Whole-limb scaling of muscle mass and force-generating capacity in amniotes

Abstract

Skeletal muscle mass, architecture and force-generating capacity are well known to scale with body size in animals, both throughout ontogeny and across species. Investigations of limb muscle scaling in terrestrial amniotes typically focus on individual muscles within select clades, but here this question was examined at the level of the whole limb across amniotes generally. In particular, the present study explored how muscle mass, force-generating capacity (measured by physiological cross-sectional area) and internal architecture (fascicle length) scales in the fore- and hindlimbs of extant mammals, non-avian saurians (‘reptiles’) and bipeds (birds and humans). Sixty species spanning almost five orders of magnitude in body mass were investigated, comprising previously published architectural data and new data obtained via dissections of the opossum Didelphis virginiana and the tegu lizard Salvator merianae. Phylogenetic generalized least squares was used to determine allometric scaling slopes (exponents) and intercepts, to assess whether patterns previously reported for individual muscles or functional groups were retained at the level of the whole limb, and to test whether mammals, reptiles and bipeds followed different allometric trajectories. In general, patterns of scaling observed in individual muscles were also observed in the whole limb. Reptiles generally have proportionately lower muscle mass and force-generating capacity compared to mammals, especially at larger body size, and bipeds exhibit strong to extreme positive allometry in the distal hindlimb. Remarkably, when muscle mass was accounted for in analyses of muscle force-generating capacity, reptiles, mammals and bipeds almost ubiquitously followed a single common scaling pattern, implying that differences in whole-limb force-generating capacity are principally driven by differences in muscle mass, not internal architecture. In addition to providing a novel perspective on skeletal muscle allometry in animals, the new dataset assembled was used to generate pan-amniote statistical relationships that can be used to predict muscle mass or force-generating capacity in extinct amniotes, helping to inform future reconstructions of musculoskeletal function in the fossil record.