatively longer, more
gracile hindlimbs than the sagittal-hinge frogs
(Zug, 1972; Emerson, 1978) and can attain greater
jumping distances (Zug, 1978). In fact, the best
jumpers measured to date are from the Hylidae
(Litoria: Pelodryadinae and Pseudacris and Acris:
Hylinae) in which eight species have been shown
to average from 20 to 26 body lengths per jump
compared to the high of 19.6 body lengths (Platymantis papuensis) measured in the best of 14
Ranoid jumpers (Zug, 1978). Thus, expanded or
flat-sided sacral diapophyses (5the absence of a
sagittal-hinge system) can serve as a successful
platform for long-distance jumping.
The most widely accepted explanation for differences in jumping performance in frogs is the
length of the hindlimb (Zug, 1972, 1978; Dobrowolska, 1973; Emerson, 1978, 1985, 1988; Choi and
Park, 1996; Choi et al., 2003; Gomes et al., 2009),
which reflects the time and distance through
which jumping forces act (Gray, 1968). However,
like the contribution of sagittal-hinge extension
versus limb extension in terrestrial jumpers, the
contribution of limb extension and fore-aft sliding
to arboreal jumping has not been demonstrated.
Because most tree frogs are able to jump far without a sagittal-hinge and iliac ridges, adaptations to
limb extension performance alone may be the primary driving locomotor mechanism in most tree
frogs. The contrast in the presence and absence of
iliac ridges in the terrestrial (sagittal-hinge) versus arboreal (lateral-bender and flat-sided morphs)
tree frogs, respectively, suggests that there are
fundamental differences in the amount of muscle
mass and perhaps primary directions of action in
controlling the relative movements of ilia, urostyle,
and axial column in these different tree frog
morphs. In addition, the relative amount of hindlimb musculature, muscle contractile properties,
and stored energy mechanisms may differ among
the sagittal-hinge and tree frog morphs (Emerson,
1978; Marsh, 1994; Choi and Park, 1996; Choi
et al., 2003; Roberts and Marsh, 2003). The arboreal hyperoliids illuminate another interesting
twist: they have the same expanded pelvic system
that has independently appeared in three other
walker/hopper families (Hemisotidae, Leiuperidae,
and Ceratophryidae) with ridges added to the
urostyle and ilia. This suggests that something is
functionally different about walker/hoppers that
have added ridges and the hyperoliids appear to
THE EVOLUTION OF LOCOMOTION IN FROGS
have adapted this system to arboreal jumping
without compromising walking and hopping.
The rhacophorids and hyperoliids of tropical
Africa are widely accepted to be the ecological analogs to the tropical American hylids. However, the
pelvic systems show these to be three very different kinds of tree frogs. Similarly, the rhacophorids
and hyperoliids, which comprise a majority of the
African tree frog taxa, are fundamentally different
in pelvic design, which may be related to differences in more savanna versus forest arboreality in
these taxa. In terms of systematics, in the past the
hyperoliids have been considered to be closely
related to the rhacophorids (Frost et al., 2006), but
their major pelvic differences add to support for
their separation within the Ranoides.
Finally, the Rhacophoridae and Hylidae contain
the two primary radiations of gliding tree frogs
(Duellman, 1970; Emerson and Koehl, 1990). Studies of gliding in frogs have shown that gliders from
these families are convergent in body morphology
and behavior related to aerodynamics during flight
(Emerson and Koehl, 1990; Emerson et al., 1990;
McCay, 2001). However, these studies have not
considered the influence of jumping per se (i.e.,
take-off velocity) in attaining gliding dynamics
when jumping from trees or that these gliding
families have converged on gliding locomotion
from divergent jumping systems. The hylids
appear to have adapted a more basal pelvic system
to arboreal jumping with long legs and gracile
bodies, whereas the rhacophorids appear to have
adapted the terrestrial sagittal-hinge jumping system for use in arboreal jumping. Here again,
understanding the relative contribution of limb
extension and pelvic movements to jumping in
these two forms is necessary to evaluate the influence of pelvic (if any) and limb design on launching performance.
