Abstract
Anuran jumping is a model system for linking muscle physiology to organismal performance. However, anuran species display substantial diversity in their locomotion, with some species performing powerful leaps from riverbanks or tree branches, while other species move predominantly via swimming, short hops or even diagonal-sequence gaits. Furthermore, many anurans with similar locomotion and morphology are actually convergent (e.g. multiple independent evolutions of 'tree frogs'), while closely related species may differ drastically, as with the walking toad (Melanophryniscus stelzneri) and bullfrog-like river toad (Phrynoides aspera) compared with other Bufonid toads. These multiple independent evolutionary changes in locomotion allow us to test the hypothesis that evolutionary increases in locomotor performance will be linked to the evolution of faster, high-power muscles. I tested the jumping, swimming and walking (when applicable) performance of 14 species of anurans and one salamander, followed by measurement of the contractile properties of the semimembranosus and plantaris longus muscles and anatomical measurements, using phylogenetic comparative methods. I found that increased jumping performance correlated to muscle contractile properties associated with muscle speed (e.g. time to peak tetanus, maximum shortening speed, peak isotonic power), and was tightly linked to relevant anatomical traits (e.g. leg length, muscle mass). Swimming performance was not correlated to jumping, and was correlated with fewer anatomical and muscular variables. Thus, muscle properties evolve along with changes in anatomy to produce differences in overall locomotor performance.
Highlights
Animals have evolved a wide array of locomotor modes to traverse their habitats, find food and mates, and avoid predators. Performance within these modes is tremendously variable, from the slow trudge of a giant tortoise to the rapid dash of a cheetah. These differences across species must be due to corresponding differences in the integrative biomechanical systems that produce these movements, and disentangling the roles of various components of these systems in determining organismal performance is a key challenge in biomechanics
To what extent are interspecific differences in performance linked to corresponding differences in muscle power, contractile speed and activation? While the mechanical output of muscle can be affected by size or muscular anatomy, changes to the force–velocity (F/V) curve can change muscle power output and shortening speed independently of overall muscle dimensions and anatomy, and activation/deactivation kinetics determine how rapidly a muscle can respond to neural activation or the cessation of activation
Phylogenetic PCAs Strong correlations appeared throughout locomotor performance variables, collapsing performance into two PC axes, termed ‘Jump Performance’ and ‘Swim Performance’ that accounted for 86.3% of variation (Table 1; all PCA axes are denoted using initial capitalization and bold font to avoid confusion)
Summary
Animals have evolved a wide array of locomotor modes (e.g. walking, swimming, flying, slithering) to traverse their habitats, find food and mates, and avoid predators. Studies using phylogenetic comparative methods have shown changes in muscle contractile properties with animal size (James et al, 2015) and a tradeoff between in vitro work-loop power and fatigue resistance (Vanhooydonck et al, 2014), though the link between animal performance and muscle properties was inconsistent (Vanhooydonck et al, 2014) It remains unknown whether muscle contractile properties are broadly conserved, evolve rapidly with changes in organismal performance, or show no correlation to locomotor evolution. Intraspecific studies showing correlations between muscle properties and whole-organism performance (Wilson et al, 2002; Wilson and James, 2004; James et al, 2005; Navas et al, 2005) suggest that selection may act upon organismal performance (Arnold, 1983), and, through this, lead to changes in muscle physiology
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