Convergently evolved muscle architecture enables high-performance ballistic movement in salamanders

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.