Conclusions and Insights From Our New
Hypothesis for the Evolution of Frog
Locomotion
We propose that the patterns revealed by the
pelvic traits and the general locomotor patterns
presented in Figure 8 represent a new starting
point for the understanding of the evolution of
locomotion in frogs. In resampling Emerson’s taxa,
we have covered only 24 of 49 extant anuran families but these families represent three-fourths of
the 6,0001 frog species and all of the major radiations. We point out that assigning family-level
states to both the morphological and locomotor
traits on the basis of a few genera has its limits.
However, we have better accounted for intraspecific variation with better intraspecific sample
sizes and improved visualization of the anatomy,
and there is evidence of substantial family-level
consistency in these traits (we examined familial
165
patterns in more taxa than reported here). The
addition of information on more taxa (or use of a
different phylogeny) will not significantly change
the major pelvic patterns that have emerged in
this study, they will only add to them. We feel confident that as the first formal phylogenetic mapping of these characters in frogs, important new
patterns and insights are revealed and several
general observations can be made.
Although frogs can be categorized into flat-sided,
round-sided, and rod-like sacral shapes, the most
general observation is that there is a wider radiation in the details of overall pelvic design in anurans indicating at least seven pelvic types (Fig. 8)
rather than the original three morphs proposed by
Emerson. The dedicated aquatic frogs, which do
not appear to use lateral bending, are the only
frogs identified so far that have ossified flat-sided
diapophyses. The walker/hopper condition is both
basal and generally conserved across the phylogeny well into the Neobatrachia. Burrowing
appears to have had a canalizing effect on caudal
rigidity via bicondyly and/or fusion at the sacrourostylic joint. Furthermore, because bicondyly
evolved well before either arboreal or terrestrial
jumping, it does not appear to have evolved for
jumping but to provide axial rigidity to lateralbending behaviors.
Long-distance jumping and jumping traits do
not appear until well within the Neobatrachia.
Thus, the ‘‘sagittal-hinge jumping is primitive’’ hypothesis of Shubin and Jenkins (1995) lacks support. Instead, the terrestrial jumpers have come to
the same design independently in widely distant
lineages suggesting a strong functional canalizing
effect on the evolution of terrestrial jumping in
frogs that tend to have larger body- and relative
hindlimb muscle masses (Marsh, 1994; Choi and
Park, 1996). Because many other frogs can jump
as far or farther than sagittal-hinge frogs, one has
to question the utility of the sagittal-hinge in
jumping and look more to comparisons of other anatomical, ecological, and physiological jumping
components. Interestingly, recent comparisons of
jumping in basal and ranid frogs have shown that
the kinematics of limb movements during the aerial phase and landing are significantly different,
suggesting that folding the body and protracting
the legs for landing may be the primary functional
role of the sagittal-hinge (Essner et al., 2010).
Arboreality, on the other hand, has been accomplished in four different ways: 1) with no change
from the basal condition; 2) with the addition of
urostylic and iliac ridges; 3) with cartilaginous
flat-sided sacra; and 4) from sagittal-hinge lineages. This suggests that transitions to climbing
adaptations (most obviously, smaller mass and the
addition of toe pads), rather than pelvic design,
may drive the move into arboreality. However, relatively longer legs appear to contribute to arborJournal of Morphology
166
S.M. REILLY AND M.E. JORGENSEN
eality in both extending the reach in climbing limb
movements and in increasing arboreal jumping
ability (Marsh, 1994; Gomes et al., 2009). Arboreality has only arisen in bicondylar forms, suggesting that the benefits of stiffening the axial column,
which we proposed for burrowing and walking,
may facilitate vertical climbing as well. The Hylidae are the only group to take flat-sided sacra into
the trees. Their appearance in the hylids and their
maintenance in nearly 900 species suggest that
cartilaginous straight-sided diapophyses are somehow significant to the success of this largest arboreal radiation. However, we need to know how the
urostyle and the flat-sided sacra function in the
hylid pelvis and whether they are more important
for climbing up or jumping down.
The generality of the basal hopping frog system,
multiple convergences on the terrestrial jumping
sagittal-hinge system, and pelvic divergences of
tree frogs show a diversity of influences of pelvic
design on frog locomotion. Still, there are other
functional aspects of frog locomotion that need to
be better understood. First, kinematic analyses of
sacroiliac and urostyle movements during jumping
and landing are needed across the array of pelvic
types to begin to understand the function of the
pelvis in frogs and how it differs in walker/hoppers, terrestrial jumpers, and arboreal jumpers.
