Tradeoffs in wholemuscle function and its ecological importance

Performance tradeoffs represent constraints on the direction of adaptive physiological evolution and therefore are fundamental for understanding the widespread occurrence of individual variation in physiological traits. Identification of the physiological mechanisms underlying constraints on vertebrate physical performance are an important research objective for evolutionary-minded functional biologists. Functional constraints can occur from negative interactions between pairs of ecologically relevant performance traits. For example, one of the most intuitive tradeoffs in muscle performance is between sprint (high power output) and endurance (high fatigue resistance) activities, which arise via differential expression of fast and slow muscle fiber types that maximize these differing activities [97]. As a consequence, increases in the performance of one task can lead to decreases in the performance of another, with the net result a compromised phenotype that is optimal for neither task. The existence and mechanistic basis of functional tradeoffs can be studied in a variety of ways, including optimality models, quantitative genetic analyses, interindividual analyses, and interspecific comparisons. The vertebrate locomotor system must often perform a variety of activities that are often antagonistic in their requirements (see Section 11.4), and as a consequence, it has been used as a model system for examining performance tradeoffs.

In parallel with the previous discussion on muscle specialization (see Section 11.4), the study of functional performance tradeoffs was first addressed within the context of interspecific comparisons, which have been very successful at identifying the range of possible functional tradeoffs that can limit the evolution of vertebrate physical performance. These studies have also recently been complemented with several interspecific comparative analyses within a phylogenetic context [74,98,99] and comparative studies of different breeds of domesticated animals [100]. For example, by comparing two dog breeds (greyhound and pit bulls) that have experienced intense artificial selection for certain physical attributes, Pasi and Carrier [100] investigated the functional tradeoffs that prevent the simultaneous optimization of both running performance and physical fighting. The same authors found that pit bulls possessed greater muscle mass distally in their limbs, larger muscles in their forelimbs than their hindlimbs, and a lower capacity for elastic energy storage in their ankle joint tendons than greyhounds [100]. Thus, physical attributes that were associated with fighting were antagonistic to running performance and thus could not have evolved simultaneously.

Regarding interindividual variation, most analyses of locomotor tradeoffs have been conducted using analyses of whole-animal performance. Somewhat surprisingly, most of these analyses have not detected the existence of functional tradeoffs in locomotor performance, despite the logical underlying basis of these physiological tradeoffs. For example, although a tradeoff between speed and endurance capacity is predicted based on individual differences in the proportions of fast, powerful fibers and slow, more fatigue-resistant fibers, when tested at the whole-animal level, most studies have found no evidence for this performance tradeoff [27,35,101-105]. However, recent studies on human decathletes have argued that such interindividual comparisons are complicated by the masking effects of variation in general physical quality [106]. This often prevents the detection of functional tradeoffs in performance despite their probable importance within each individual and their influence on the directions of adaptive evolutionary change.

Although previous inter- and intraspecific comparative studies have been successful at identifying the possible functional constraints operating on the vertebrate locomotor system, they have not allowed detailed analyses of the mechanistic bases of these hypothesized tradeoffs. Studies of performance tradeoffs at the level of the whole muscle allow direct investigations of the importance of functional tradeoffs at the level at which they are presumed to operate, and they help in understanding how some of these constraints might be overridden by processes occurring at higher levels of organization, so as to be obscured in the context of interindividual studies. Few studies have tested the extent of performance tradeoffs in whole-muscle performance. Interindividual analyses of muscle physiology can determine both whether functional tradeoffs can be detected in whole muscle and the magnitude of any possible performance tradeoffs. Based on comparisons of different isolated muscle fiber types, we know that variation in the specific force- and velocity-dependent properties as well as the mechanical power production capabilities of a muscle are related to the specific muscle fiber type and the proportion of certain myosin isoforms expressed within the fibers (see Section 11.4). A recent comparative analysis of 11 different species of Phrynosomatid lizards [18] also showed that the percentage of fast oxidative glycolytic muscle fibers was negatively correlated with the percentage of fast glycolytic fibers. Several recent studies have also directly investigated the extent of functional tradeoffs in whole-muscle performance by using the work-loop technique to analyze the contractile properties of isolated skeletal muscle [105,107,108].

