Locomotor function shapes the passive mechanical properties and operating lengths of muscle

Abstract

Locomotor muscles often perform diverse roles, functioning as motors that produce mechanical energy, struts that produce force and brakes that dissipate mechanical energy. In many vertebrate muscles, these functions are not mutually exclusive and a single muscle often performs a range of mechanically diverse tasks. This functional diversity has obscured the relationship between a muscle's locomotor function and its mechanical properties. I use hopping in toads as a model system for comparing muscles that primarily produce mechanical energy with muscles that primarily dissipate mechanical energy. During hopping, hindlimb muscles undergo active shortening to produce mechanical energy and propel the animal into the air, whereas the forelimb muscles undergo active lengthening to dissipate mechanical energy during landing. Muscles performing distinct mechanical functions operate on different regions of the force–length curve. These findings suggest that a muscle's operating length may be shaped by potential trade-offs between force production and sarcomere stability. In addition, the passive force–length properties of hindlimb and forelimb muscles vary, suggesting that passive stiffness functions to restrict the muscle's operating length in vivo . These results inform our understanding of vertebrate muscle variation by providing a clear link between a muscle's locomotor function and its mechanical properties.