Second, comparative studies of the musculature of
the pelvic region are needed in light of differences
of sacral shape, iliac and urostyle ridges, and
mono- versus bicondyly. Third, a broader study of
limb design and function in relation to limb and
body size is needed across frogs with different pelvic designs. Hindlimb length has been shown to
scale with jumping performance in both allometric
(Zug, 1972; Emerson, 1985) and phylogenetically
corrected (Gomes et al., 2009) comparisons in
frogs. Other important features of the limb (takeoff velocity and hindlimb muscle mass, architecture, contractile properties, and enzyme activity)
have also been shown to vary among small taxonomic samples of hopping frogs, tree frogs, and
ranids (Calow and Alexander, 1973; Marsh, 1994;
Choi and Park, 1996; Lutz and Rome; 1996; Olson
and Marsh, 1998; Gillis and Biewener, 2000; Choi
et al., 2003; Roberts and Marsh, 2003). However,
these studies have not consistently related limb
features to relative hindlimb muscle mass and
body mass (Gomes et al., 2009). We need analyses
that will help us understand the differences in the
legs of a toad, a bull frog, and different tree frogs
in relation to body mass, launch velocity, and jump
distance.
Finally, we made two observations in relation to
some of Emerson’s traits. First, we could not find
consistent evidence of ligament scars for the dorsal
iliosacral ligaments of frogs. There is usually a
smooth surface at the insertion site of the dorsal
iliosacral ligaments. Second, the ilio-ilial ligament
Journal of Morphology
she used as characteristic of the fore-aft-slider
morph is present in all frogs we have examined,
albeit in a very thin state. Emerson posited that
this ligament was a thickening of the lumbodorsal
fascia forming a cuff-like band that binds the ilia
to the sacrum (Emerson and De Jongh, 1980). This
fascial cuff appears to be present in all frogs.
Thus, the loss of the dorsal iliosacral ligament,
rather than the presence of the ilio-ilial ligament,
may be the definitive ligamentous trait for the
fore-aft slider morph.
In sum, the early frogs did ‘‘leap forward, high
over it.’’ However, our analysis suggests that the
initial leap the frog bauplan afforded was a performance increase to hopping locomotion. This
may have been a significant increase ‘‘high over’’
the leaping distances of generalized ancestral and
other tetrapods but it was not a leap to sagittalhinge jumping. The generalized frog is a walker
that can hop better than most vertebrates with
some proclivity toward burrowing. Later, from a
myriad of neobatrachian walker/hopper frogs,
many lineages adopted striking patterns of convergence to increase jumping distance on land and
others followed divergent patterns to climb and
jump in the trees.
ACKNOWLEDGMENTS
The authors thank Sarah Gutzwiler, Brian Folt,
and Ashley Micelli for assistance with radiographic data collection and management. Joe Eastman provided radiographic, film development
resources and advice. Jeff Brown and the OUCOM
Communication Department provided digital scanning facilities for radiographs. They are grateful to
the following museums and collections staff for
X-ray assistance and loan material (Appendix):
Linda Trueb, Rafe Brown, and Andrew Campbell
in the Department of Herpetology at the University of Kansas; Alan Resetar at the Field Museum;
Jim McGuire and Carol Spencer at the Museum of
Vertebrate Zoology; Robert Drewes and Jens Vindum at the California Academy of Sciences; and
Jonathan Losos and José Rosado at the Museum
of Comparative Zoology. Larry Witmer and Ryan
Ridgely of the OU micro-CT facility provided assistance with CT scanning. Finally, they thank Rick
Essner for many valuable discussions and insights
into basal and crown frogs and how they differ in
locomotion.
LITERATURE CITED
Abourachid A, Green DM. 1999. Origins of the frog-kick? Alternate-leg swimming in primitive frogs, families Leiopelmatidae
and Ascaphidae. J Herpetol 33:657–663.
Báez AM, Basso NG. 1996. The earliest known frogs of the Jurassic of South America: Review and cladistic appraisal of
their relationship. Münchner Geowiss Abh A 30:131–158.
THE EVOLUTION OF LOCOMOTION IN FROGS
Báez AM, Nicoli L. 2004. A new look at an old frog: The Jurassic Notobatrachus Rieg from Patagonia. Ameghiniana 41:257–
270.
