Monitoring muscle over three orders of magnitude: Widespread positive allometry among locomotor and body support musculature in the pectoral girdle of varanid lizards (Varanidae)

There is a functional trade-off in the design of skeletal muscle. Muscle strength depends on the number of muscle fibers in parallel, while shortening velocity and operational distance depend on fascicle length, leading to a trade-off between the maximum force a muscle can produce and its ability to change length and contract rapidly. This trade-off becomes even more pronounced as animals increase in size because muscle strength scales with area (length(2)) while body mass scales with volume (length(3)). In order to understand this muscle trade-off and how animals deal with the biomechanical consequences of size, we investigated muscle properties in the pectoral girdle of varanid lizards. Varanids are an ideal group to study the scaling of muscle properties because they retain similar body proportions and posture across five orders of magnitude in body mass and are highly active, terrestrially adapted reptiles. We measured muscle mass, physiological cross-sectional area, fascicle length, proximal and distal tendon lengths, and proximal and distal moment arms for 27 pectoral girdle muscles in 13 individuals across 8 species ranging from 64 g to 40 kg. Standard and phylogenetically informed reduced major axis regression was used to investigate how muscle architecture properties scale with body size. Allometric growth was widespread for muscle mass (scaling exponent >1), physiological cross-sectional area (scaling exponent >0.66), but not tendon length (scaling exponent >0.33). Positive allometry for muscle mass was universal among muscles responsible for translating the trunk forward and flexing the elbow, and nearly universal among humeral protractors and wrist flexors. Positive allometry for PCSA was also common among trunk translators and humeral protractors, though less so than muscle mass. Positive scaling for fascicle length was not widespread, but common among humeral protractors. A higher proportion of pectoral girdle muscles scaled with positive allometry than our previous work showed for the pelvic girdle, suggesting that the center of mass may move cranially with body size in varanids, or that the pectoral girdle may assume a more dominant role in locomotion in larger species. Scaling exponents for physiological cross-sectional area among muscles primarily associated with propulsion or with a dual role were generally higher than those associated primarily with support against gravity, suggesting that locomotor demands have at least an equal influence on muscle architecture as body support. Overall, these results suggest that larger varanids compensate for the increased biomechanical demands of locomotion and body support at higher body sizes by developing larger pectoral muscles with higher physiological cross-sectional areas. The isometric scaling rates for fascicle length among locomotion-oriented pectoral girdle muscles suggest that larger varanids may be forced to use shorter stride lengths, but this problem may be circumvented by increases in limb excursion afforded by the sliding coracosternal joint.