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.
Elastically powered ballistic movements, such as tongue projection, are common in nature, likely due to benefits such as increased acceleration and distance of movement, and decreased thermal sensitivity imparted by elastic mechanisms. Within Plethodontidae, both muscle‐powered and elastically powered ballistic tongue projection occur. Thus, we examine how elastically powered ballistic tongue projection morphology has evolved from muscle powered projection at the level of the projector muscles (m. subarcualis rectus [SAR]). We find that two main SAR morphologies have evolved within Plethodontidae. The first SAR morphology is conducive to elastically powered ballistic projection. This ballistic SAR morphology has evolved multiple, independent times within Plethodontidae, and results from the correlated evolution of several traits including increased collagen aponeuroses, larger SAR muscles, and the loss of inner myofibers attaching directly to the tongue skeleton. While the independent evolution of ballistic SAR morphology has arrived at a similar anatomical design, other tongue structures such as tongue attachment and skeleton folding type varies among species with a ballistic SAR morphology. The second morphology is conducive to muscle‐powered projection and is similar to morphology found in an outgroup, Salamandridae. The SAR of these species have inner myofibers that attach to the tongue skeleton, limiting projection distance, coupled with reduced collagen aponeuroses present in relatively small projector muscles. This SAR morphology has likely been retained from ancestors or may be related to feeding ecology. Overall, a ballistic SAR morphology has evolved repeatedly and independently due to the correlated evolution of several SAR traits, including the loss of inner myofibers, which is likely a defining feature of ballistic projection.
more » « less- PAR ID:
- 10458717
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Journal of Morphology
- Volume:
- 281
- Issue:
- 2
- ISSN:
- 0362-2525
- Page Range / eLocation ID:
- p. 196-212
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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