Brown LE, Crespo EG. 2000. The burrowing behavior of the
midwife toads Alytes cisternasii and Alytes obstetricans
(Anura, Discoglossidae). Alytes 17:101–113.
Calow LJ, Alexander RMcn. 1973. A mechanical analysis of the
hind leg of a frog (Rana temporaria). J Zool Lond 171:293–
321.
Choi I, Park K. 1996. Variations in take-off velocity of anuran
amphibians: Relation to morphology, muscle contractile function and enzyme activity. Comp Biochem Physiol A 113:393–
400.
Choi I, Shim JH, Ricklefs RE. 2003. Morphometric relationships
of take-off speed in anuran amphibians. J Exp Biol A 299:99–
102.
Dobrowolska H. 1973. Body part proportions in relation to
mode of locomotion in anurans. Zool Polon 23:59–108.
Duellman WE. 1970. The hylid frogs of Middle America.
Monogr Mus Nat Hist Univ Kansas 1:1–753.
Duellman WE, Trueb L. 1994. The Biology of Amphibians. Baltimore, MD: Johns Hopkins University Press.
Emerson SB. 1978. Allometry and jumping in frogs: Helping
the twain to meet. Evolution 32:551–564.
Emerson SB. 1979. The iliosacral articulation in frogs: Form
and function. Biol J Linn Soc 11:153–168.
Emerson SB. 1982. Frog postcranial morphology: Identification
of a functional complex. Copeia 3:603–613.
Emerson SB. 1985. Jumping and leaping. In: Hildebrand M,
Bramble DM, Leim KF, Wake DB, editors. Functional Vertebrate Anatomy. Cambridge, MA: Belknap Press. pp 58–72.
Emerson SB. 1988. Convergence and morphological constraint
in frogs: Variation in postcranial morphology. Fieldiana 43:1–
19.
Emerson SB, De Jongh HJ. 1980. Muscle activity at the iliosacral articulation in frogs. J Morphol 166:129–144.
Emerson SB, Koehl MAR. 1990. The interaction of behavioral
and morphological change in the evolution of a novel locomotor type: ‘‘Flying’’ frogs. Evolution 44:1931–1946.
Emerson SB, Travis J, Koehl MAR. 1990. Functional complexes,
and additivity in performance: A test case with ‘flying’ frogs.
Evolution 44:2153–2157.
Essner RL, Suffian DJ, Bishop PJ, Reilly SM. 2010. Landing in
basal frogs: Evidence of saltational patterns in the evolution
of anuran locomotion. Naturwissenschaften DOI: 10.1007/
s00114-010-0697-4.
Estes R, Reig OA. 1973. The early fossil record of frogs: A
review of the evidence. In: Vial JL, editor. Evolutionary Biology of the Anurans: Contemporary Research on Major Problems. Columbia, MO: University of Missouri Press. pp 11–63.
Evans SE, Borsuk-Bialynicka M. 1998. A stem-group frog from
the early Triassic of Poland. Acto Palaento Pol 43:573–580.
Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad
CFB, de Sa’ RO, Channing A, Wilkinson M, Donnellan SC,
Raxworthy CJ, Campbell JA, Blotto BL, Moler P, Drewes RC,
Nussbaum RA, Lynch JD, Green DM, Wheeler WC. 2006. The
amphibian tree of life. Bull Am Mus Nat Hist 297:1–370.
Gao K-Q, Wang Y. 2001. Mesozoic anurans from Lianoning
Province, China, and phylogenetic relationships of archeobatrachian anuran clades. J Vert Paleontol 21:460–473.
Gao K-Q, Chen S. 2004. A new frog (Amphibia: Anura) from the
lower Cretaceous of western Liaoning, China. Cretac Res
25:761–769.
Gaupp E. 1896. Anatomie des Frosches. I. Lehre vom Skelet
und vom Muskelsystem. Braunschweig: Friedrich Vieweg und
Sohn.
Gillis GB, Biewener AA. 2000. Hindlimb extensor muscle function during jumping and swimming in the toad (Bufo marinus). J Exp Biol 203:3547–3563.
