How to build your dragon: scaling of muscle architecture from the world’s smallest to the world’s largest monitor lizard

BACKGROUND: 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. 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. RESULTS: Scaling 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. CONCLUSIONS: Both 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 MATERIAL: The online version of this article (doi:10.1186/s12983-016-0141-5) contains supplementary material, which is available to authorized users.