Using interindividual analyses of whole-muscle performance, tradeoffs between maximum power output and fatigue resistance were detected in both isolated mouse and frog muscle [105,107,108]. Despite the lack of a detectable tradeoff between speed and endurance in whole-animal performance of the frog Xenopus laevis, a clear tradeoff between power and fatigue resistance was still found in peroneus muscle [105]. Interindividual analyses of whole gastrocnemius muscle performance of the toad Bufo viridus demonstrated tradeoffs between fatigue resistance and both maximum power output and stress of the muscle [108] (Figures 11.2A and 11.2B). In addition, this correlative analysis showed a significant positive relationship between power output and maximum stress [108]. Thus, increases in maximum stress of an individual muscle leads to simultaneous increases in maximum power output (Figure 11.2C) and decreases in fatigue resistance [108]. Surprisingly, no significant correlations were detected between whole muscle performance of B. viridus and muscle fiber type composition. Future studies should investigate the relationship between interindividual variation in whole-muscle performance and the predicted underlying relationship with the muscle's morphological structure.

11.6 conclusions

Throughout this chapter, we have argued that interindividual differences are of great importance in evolutionary physiology because they are likely to reflect intrinsic variability upon which natural selection can potentially act [109]. Such variability might have an underlying basis in the physiological traits of individuals, among which those related to skeletal muscle traits, including size, morphology and physiology, are particularly relevant for being closely related to behavioral performance and, likely, to the ecological success of individuals [39,46,108,110]. The assumption of a logical relationship between muscle performance and ecological success permeates the literature, but studies directly investigating such relationships are scarce. Similarly, attempts to investigate the strength of phenotypic selection on biomechan-ical quantitative traits are scant (see, e.g., Ref. [4]), an observation that is true of physiological traits in general [111]. The study of the nature, reproducibility, and ecological consequences of interindividual variation of muscle physiology, therefore, is an integrative and contemporary field of research.

Although the theoretical links relating muscle mechanics, behavioral performance, and evolution seem rather well-established, empirical evidence is missing. Such empirical support is not just a formality, but also an essential task to understanding how

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FIGURE 11.2 Correlations between several measures of in vitro muscle performance for the gastrocnemius muscle of the toad Bufo viridus. Measures of isolated muscle performance reported are (A) maximum net power output, (B) maximum isometric stress, and (C) fatigue resistance of power output during a fatigue run at 5 Hz. All correlations were statistically significant at the level of P < 0.05. (Modified after Wilson, R.S. et al., J. Comp. Physiol., 174B, 453, 2004.)

muscle physiology evolves. For example, studies showing short-term reproducibility of behavioral performance are becoming abundant, but studies across years [34], temperatures [39], or ecological settings [38] are still uncommon. If behavioral performance ranks are context dependent, the relationship between behavioral performance and fitness would be of a more complex nature than usually stated in the literature. Understanding how the morphophysiology of skeletal muscle changes along the lifetime of individuals in response to relevant ecophysiological variables and how these changes affect the behavioral performance of individuals, would be an important contribution of muscle physiologists to the evolution of behavioral performance, a main issue in evolutionary physiology. Interesting contributions from this standpoint include how skeletal muscle responds to changes in ecophysiological variables such as ontogeny, level of activity, temperature, availability of resources, and duration of hypometabolic states, for example, estivation or hibernation. Additionally, very few studies have used training as a tool to explore the scope for changes in behavioral performance in vertebrate ectotherms (see, e.g., Ref. [112]).

