The diversity and evolution of locomotor muscle properties in anurans

Abstract

Anuran jumping is a model system for linking muscle physiology to organismal performance. However, anuran species display substantial diversity in their locomotion, with some species performing powerful leaps from riverbanks or tree branches, while other species move predominantly via swimming, short hops or even diagonal-sequence gaits. Furthermore, many anurans with similar locomotion and morphology are actually convergent (e.g. multiple independent evolutions of 'tree frogs'), while closely related species may differ drastically, as with the walking toad (Melanophryniscus stelzneri) and bullfrog-like river toad (Phrynoides aspera) compared with other Bufonid toads. These multiple independent evolutionary changes in locomotion allow us to test the hypothesis that evolutionary increases in locomotor performance will be linked to the evolution of faster, high-power muscles. I tested the jumping, swimming and walking (when applicable) performance of 14 species of anurans and one salamander, followed by measurement of the contractile properties of the semimembranosus and plantaris longus muscles and anatomical measurements, using phylogenetic comparative methods. I found that increased jumping performance correlated to muscle contractile properties associated with muscle speed (e.g. time to peak tetanus, maximum shortening speed, peak isotonic power), and was tightly linked to relevant anatomical traits (e.g. leg length, muscle mass). Swimming performance was not correlated to jumping, and was correlated with fewer anatomical and muscular variables. Thus, muscle properties evolve along with changes in anatomy to produce differences in overall locomotor performance.

Morphological and kinematic specializations of walking frogs

“…PGLS regression provides a better fit of the data compared with a standard ANCOVA, and indicate frogs specialized in quadrupedal walking have significantly reduced asymmetry in fore‐ and hindlimb lengths compared with other anurans (). This pattern is consistent with findings that suggest walking species tend to have shorter hindlimbs relative to snout vent length (Astley, ). Our analysis indicates fore‐ to hindlimb length ratios in our walking frogs are similar to those measured in small cursorial mammals (Figure ; Biewener, ).…”

“…As seen in another specialized anuran walker, K. maculata maintains average jumping capabilities in comparison with other anurans (Porro, Collings, Eberhard, Chadwick, & Richards, ). In contrast, Astley () found walkers tend to have inferior jump performance and shorter hindlimb lengths relative to body length. Since asymmetry in limb length appears to be maintained to preserve jumping performance as a predator avoidance strategy, then quadrupedal walkers need to make kinematic adjustments to accommodate their body plan.…”

“…We collected all 3D video kinematic data under standardized conditions at approximately 232 ° C at UCI and 282 ° C at Brown University. In spite of temperature differences, there was some overlap in walking speed between the K. senegalensis trials in this study and those in Astley, . We recorded the 3D kinematics of quadrupedal walking events for each species with two high‐speed video cameras.…”

“…bifasciatus , which we rarely observed jump (personal observation). Although some other species of anurans will walk on rare occasions, this behavior is extremely infrequent and difficult to elicit consistently, particularly for repeated cycles; prior experiments by one author failed to produce walking behavior in numerous other species in the lab (Astley, ). Although the rarer three species had lower sample sizes, we filmed a number of trials per individual within a species to reduce intraspecific error via repeated‐measures statistics (see Table ).…”

Phylogenetic patterns and correlation of key structures for jumping: bone crests and cross‐sectional areas of muscles in Leptodactylus (Anura, Leptodactylidae)

“…The relationship between locomotor mode and morphological diversity in anurans has been little explored from a comparative perspective (Zug, , ; Emerson, ) and only in the last years has an explicit phylogenetic framework been incorporated (Nauwelaerts et al. ; Reilly & Jorgensen, ; Jorgensen & Reilly, ; Astley, ). At a more exclusive level, research is even scarcer, e.g.…”