Gomes FR, Rezende EL, Grizante MB, Navas CA. 2009. The
evolution of jumping performance in anurans: Morphological
correlates and ecological implications. J Evol Biol 22:1088–
1097.
167
Grant T, Frost DR, Caldwell JP, Gagliardo R, Haddad CFB,
Kok PJR, Means BD, Noonan BP, Schargel W, Wheeler WC.
2006. Phylogenetic systematics of dart-poison frogs and their
relatives (Anura: Athesphatanura: Dendrobatidae). Bull Am
Mus Nat Hist 299:1–262.
Gray J. 1968. Animal Locomotion. London: William Cloes and
Sons, Ltd. 479 p.
Green TL. 1931. On the pelvis of the Anura: A study in adaptation and recapitulation. Proc Zool Soc Lond 1931:1259–1291.
Hedges SB, Duellman WE, Heinicke MP. 2008. New World
direct-developing frogs (Anura: Terrarana): Molecular phylogeny, classification, biogeography, and conservation. Zootaxa
1737:1–182.
Jenkins FA, Shubin NH. 1998. Prosalirus bitis and the anuran
caudopelvic mechanism. J Vert Paleontol 18:495–510.
Kargo WJ, Nelson F, Rome C. 2002. Jumping in frogs: Assessing the design of the skeletal system by an anatomically realistic modeling and forward dynamic simulation. J Exp Biol
205:1683–1702.
Lutz GJ, Rome LC. 1996. Muscle function during jumping in
frogs. I. Sarcomere length, change, EMG pattern, and jumping performance. Am J Physiol 271:C563–C570.
Maddison WP, Maddison DR. 2009. Mesquite: A Modular System for Evolutionary Analysis, Version 2.72. Available
at:http://mesquiteproject.org.
Marsh RL. 1994. Jumping ability of anuran amphibians. Adv
Vet Sci Comp Med 38:51–111.
McCay MG. 2001. Aerodynamic stability and maneuverability
of the gliding frog Polypedates dennysi. J Exp Biol 204:2817–
2826.
Nauwelaerts S, Aerts P. 2002. Two distinct gait types in swimming frogs. J Zool Lond 258:183–188.
Nevo E. 1968. Pipid frogs from the early Cretaceous of Israel
and pipid evolution. Bull Mus Comp Zool Harvard 136:255–
318.
Olson JM, Marsh RL. 1998. Activation patterns and length
changes in hindlimb muscles of the bullfrog Rana catesbiana
during jumping. J Exp Biol 201:2763–2777.
Přikryl T, Aerts P, Havelková P, Herrel A, Roček Z. 2009. Pelvic
and thigh musculature in frogs (Anura) and origin of anuran
jumping locomotion. J Anat 214:100–139.
Pugener LA. 2002. The vertebral column and spinal nerves of
Anurans [Dissertation]. Lawrence, KS: University of Kansas.480p.
Pugener LA, Maglia AM. 2009. Developmental evolution of the
anuran sacro-urostylic complex. SA J Herpetol 4:193–209.
Rage JC, Roček Z. 1986. Triadobatrachus revisited. In: Roček Z,
editor. Studies in Herpetology. Prague: Charles University. pp
255–258.
Rage JC, Roček Z. 1989. Redescription of Triadobatrachus massinoti (Piveteau, 1936) an anuran amphibian from the early
Triassic. Palaeontographica A 206:1–16.
Ritland RM. 1955. Studies on the postcranial morphology of
Ascaphus truei. II. Myology. J Morphol 97:215–282.
Roberts TJ, Marsh RL. 2003. Probing the limits of muscle powered accelerations: Lessons from jumping bullfrogs. J Exp
Biol 206:2567–2580.
Roček Z. 2008. The late Cretaceous frog Gobiates from Central
Asia: Its evolutionary status and possible phylogenetic relationships. Cretac Res 29:577–591.
Roček Z, Nessov LA. 1993. Cretaceous anurans from Central
Asia. Palaeontographica A 226:1–54.
Roelants K, Bossuyt F. 2005. Archeobatrachian paraphyly and
pangean diversification of crown group frogs. Syst Biol
54:111–126.
Sanchiz FB. 1986. A reconstruction of the Anuran locomotor
synthetotype. In: Roček Z, editor. Studies in Herpetology.
