Joint angular excursions during cyclical behaviors differ between tetrapod feeding and locomotor systems

Abstract

Tetrapod musculoskeletal diversity is usually studied separately in feeding and locomotor systems. However, comparisons between these systems promise important insight into how natural selection deploys the same basic musculoskeletal toolkit—connective tissues, bones, nerves and skeletal muscle—to meet the differing performance criteria of feeding and locomotion. In this study, we compare average joint angular excursions during cyclic behaviors– chewing, walking and running–in a phylogenetic context to explore differences in the optimality criteria of these two systems. Across 111 tetrapod species, average limb-joint angular excursions during cyclic locomotion are greater and more evolutionarily labile than those of the jaw joint during cyclic chewing. We argue that these findings reflect fundamental functional dichotomies between tetrapod locomotor and feeding systems. Tetrapod chewing systems are optimized for precise application of force over a narrower, more controlled and predictable range of displacements, the principal aim being to fracture the substrate, the size and mechanical properties of which are controlled at ingestion and further reduced and homogenized (respectively) by the chewing process. In contrast, tetrapod limbed locomotor systems are optimized for fast and energetically efficient application of force over a wider and less predictable range of displacements, the principal aim being to move the organism at varying speeds relative to a substrate whose geometry and mechanical properties need not become more homogenous as locomotion proceeds. Hence, the evolution of tetrapod locomotor systems has been accompanied by an increasing diversity of limb-joint excursions, as tetrapods have expanded across a range of locomotor substrates and environments.