Movements of vastly different performance have similar underlying muscle physiology

Abstract

Many animals use elastic-recoil mechanisms to power extreme movements, achieving levels of performance that would not be possible using muscle power alone. Contractile performance of vertebrate muscle depends strongly on temperature, but the release of energy from elastic structures is far less thermally dependent, thus elastic recoil confers thermal robustness to whole-animal performance. Here we explore the role that muscle contractile properties play in the differences in performance and thermal robustness between elastic and non-elastic systems by examining muscle from two species of plethodontid salamanders that use elastically powered tongue projection to capture prey and one that uses non-elastic tongue projection. In species with elastic mechanisms, tongue projection is characterized by higher mechanical power output and thermal robustness compared with tongue projection of closely related genera with non-elastic mechanisms. In vitro and in situ muscle experiments reveal that species differ in their muscle contractile properties, but these patterns do not predict the performance differences between elastic and non-elastic tongue projection. Overall, salamander tongue muscles are similar to other vertebrate muscles in contractile performance and thermal sensitivity. We conclude that changes in the tongue-projection mechanism, specifically the elaboration of elastic structures, are responsible for high performance and thermal robustness in species with elastic tongue projection. This suggests that the evolution of high-performance and thermally robust elastic-recoil mechanisms can occur via relatively simple changes to morphology, while muscle contractile properties remain relatively unchanged.