Prague: Charles University. pp 111–115.
Schluter D, Price T, Mooers AO, Ludwig D. 1997. Likelihood of
ancestor states in adaptive radiation. Evolution 51:1699–
1711.
Shubin NH, Jenkins FA. 1995. An early Jurassic jumping frog.
Nature 377:49–52.
Journal of Morphology
168
S.M. REILLY AND M.E. JORGENSEN
Stephenson EW. 1952. The vertebral column and appendicular
skeleton of Leiopelma hochstetteri Fitzinger. Trans R Soc New
Zeal 79:601–613.
Twain M. 1867. The Celebrated Jumping Frog of Calaveras
County. New York: C.H. Webb. 198 p.
Van der Meijden A, Vences M, Hoegg S, Biostel R, Channing A,
Meyer A. 2007. Nuclear phylogeny of narrow-mouthed toads
(Family Microhylidae) and a discussion of competing hypotheses concerning their biogeographical origins. Mol Phylogenet
Evol 44:1017–1030.
Van Dijk DE. 2002. Longitudinal sliding articulations in pipid
frogs. S Afr J Sci 98:555–556.
Whiting HP. 1961. Pelvic girdle in amphibian locomotion. Symp
Zool Soc Lond 5:43–57.
Zug GR. 1972. Anuran locomotion: Structure and function. I.
Preliminary observations on relation between jumping and
osteometrics of appendicular and post-axial skeleton. Copeia
4:613–624.
Zug GR. 1978. Anuran Locomotion—Structure and function. II.
Jumping performance of semiaquatic, terrestrial, and arboreal frogs. Smiths Contr Zool 276:1–31.
APPENDIX
Material examined. Specimens are from the following collections: CAS, California Academy of Sciences; FMNH, Field Museum of Natural History; KU, Natural History Museum, University of Kansas; MCZ, Museum of Comparative Zoology, Harvard University; MEJ, Michael E. Jorgensen personal
collection; MVZ, Museum of Vertebrate Zoology, University of
California, Berkeley. Asterisks indicate micro-CT specimens.
Alytidae: Alytes obstetricans, MVZ148850, 148851, 148867,
148874, 148875; Discoglossus pictus, MVZ162442, 162446,
162449, 162451, 162456. Arthroleptidae: Cardioglossa leucomystax, MCZ46624, 46627, 46629, 46631, 46623. Bombinatoridae: Bombina maxima, FMNH232977, 49522, 49520, 49519,
232978; Bombina orientalis, MEJ*. Bufonidae: Rhinella marinus, MEJ; MCZ135098, 135099, 135097, 110976, 110979;
Anaxyrus americanus, MEJ*; Rhaebo haematiticus, KU32601,
32602, 32604, 32606, 42688, 102130; Epidalea calamita,
CAS27311, 87109, 98080, CAS-SUA21701; Atelopus spumarius,
KU211676*, 211677, 211680, 211682, 212530; Melanophryniscus
stelzneri, KU93181, 179536, 197288, 197289, 197290; Pedostibes
hosii, FMNH148055, 148058*, 148057, 148050, 148053. Ceratophryidae (Telmatobiinae): Telmatobius brevipes, KU212436,
212440, 212415, 212445, 212439. Cycloramphidae: Rhinoderma darwinii, KU161544, 161546, 161540, 161538, 161539,
161533*. Dendrobatidae: Dendrobates auratus, KU33091,
36052, 36053, 36057, 36350; Oophaga pumilio, MEJ*;
KU33038, 33042, 33043, 33057, 65295. Eleutherodactilidae:
Eleutherodactylus coqui, KU180536, 180503, 180635, 180517,
180525, 180533. Hemisotidae:
Hemisus marmoratus,
CAS160298, 160299, 160300, 160301, 160336; MEJ*. Hylidae
(Hylinae): Hyla cinerea, MEJ; Hyla versicolor, MEJ; Smilisca
baudinii, KU156962, 156961, 296164, 296160, 296165, 78466;
Journal of Morphology
Trachycephalus jordani, KU146598, 202747, 164482, 132461,
146591, 164489; Triprion petasatus, KU296254, 71448, 71446,
296252*, 296292, 296289; Pseudacris triseriata, KU39267,
39260, 224624, 39291, 39302, 224625. Hylidae (Phyllomedusinae): Agalychnis callidryas, KU86497, 86480, 86481, 86488,
86499, 86502; Pachymedusa dachnicolor, KU57921, 57923,
57924, 57927, 57920, MEJ*; Phyllomedusa sauvagii, MEJ*.
