Got rhythm? Rhythmicity differences reflect different optimality criteria in feeding and locomotor systems

Abstract

Evolutionary analyses of joint kinematics and muscle mechanics suggest that, during cyclic behaviors, tetrapod feeding systems are optimized for precise application of forces over small displacements during chewing, whereas locomotor systems are more optimized for large and rapid joint excursions during walking and running. If this hypothesis is correct, then it stands to reason that other biomechanical variables in the feeding and locomotor systems should also reflect these divergent functions. We compared rhythmicity of cyclic jaw and limb movements in feeding and locomotor systems in 261 tetrapod species in a phylogenetic context.Accounting for potential confounding variables, our analyses reveal higher rhythmicity of cyclic movements of the limbs than of the jaw. Higher rhythmicity in the locomotor system corroborates a hypothesis of stronger optimization for energetic efficiency: deviation from the limbs' natural frequency results in greater variability of center of mass movements and limb inertial changes, and therefore more work by limb muscles. Relatively lower rhythmicity in the feeding system may be a consequence of the necessity to prevent tooth breakage and wear, the greater complexity of coordination with tongue movements, and/or a greater emphasis on energy storage in elastic elements rather than the kinetics of limb movement.

Rhythmic chew cycles with distinct fast and slow phases are ancestral to gnathostomes

“…As groups, fishes and salamanders chew rhythmically (23.7 ± 2.1% and 21.2 ± 3.2%, respectively), even compared to mammals (23.05 ± 12.19; n = 78 [8]). A recent analysis of chew and locomotion cycle CVs for six salamander species reported a significantly higher chewing grand average (50.44 ± 33.12%) [50] than our data for the same six species (18.55 ± 2.53%), a difference that may be due to small sample sizes in that study. In that context, it is important to note that CV can be significantly affected by small sample sizes [44], and ) for chew cycle durations collected from 12 species of basal aquatic-feeding anamniotes (mapped onto phylogeny pruned from [48]); chondrichthyans (Chiloscyllium and Potamotrygon), a basal actinopterygian (Polypterus), a basal sarcopterygian (Protopterus) and eight salamander species.…”

“…Using our results, the analysis of Faltings et al . [50] would suggest that chewing and locomotion are equally rhythmic (22.20 ± 5.66%) in those six amphibian species.…”