Evolution of a high-performance and functionally robust musculoskeletal system in salamanders

Abstract

The evolution of ballistic tongue projection in plethodontid salamanders—a high-performance and thermally robust musculoskeletal system—is ideal for examining how the components required for extreme performance in animal movement are assembled in evolution. Our comparative data on whole-organism performance measured across a range of temperatures and the musculoskeletal morphology of the tongue apparatus were examined in a phylogenetic framework and combined with data on muscle contractile physiology and neural control. Our analysis reveals that relatively minor evolutionary changes in morphology and neural control have transformed a muscle-powered system with modest performance and high thermal sensitivity into a spring-powered system with extreme performance and functional robustness in the face of evolutionarily conserved muscle contractile physiology. Furthermore, these changes have occurred in parallel in both major clades of this largest family of salamanders. We also find that high-performance tongue projection that exceeds available muscle power and thermal robustness of performance coevolve, both being emergent properties of the same elastic-recoil mechanism. Among the taxa examined, we find muscle-powered and fully fledged elastic systems with enormous performance differences, but no intermediate forms, suggesting that incipient elastic mechanisms do not persist in evolutionary time. A growing body of data from other elastic systems suggests that similar coevolution of traits may be found in other ectothermic animals with high performance, particularly those for which thermoregulation is challenging or ecologically costly.