Individual variation in behavioral performance and muscle physiology

Whether the behavioral performance* of vertebrate ectotherms relates to underlying physiological characteristics and adaptive consequences has been a central question in evolutionary physiology. From the range of performance measures that may be investigated, studies of locomotor performance have offered particular insight into these questions. The evolution of specific traits underlying locomotor performance may occur during historical ecological transitions and are thus likely to have adaptive consequences. For example, phylogenetic comparative approaches were initially used to provide evidence for adaptive differences in locomotor performance among

* Behavioral performance admittedly involves more than active behaviors, but in this chapter we restrict the term to the quantifiable maximum performance of animals during active behaviors that involve the production of mechanical force by skeletal muscle.

lizard species [16,17]. These early patterns have been confirmed by more recent studies focusing simultaneously on sprint performance and muscle physiology. In the family Phrynosomatidae, which encompasses the genus Sceloporus, sand lizards (Uta and related lizards), and horned lizards (Phrynosoma and related lizards), sand lizards are the fastest in the clade and have comparatively faster glycolytic fibers

[18]. Similarly, in the lizard genus Tropidurus, the sand dune endemic species T. psamonastes exhibits higher sprint speeds on sand and a higher proportion of glycolytic fibers than the sister species T. itambere, which is endemic to rocky outcrops

[19]. Convergent evolution of performance traits suggesting adaptive trends have been reported in other taxa of ectothermic vertebrates, including the muscle design of unrelated fish taxa that are ecologically similar [20,21] or the peculiar ability of unrelated high-elevation tropical anurans to be active at low temperatures [22].

Given the observed and presumably adaptive variation in behavioral performance and muscle physiology among species, questions arise concerning the relationships between this higher-level variation and variation among individuals within a population. This is a central issue in evolutionary physiology because adaptive shifts in the behavioral performance traits of vertebrates are believed to begin within populations and have three requirements: (1) significant repeatable variation among individuals, (2) heritability of the trait, and (3) variation in the trait influencing the survival or reproductive success of the individual (i.e., fitness) [23,24]. Testing the set of requirements for the evolution of a physiological performance trait is a challenging enterprise, so most of the data available are fragmented (see next paragraph). Not all reported interindividual variation in performance is both repeatable and has a heritable basis. For example, nonheritable variation may result from health or reproductive state. Interindividual variation due to ontogenetic development might also be difficult to analyze in this context, particularly in amphibians, because it might involve heritable and environmentally induced variation. Metamorphosis involves dramatic morphological transitions, and behavioral performance ranks before and after metamorphosis may not be maintained [25,26]. Studies using adult individual vertebrate ectotherms in similar conditions of health, reproductive state, and season would be ideal to address the question of whether reproducible variability exists within populations.

Moving to the second postulate, the heritability of performance traits is assumed given interspecific adaptive trends, but direct evidence and attempts at quantification are scarce. Metabolic rates during intense exercise [24], sprint speed and endurance in lizards [27], as well as various other metabolic traits related to performance and exercise physiology, are at least partially heritable and respond to artificial selection in the laboratory [28,29]. Finally, and regarding the relationship between behavioral performance and fitness, faster garter snakes have more chance of survival than slower counterparts [30], and lizard hatchling survival is positively correlated with body size, sprint speed, and stride length, but negatively correlated with growth rate [4,31]. In amphibians, phenotypic plasticity in larval forms leads to deeper tails in environments with odonate larvae, and these morphs have increased chances of survival [32], partially due to increased swimming speed [33] but perhaps more importantly due to the deflection of attacks away from the vulnerable head region to the tail [32].

The occurrence of reproducible individual variation in the behavioral performance of vertebrates has been well documented in lizards, fish, and amphibians [26,34-39], although this literature encompasses two different approaches to the question. On the one hand, some researchers focus on what animals do under natural conditions, testing the reproducibility of behavioral performances in undisturbed animals. However, behavioral performance in nature might vary among individuals independently of their capacity to produce force of work. A cleaner link between behavior and physiology would be expected when attempts are made to elicit the maximal performance in an individual. Maximal performance is more likely to be affected by body size (see Section 11.3), as clearly illustrated in the jumping performance of anuran amphibians [40-43] either via effects on whole body mechanics or on muscle performance [41,44]. Interindividual differences in maximum performance may also be related to body shape and morphometric traits such as relative hind limb length and relative tail length, as shown for the locomotor performance of hatchling lizards [27]. In the iguanid lizard Ctenosaura similes, running endurance is mass dependent and related to relative differences in organ mass, particularly thigh muscle mass [45], and compatible findings have been reported for salamanders [46]. In the tree-frog Hyla multilineata, a significant amount of variance in maximum jump distance among individuals is related to a combination of factors, including the metabolic profile and mass of the plantaris muscle and total hind limb muscle mass [47].

Most of the information available regarding interindividual variation in the natural behaviors of vertebrate ectotherms comes from studies with amphibians. Both discrete and continuous behavioral diversity have been reported within populations of salamanders [48] and frogs [49], showing, for example, consistent variation among individuals in antipredator behaviors that might depend only partially or not at all on body size. For most anurans, females select males as reproductive partners based on call structure and intensity [50,51]. However, individuals of some species are silent "satellite males" that do not call but attempt to grasp females on their way to a calling male [51]. The relationship between this sort of interindividual variation in behavioral strategies and variation in physiological traits, particularly muscle physiology, has been poorly studied, and the data available do not point to a simple pattern. For the North American spring peepers (Pseudacris crucifer), persistent calling is considered fundamental for the ability of males to obtain copulations [52]; however, both satellite and calling males coexist within populations. Analyses of the muscle aerobic capacity of satellite males indicate that they are not physiologically inferior to calling males, suggesting these alternative mating strategies are not necessarily related to physiological potential [53]. Similarly, individual Bufo toads differ in their number of attempts to clasp females, but this does not appear to be related to the metabolic physiology of individuals [54]. Interindividual differences in behavior have been reported in various species of male anurans, for example regarding the extent to which calling activity decreases through the night or the time of night at which animals retreat [55], but differences of this sort seem unrelated to an eventual depletion of muscle glycogen reserves [56,57]. These papers, although focused on specific physiological traits, suggest that natural behavioral variation among individuals might occur in the absence of concomitant physiological differentiation. In contrast, clear consistency between behavior and physiology exist in Scinax hiemalis, a tree-frog that when threatened in the field chooses between feigning death, remaining immobile, or jumping away. In the laboratory, behavioral responses when faced with sudden disturbance are associated with both body size and absolute ability of individuals to jump, a trait probably associated with the muscle physiology of individuals [49].

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