Differences in muscle mechanics underlie divergent optimality criteria between feeding and locomotor systems

Tetrapod musculoskeletal diversity is usually studied separately in feeding and locomotor systems. However, direct 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. Recent studies using this approach have proposed that the feeding system is optimized for precise application of high forces and the locomotor system is optimized for wide and rapid joint excursions for minimal energetic expenditure. If this hypothesis is correct, then it stands to reason that other anatomical and biomechanical variables within the feeding and locomotor systems should reflect these diverging functions. To test this hypothesis, we compared muscle moment arm lengths, mechanical advantages, and force vector orientations of two jaw elevator muscles (m. temporalis and m. superficial masseter), an elbow flexor (m. brachialis) and extensor (m. triceps- lateral head), and a knee flexor (m. biceps femoris-short head) and extensor (m. vastus lateralis) across 18 species of primates. Our results show that muscles of the feeding system are more orthogonally oriented relative to the resistance arm (mandible) and operate at relatively large moment arms and mechanical advantages. Moreover, these variables show relatively little change across the range of jaw excursion. In contrast, the representative muscles of the locomotor system have much smaller mechanical advantages and, depending on joint position, smaller muscle moment arm lengths and almost parallel orientations relative to the resistance arm. These patterns are consistent regardless of phylogeny, body mass, locomotor mode, and feeding specialization. We argue that these findings reflect fundamental functional dichotomies between tetrapod locomotor and feeding systems. By organizing muscles in a manner such that moment arms and mechanical advantage are relatively small, the locomotor system can produce broad joint excursions and high angular velocities with only small muscular contraction. As such, the anatomical organization of muscles within the limbs allows striding animals to move relatively rapidly and with minimal energetic expenditure. In contrast, the anatomical configuration of muscles in the feeding system, at least m. superficial masseter and m. temporalis, favors their force-producing capacity at the expense of excursion and velocity.