Abstract
BackgroundThe functional design of skeletal muscles is shaped by conflicting selective pressures between support and propulsion, which becomes even more important as animals get larger. If larger animals were geometrically scaled up versions of smaller animals, increases in body size would cause an increase in musculoskeletal stress, a result of the greater scaling of mass in comparison to area. In large animals these stresses would come dangerously close to points of failure. By examining the architecture of 22 hindlimb muscles in 27 individuals from 9 species of varanid lizards ranging from the tiny 7.6 g Varanus brevicauda to the giant 40 kg Varanus komodoensis, we present a comprehensive dataset on the scaling of musculoskeletal architecture in monitor lizards (varanids), providing information about the phylogenetic constraints and adaptations of locomotor muscles in sprawling tetrapods.ResultsScaling results for muscle mass, pennation and physiological cross-sectional area (PCSA), all suggest that larger varanids increase the relative force-generating capacity of femur adductors, knee flexors and ankle plantarflexors, with scaling exponents greater than geometric similarity predicts. Thus varanids mitigate the size-related increases in stress by increasing muscle mass and PCSA rather than adopting a more upright posture with size as is shown in other animals. As well as the scaling effects of muscle properties with body mass, the variation in muscle architecture with changes in hindlimb posture were also prominent. Within varanids, posture varies with habitat preference. Climbing lizards display a sprawling posture while terrestrial lizards display a more upright posture. Sprawling species required larger PCSAs and muscle masses in femur retractors, knee flexors, and ankle plantarflexors in order to support the body.ConclusionsBoth size and posture-related muscle changes all suggest an increased role in support over propulsion, leading to a decrease in locomotor performance which has previously been shown with increases in size. These estimates suggest the giant Pleistocene varanid lizard (Varanus megalania priscus) would likely not have been able to outrun early humans with which it co-habitated the Australian landmass with.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-016-0141-5) contains supplementary material, which is available to authorized users.
Highlights
The functional design of skeletal muscles is shaped by conflicting selective pressures between support and propulsion, which becomes even more important as animals get larger
Body morphology scaling Before we determined the influence of size on muscle architecture and function, it was important to understand how the limb segments themselves responded to changes in size (Additional file 1: Table S1)
Hindlimb segments lengths, tail length and pelvic width all scaled as expected from isometry, with an exception being pelvic height, which scaled larger than expected from isometry 0.40 (0.35–0.45)
Summary
The functional design of skeletal muscles is shaped by conflicting selective pressures between support and propulsion, which becomes even more important as animals get larger. If larger animals were geometrically scaled up versions of smaller animals, increases in body size would cause an increase in musculoskeletal stress, a result of the greater scaling of mass in comparison to area In large animals these stresses would come dangerously close to points of failure. McMahon [5, 6] proposed that muscles need not scale with these static stress similar proportions to maintain stresses at equivalent ratios (safety factors), but rather need to scale as elastically similar proportions Under these conditions, lengths are expected to scale proportional to M0.25, diameters to M0.375 and cross-sectional areas to M0.75. Lengths are expected to scale proportional to M0.25, diameters to M0.375 and cross-sectional areas to M0.75 Even these lower scaling exponents suggests that the architecture of skeletal muscle may shift toward a mechanical role in support at the cost of propulsion as size increases
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