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

Significance Ballistic tongue projection in lungless salamanders displays both extreme performance and thermal robustness, with the power of projection far exceeding the available muscle power even at low body temperatures. Our comparative analysis reveals that relatively minor changes in the musculoskeletal morphology of the tongue apparatus and in the timing of muscle activation have, through evolutionary time, transformed a muscle-powered system with modest performance and high thermal sensitivity into a spring-powered system with extreme performance and thermal robustness, in parallel in both major groups of this largest family of salamanders. High performance and thermal robustness evolve together, indicating they are both properties of the same elastic-recoil, “bow-and-arrow” mechanism. Similar evolutionary patterns may be found in other ectothermic animals with extreme performance.