Muscle-Tendon Unit Properties in Mice Bred for High Levels of Voluntary Running: Novel Physiologies, Coadaptation, Trade-Offs, and Multiple Solutions in the Evolution of Endurance Running

AbstractMuscle-tendon unit (MTU) morphology and physiology are likely major determinants of locomotor performance and therefore Darwinian fitness. However, the relationships between underlying traits, performance, and fitness are complicated by phenomena such as coadaptation, multiple solutions, and trade-offs. Here, we leverage a long-running artificial selection experiment in which mice have been bred for high levels of voluntary running to explore MTU adaptation, as well as the role of coadaptation, multiple solutions, and trade-offs, in the evolution of endurance running. We compared the morphological and contractile properties of the triceps surae complex, a major locomotor MTU, in four replicate selected lines to those of the triceps surae complex in four replicate control lines. All selected lines have lighter and shorter muscles, longer tendons, and faster muscle twitch times than all control lines. Absolute and normalized maximum shortening velocities and contractile endurance vary across selected lines. Selected lines have similar or lower absolute velocities and higher endurance than control lines. However, normalized shortening velocities are both higher and lower in selected lines than in control lines. These findings potentially show an interesting coadaptation between muscle and tendon morphology and muscle physiology, highlight multiple solutions for increasing endurance running performance, demonstrate that a trade-off between muscle speed and endurance can arise in response to selection, and suggest that a novel physiology may sometimes allow this trade-off to be circumvented.