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 sagittal-hinge-type pelvis posited to be related to long-distance jumping performance. The most basal living (Ascaphus) and fossil (Prosalirus) frogs are described as sagittal-hinge 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 ancestral-character 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 lateral-bending behaviors rather than sagittal bending.
Frogs are one of the most speciose groups of vertebrate tetrapods (> 6200sp) with a diverse array of locomotor behaviours. Despite the impressive diversity in frog locomotor behaviours, there remains a paucity of information on the relationship between skeletal variation and locomotor mode in frogs and the evolutionary patterns in which these relationships are framed across the frog phylogeny. Our current understanding of the evolution of frog locomotion shows that hopping transitioned into jumping within the Neobatrachia where a variety of pelvic/hindlimb length patterns and locomotor niches have appeared, but this has yet to be studied over a broad taxonomic sample of frogs. Although limb length remains as the primary predictor of leaping performance, pelvic and sacral morphometrics have not been quantified in relation to limb proportions, body size and locomotor mode and previous studies have not sampled more than 24 families. We present a large-scale phylogenetic comparison of skeletal morphometrics in relation to locomotor mode in 188 genera from 37 families. Osteological variation in limb/pelvic girdle morphometrics and pelvic traits that are posited to be associated with locomotor mode were analysed to identify which aspects of the frog skeleton are the best descriptors of locomotor mode. Our results, contrary to previous work, reveal that the greatest axis of variation in frogs is represented by the shape of the sacrum with two pelvic morphologies evident in qualitative and quantitative ancestral trait reconstructions. Limb morphology was not significantly different across most locomotor modes, but we identified several outliers in hindlimb phylomorphospace. Patterns of sacral evolution together with hindlimb length outliers reveal how the general bauplan of this successful group of vertebrate tetrapods is constrained, has radiated and has converged on certain phenotypes to fill an array of locomotor modes.
Summary While most frogs maximize jump distance as an escape behaviour, toads have traded jump distance for endurance with a strategy of hopping repeatedly. This strategy has enabled toads to expand across the continents as one of the most diverse groups of anurans. Multiple studies have revealed physiological endurance adaptations for sustained hopping in toads, however, the kinematics of their sequential hopping behaviour, per se, has not been studied. We compared kinematics and forces of single hops and multiple hopping sequences and quantified field performance of hopping behaviours in free ranging toads of three species and discovered a novel aspect of locomotion adaptation that adds another facet to their exceptional terrestrial locomotor abilities. We found that bouts of repeated hopping are actually a series of bounding strides where toads rotate on their hands and then land on their extended their feet and jump again without stopping. In addition, free‐ranging toads appear to use bounding locomotion more frequently than single hops. Bounding in toads has the advantage of maintaining velocity and producing longer jump distances. In comparison to single hops, cyclic bounding steps reduce energy expenditure and appear to provide limb loading dynamics better suited for potential cycling of elastic energy from stride to stride than would be possible with repeated single hops. This is the first case of the common use of a bounding gait outside of mammals. Bounding adds a key terrestrial locomotor trait to the toad's phenotype that may help explain their history of global expansion and the challenges to modern faunas as introduced toads rapidly invade new ecosystems today.
The evolutionary origin of Lissamphibia likely involved heterochrony, as demonstrated by the biphasic lifestyles of most extant orders, differences between Anura (with tadpole-to-froglet metamorphosis) and Urodela (which lack strongly defined metamorphosis), and the appearance of direct development among separate lineages of frogs. Patterns in the timing of appearance of skeletal elements (i.e., ossification sequence data) represent a possible source of information for understanding the origin of Lissamphibia, and with the advent of analytical methods to directly optimize these data onto known phylogenies, there has been a renewed interest in assessing the role of changes in these developmental events. However, little attention has been given to the potential impact of variation in ossification sequence data--this is particularly surprising given that different criteria for collecting these data have been employed. Herein, new and previously published ossification data are compiled and all pairs of data for same-species comparisons are selected. Analyses are run to assess the impact of using data that were collected by different methodologies: (1) wild- versus lab-raised animals; (2) different criteria for recognizing timing of ossification; and (3) randomly selecting ossification sequences for species from which multiple studies have been published, but for which the data were collected by different criteria. Parsimov-based genetic inference is utilized to map ossification sequence data onto an existing phylogeny to reconstruct ancestral sequences of ossification and infer instances of heterochrony. All analyses succeeded in optimizing sequence data on internal nodes and instances of heterochrony were identified. However, among all analyses little congruence was found in reconstructed ancestral sequences or among inferred instances of heterochrony. These results indicate a high degree of variation in timing of ossification, and suggest a cautionary note about use of these data, particularly given that in most instances issues associated with the original sources of data (e.g., wild- vs. lab-raised animals; or criteria for identification of earliest ossification) are not addressed. Potential sources of variation in the original data are discussed and may explain the incongruence observed here.
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