The importance of comparative physiology: mechanisms, diversity and adaptation in skeletal muscle physiology and mechanics

Abstract

Skeletal muscle powers animal movement, making it an important determinant of fitness. The classic excitation–contraction coupling, sliding-filament and crossbridge theories are thought to describe the processes of muscle activation and the generation of force, work and power. Here, we review how the comparative, realistic muscle physiology typified by Journal of Experimental Biology over the last 100 years has supported and refuted these theories. We examine variation in the contraction rates and force–length and force–velocity relationships predicted by these theories across diverse muscles, and explore what has been learnt from the use of workloop and force-controlled techniques that attempt to replicate aspects of in vivo muscle function. We suggest inclusion of features of muscle contraction not explained by classic theories in our routine characterization of muscles, and the use of phylogenetic comparative methods to allow exploration of the effects of factors such as evolutionary history, ecology, behavior and size on muscle physiology and mechanics. We hope that these future directions will improve our understanding of the mechanisms of muscle contraction, allow us to better characterize the variation in muscle performance possible, and enable us to infer adaptation.

Tradeoffs between bite force and gape in Eulemur and Varecia

“…One possibility is that the generalized muscle length‐force curve used in our model does not accurately represent the length dependency of force generation of jaw adductor muscles tested in this study. Considerable variation in the width of normalized length‐force relationships has been observed in muscles (Mendoza et al, 2023). Most of the differences in width are between vertebrate and invertebrate muscle, but some variation is present within vertebrate skeletal muscle.…”

The effect of muscle ultrastructure on the force, displacement and work capacity of skeletal muscle

“…Unfortunately, there is limited empirical evidence on the variation of force-length curve width and work density across muscles with different actin and myosin filament lengths. The width of fibre or muscle stress-length relationships varies considerably [3,82]. However, our findings suggest that this variation relative fibre length l s /l opt (1) 0.5 1 1.5 2 relative fibre length l s /l opt (1) frog sartorius (l sarc = 2.17 µm) cockroach femur (l sarc = 4.77 µm) lobster claw closer (l sarc = 9.17 µm) l sarc = 2 µm l sarc = 4.6 µm l sarc = 9 µm real sarcomeres, 0.25σ max idealized sarcomeres, 0.25σ max idealized sarcomeres, 0.5σ max real sarcomeres, 0.5σ max idealized sarcomeres, 0.75σ max real sarcomeres, 0.75σ max is likely related to factors other than variation in actin and myosin filament length.…”

“…Skeletal muscle generates the mechanical output required for the majority of animal movements through interactions between the contractile protein filaments: actin, myosin and titin. Considerable variation in muscle and organismal performance is exhibited across muscles and species, and this diversity is underpinned by variation in muscle structure and physiology [1][2][3][4][5]. For example, leaf-cutter ants display structural adaptations in their mandibular closer muscle that enable generation of the high forces required for cutting [6], and birds have long pectoralis muscle fibres [1] with fast myosin isoforms [7] to satisfy the substantial work and power requirements of flight.…”

“…Myosin isoform, actin and myosin filament lengths, and gross muscle architecture vary across muscles, and these variations have been associated with specialization for different aspects of performance [1][2][3][4][5]. Vertebrate muscle has a highly conserved muscle ultrastructure [41][42][43][44][45][46][47].…”

Beyond power limits: the kinetic energy capacity of skeletal muscle

“…Movement is essential for all animals, and muscle is what drives animal movement (Alexander, 2003;Biewener and Patek, 2018;Dickinson et al, 2000;McMahon, 1984). What muscle can and cannot do is thus a fundamental question in zoology (Biewener, 2016;Daniel and Tu, 1999;Higham et al, 2016;Mendoza et al, 2023). Two rudimentary mechanical properties are thought to characterise each unit of muscle mass as a motor: its maximum work density, and its maximum power density (Bennet-Clark, 1977;Borelli, 1680;Gabriel, 1984;Hill, 1950b).…”