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1. Does the unusual phenomenon of sustained force circumvent the speed–endurance trade-off in the jaw muscle of the southern alligator lizard (Elgaria multicarinata)?

   https://doi.org/10.1242/jeb.247979  

   Nguyen, Allyn; Leong, Kyle; Holt, Natalie C (January 2025, Journal of Experimental Biology)

   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. 

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2. 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

   https://doi.org/10.1086/731307  

   Castro, Alberto A; Nguyen, Allyn; Ahmed, Saad; Garland, Theodore; Holt, Natalie C (July 2024, Ecological and Evolutionary Physiology)

   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. 

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3. Evolution of hindlimb bone dimensions and muscle masses in house mice selectively bred for high voluntary wheel-running behavior

   https://doi.org/10.1002/jmor.20809  

   Castro, Alberto A.; Garland, Theodore (March 2018, Journal of Morphology)

   We have used selective breeding with house mice to study coadaptation of morphology and physiology with the evolution of high daily levels of voluntary exercise. Here, we compared hindlimb bones and muscle masses from the 11th generation of four replicate High Runner (HR) lines of house mice bred for high levels of voluntary wheel running with four non‐selected control (C) lines. Mass, length, diameter, and depth of the femur, tibia‐fibula, and metatarsal bones, as well as masses of gastrocnemius and quadriceps muscles, were compared by analysis of covariance with body mass or body length as the covariate. Mice from HR lines had relatively wider distal femora and deeper proximal tibiae, suggesting larger knee surface areas, and larger femoral heads. Sex differences in bone dimensions were also evident, with males having thicker and shorter hindlimb bones when compared with females. Several interactions between sex, linetype, and/or body mass were observed, and analyses split by sex revealed several cases of sex‐specific responses to selection. A subset of the HR mice in two of the four HR lines expressed the mini‐muscle phenotype, characterized mainly by an ∼50% reduction in hindlimb muscle mass, caused by a Mendelian recessive mutation, and known to have been under positive selection in the HR lines. Mini‐muscle individuals had elongated distal elements, lighter and thinner hindlimb bones, altered 3rd trochanter muscle insertion positions, and thicker tibia‐fibula distal widths. Finally, several differences in levels of directional or fluctuating asymmetry in bone dimensions were observed between HR and C, mini‐ and normal‐muscled mice, and the sexes. This study demonstrates that skeletal dimensions and muscle masses can evolve rapidly in response to directional selection on locomotor behavior. 

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4. Can a Hybrid Line Break a Selection Limit on Behavioral Evolution in Mice?

   https://doi.org/10.1007/s10519-024-10209-7  

   Hiramatsu, Layla; Careau, Vincent; Garland, Theodore (January 2025, Behavior Genetics)

   Abstract Artificial selection yielded four replicate high runner (HR) lines of mice that reached apparent selection limits (~ threefold increase in wheel revolutions per day vs. four control lines), despite maintenance of additive genetic variance. After 68 generations, we used animal models to test for changes in additive-genetic variances and covariance of the two measured components (average speed and duration) of running distance. We also attempted to break the selection limit by crossing two HR lines, then continuing directional selection on this hybrid line and on the two parental lines for nine generations. The genetic correlation between speed and duration was positive in the base population, but evolved to be negative in the two parental HR lines. Although heritability for both speed and duration (but not distance) increased in the hybrid line, their genetic correlation remained negative. Hybrid F₁mice from generation 68 parents showed heterosis for running distance, which was lost in subsequent generations, and the hybrid line did not exceed the limit. Both male and female hybrids ran faster than parental lines for most generations, but running duration was intermediate or reduced, reflecting their negative genetic correlation. The evolved genetic trade-off between speed and duration may explain the inability for the hybrid line to break the selection limit for distance run, despite renewed additive genetic variance for at least one of its component traits. 

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5. Metabolic reprogramming underlies cavefish muscular endurance despite loss of muscle mass and contractility

   https://doi.org/10.1073/pnas.2204427120  

   Olsen, Luke; Levy, Michaella; Medley, J. Kyle; Hassan, Huzaifa; Miller, Brandon; Alexander, Richard; Wilcock, Emma; Yi, Kexi; Florens, Laurence; Weaver, Kyle; et al (January 2023, Proceedings of the National Academy of Sciences)

   Physical inactivity is a scourge to human health, promoting metabolic disease and muscle wasting. Interestingly, multiple ecological niches have relaxed investment into physical activity, providing an evolutionary perspective into the effect of adaptive physical inactivity on tissue homeostasis. One such example, the Mexican cavefishAstyanax mexicanus,has lost moderate-to-vigorous activity following cave colonization, reaching basal swim speeds ~3.7-fold slower than their river-dwelling counterpart. This change in behavior is accompanied by a marked shift in body composition, decreasing total muscle mass and increasing fat mass. This shift persisted at the single muscle fiber level via increased lipid and sugar accumulation at the expense of myofibrillar volume. Transcriptomic analysis of laboratory-reared and wild-caught cavefish indicated that this shift is driven by increased expression ofpparγ—the master regulator of adipogenesis—with a simultaneous decrease in fast myosin heavy chain expression. Ex vivo and in vivo analysis confirmed that these investment strategies come with a functional trade-off, decreasing cavefish muscle fiber shortening velocity, time to maximal force, and ultimately maximal swimming speed. Despite this, cavefish displayed a striking degree of muscular endurance, reaching maximal swim speeds ~3.5-fold faster than their basal swim speeds. Multi-omic analysis suggested metabolic reprogramming, specifically phosphorylation of Pgm1-Threonine 19, as a key component enhancing cavefish glycogen metabolism and sustained muscle contraction. Collectively, we reveal broad skeletal muscle changes following cave colonization, displaying an adaptive skeletal muscle phenotype reminiscent to mammalian disuse and high-fat models while simultaneously maintaining a unique capacity for sustained muscle contraction via enhanced glycogen metabolism. 

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