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ABSTRACT The jaw muscles of the southern alligator lizard, Elgaria multicarinata, are used in prolonged mate-holding behavior, and also to catch fast prey. In both males and females, these muscles exhibit an unusual type of high endurance known as sustained force in which contractile force does not return to baseline between subsequent contractions. This phenomenon is assumed to facilitate the prolonged mate-holding observed in this species. Skeletal muscle is often subject to a speed–endurance trade-off. Here, we determined the isometric twitch, tetanic and isotonic force–velocity properties of the jaw muscles at ∼24°C as metrics of contractile speed and compared these properties with a more typical thigh locomotory muscle to determine whether endurance by sustained force allows for circumvention of the speed–endurance trade-off. The specialized jaw muscle was generally slower than the more typical thigh muscle: time to peak twitch force, twitch 90% relaxation time (P<0.01), and tetanic 90% and 50% relaxation times (P<0.001) were significantly longer, and force–velocity properties were significantly slower (P<0.001) in the jaw than the thigh muscle. However, there seemed to be greater effects on relaxation rates and shortening velocity than on force rise times: there was no effect of muscle on time to peak, or 50% of tetanic force. Hence, the jaw muscle of the southern alligator lizard does not seem to circumvent the speed–endurance trade-off. However, the maintenance of force rise times despite slow relaxation, potentially enabled by the presence of hybrid fibers, may allow this muscle to meet the functional demand of prey capture. 

Muscle-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. 

ABSTRACT A trade-off between locomotor speed and endurance occurs in various taxa, and is thought to be underpinned by a muscle-level trade-off. Among four replicate high runner (HR) lines of mice, selectively bred for voluntary wheel-running behavior, a negative correlation between average running speed and time spent running has evolved. We hypothesize that this trade-off is due to changes in muscle physiology. We studied the HR lines at generation 90, at which time one line (L3) is fixed for the mini-muscle phenotype, another is polymorphic (L6) and the others (L7, L8) lack mini-muscle individuals. We used in situ preparations to quantify the contractile properties of the triceps surae muscle complex. Maximal shortening velocity varied significantly, being lowest in mini-muscle mice (L3 mini=25.2 mm s−1, L6 mini=25.5 mm s−1), highest in normal-muscle mice L6 and L8 (40.4 and 50.3 mm s−1, respectively) and intermediate in normal-muscle L7 mice (37.2 mm s−1). Endurance, measured both as the slope of the decline in force and the proportion of initial force that could be sustained, also varied significantly. The slope was shallowest in mini-muscle mice (L3 mini=−0.00348, L6 mini=−0.00238), steepest in lines L6 and L8 (−0.01676 and −0.01853), and intermediate in L7 (−0.01145). Normalized sustained force was highest in mini-muscle mice (L3 mini=0.98, L6 mini=0.92) and lowest in L8 (0.36). There were significant, negative correlations between velocity and endurance metrics, indicating a muscle-level trade-off. However, this muscle-level trade-off does not seem to underpin the organismal-level speed and endurance trade-off previously reported as the ordering of the lines is reversed: the lines that run the fastest for the least time have the lowest muscle complex velocity and highest endurance. 

Muscle contraction is a three-dimensional process, as anyone who has observed a bulging muscle knows. Recent studies suggest that the three-dimensional nature of muscle contraction influences its mechanical output. Shape changes and radial forces appear to be important across scales of organization. Muscle architectural gearing is an emerging example of this process.