Hylidae (Pelodryadinae): Litoria nasuta, KU136338, 133653,
133655, 133656, 133657; CAS78621*, 78616, 78594. Hyperoliidae: Kassina senegalensis, CAS146397, 146401, 151196,
151197, 151198; Hyperolius lateralis, CAS180144, 180145,
180146, 180147, 180149. Leiopelmatidae: Ascaphus montanus,
CAS175151,
175159*,
175153;
Ascaphus
truei,
MVZ190814*, 190815, 190816, 190817, 190818; CAS187926,
179037, 187927; Leiopelma hochstetteri, CAS6709, 6707;
FMNH195489*, 58912, 58210, 58212. Leiuperidae: Engystomops pustulosus, MCZ9253, 9252, 9263, 9256, 1401. Leptodactylidae: Leptodactylus pentadactylus, KU100354, 25714, 65707,
30407, 65709, 33165; Leptodactylus gracilis, MEJ*; Paratelmatobius lutzii, KU92977, 92978, 92980*; MCZ64345. Limnodynastidae: Notaden bennetti, FMNH97662, 97661, 97660,
97657,
97659.
Megophryidae:
Megophrys
nasuta,
FMNH156560, 156557, 156556, 148300, 148299; Ophryophryne
microstoma, MVZ223701*, 223706, 223709, 223715, 223719.
Microhylidae (Asterophryninae): Cophixalus cheesmanae,
MCZ81607, 98838, 98839, 98848, 98888. Microhylidae
(Microhylinae): Microhyla berdmorei, MCZ132422, 132478,
132479, 132480, 132481; Kaloula pulchra, KU296869, 312761,
296846, 222673, 222672; Glyphoglossus molossus, MCZ23413,
23414, 4863, 4864; KU312757*; Chaperina fusca, KU309555,
309548, 311389, 309549*, 309545. Microhylidae (Phrynomerinae): Phrynomantis bifasciatus, KU207509, 195791, 195792,
173022, 173024; MEJ*. Microhylidae (Gastrophryninae):
Gastrophryne carolinensis, KU154170, 155022, 154167, 154169,
154168; Hypopachus variolosus, MCZ26390, 26394, 26532,
26533, 21312; Dasypops schirchi, KU93249, 93250*; MCZ58409,
52170, 58410. Microhylidae (Kalophryninae): Kalophrynus
pleurostigma, KU301847, 309650, 301848, 309970*, 309971.
Microhylidae: Myersiella subnigra, KU93262*. Myobatrachidae: Pseudophryne bibronii, MCZ87311, 84403, 83712, 84405,
84398; Myobatrachus gouldii, MCZ58816, 18364, 18363, 18362;
KU125359*. Pelobatidae: Pelobates cultripes, CAS156259,
156260, 156261, 156262. Pipidae: Xenopus laevis, MEJ; Pipa
pipa, MCZ56277, 56278, 57341, 85574, 85575, 85576; Pseudhymenochirus merlini, KU207823, 207820, 207826, 207825*,
207817. Ptychadenidae: Ptychadena anchietae, KU196060,
196062*, 196067, 196058, 196061; Hildebrandia ornata,
CAS154657, 154658, 202702, 202703. Ranidae: Lithobates
pipiens, MEJ*; Lithobates catesbeianus, MEJ; Amolops hosii,
KU155672, 155667*, 155668; Meristogenys jerboa, KU155612*,
155604, 155607, 155606, 155610. Rhacophoridae: Rhacophorus viridis, CAS23754, 23755, 23765, 23769, 23772; Rhacophorus chenfui, KU311851, 311853, 311852*, 311846, 311849; Chiromantis xerampelina, KU195913, 195919, 195922*, 195917,
195915. Rhinophrynidae: Rhinophrynus dorsalis, KU86643,
86649, 86639, 86642, 86644*, 86645, 86646. Scaphiopodidae:
Scaphiopus hammondii, MEJ*; MCZ44381, 44390, 44388,
44391, 44380.