The study of functional tradeoffs in skeletal muscle also emerges as a field that deserves further attention. There is enough evidence to state clearly that certain muscle traits cannot be simultaneously maximized, and research along these lines still has much to offer. Phenotypic tradeoffs, however, might relate muscle properties to other important traits of natural history. As an example, hatchling survival and sprint speed seem inversely correlated in some lizards [31]. Such findings pose questions regarding how an investment in the production of skeletal muscle might vary among individuals in ways that might be consequential for fitness. If such patterns abound, it would be quite incorrect to assume simplistically that the fastest lizards are the fittest. Studies relating muscle function with life-history traits such as time for maturity, growth rate, hatchling survival, and other traits are very uncommon but are needed. The relationship between fitness and behavioral performance is further complicated by the observation that differences in muscle performance among individuals may not necessarily be coupled with differences in undisturbed (e.g., field) behavioral performance (see Section 11.2). Related questions emerge, however, given that differences among individuals in their activity patterns could, at least in theory, cause differentiation in various aspects of exercise physiology through training effects.

Many questions remain to be answered regarding the role of body size as a factor explaining interindividual variation in muscle performance. It is clear that no one scaling law is universal in its prediction of changes in performance or function with body size. For example, the scaling of maximal acceleration during jumping within and across Anolis lizard species demonstrates positive allometry in smaller lizards but no relationship in larger lizards [73]. Wilson et al. [42] have also demonstrated a discontinuous scaling relationship with positive allometry between maximum jump distance and body mass in frogs of smaller size and then body size independence in larger frogs. The nature of such discontinuities is fundamental to evolutionary physiology because scaling patterns might differ at contrasting body masses due to different selective pressures associated with ecological performance. Perhaps in some species of frogs, small individuals must jump a minimum absolute distance to be ecologically functional, whereas larger individuals exhibit mass independence of jump distance because they have exceeded a critical level of ecologically relevant performance [42].

Although the scaling relationships of locomotion in running animals have received a large amount of attention, they have not been considered in such a clear ecological context as in the jumping studies mentioned above. For instance, various predictions have been made that limb dimensions should scale according to geometric [113] or elastic similarity [114], and that the energetic cost of locomotion is dependent on the rate at which force is produced and stride frequency [115,116].

The generally assumed extension of these hypotheses is that such physical constraints of body size dictate the stride frequency used at any animal size, which in turn dictates the maximal shortening velocity of muscle (for a review, see [117]). However, as discussed in Section 11.3 (see also [62]), the power produced at any stride frequency is dependent on a range of muscle mechanical properties, not just maximum shortening velocity. Pellegrino and collaborators [61] have also postulated that the higher energy cost of locomotion in small animals is due to their higher relative muscle power output, i.e., they have faster muscles that produce more power, incurring a greater energetic cost. Other important constraints may act, however, because viable individuals within a species are likely to be those attaining locomotory performances that grant appropriate ecological performance. Among lizards, for example, larger individuals with longer legs and stride lengths could reach a threshold speed by using a lower stride frequency. They could, therefore, exhibit slower maximal muscle shortening velocity and contraction kinetics, and hence relatively lower energetic cost.

Multidisciplinary studies involving muscle physiology and biomechanics, ecology, and evolution are important to fully understand the relationships between organismal performance and fitness. They are needed also to understand how the possible mechanistic bases of interindividual behavioral variation may indicate the role physiology plays in constraining the behavioral tactics used by ectotherms. The relationships between behavioral and physiological performance are evident only when experiments involve animals forced to perform near their maximal possibilities, and yet studies with vertebrate ectotherms in the field do not show a clear relationship between behavior and exercise physiology. Little is known about the nature and significance of interindividual variation in the skeletal muscle of vertebrate ectotherms: Is interindividual diversity in muscle performance similar among populations of related species? If not, why not? To what extent is interindividual variation merely noise, or does it reflect behavioral strategies coexisting within populations? Why do relationships between individual field behavior and physiology seem absent is some species? Perhaps many such taxa most frequently perform well below their maximal potential, but if so, what would be the real impact of behavioral performance on fitness? This relationship is assumed to exist, but it is mainly a sensible theoretical premise for which direct empirical support is limited to very few studies [118,119]. Further efforts favoring an integrative perspective of the mechanistic causes and ecological consequences of interindividual variation are, therefore, very much needed.

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