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Synopsis Sexual selection drives the evolution of a broad diversity of traits, such as the enlarged claws of fiddler crabs, the high-energy behavioral displays of hummingbirds, the bright red plumage of house finches, the elaborated antennae of moths, the wing “snapping” displays of manakins and the calculated calls of túngara frogs. A majority of work in sexual selection has aimed to measure the magnitude of these traits. Yet, we know surprisingly little about the physiology shaping such a diversity of sexually selected behavior and supportive morphology. The energetic properties underlying sexual signals are ultimately fueled by metabolic machinery at multiple scales, from mitochondrial properties and enzymatic activity to hormonal regulation and the modification of muscular and neural tissues. However, different organisms have different physiological constraints and face various ecological selection pressures; thus, selection operates and interacts at multiple scales to shape sexually selected traits and behavior. In this perspective piece, we describe illustrative case studies in different organisms to emphasize that understanding the physiological and energetic mechanisms that shape sexual traits may be critical to understanding their evolution and ramifications with ecological selection. We discuss (1) the way sexual selection shapes multiple integrated components of physiology, behavior, and morphology, (2) the way that sexually selected carotenoid pigments may reflect some aspects of cellular processes, (3) the relationship between sexually selected modalities and energetics, (4) the hormone ecdysone and its role in shaping sex-specific phenotypes in insects, (5) the way varied interaction patterns and social contexts select for signaling strategies that are responsive to social scenes, and (6) the role that sexual selection may have in the exploitation of novel thermal niches. Our major objective is to describe how sexually selected behavior, physiology, and ecology are shaped in diverse organisms so that we may develop a deeper and more integrated understanding of sexual trait evolution and its ecological consequences. 

Abstract Females and males can exhibit striking differences in body size, relative trait size, physiology, and behavior. As a consequence, the sexes can have very different rates of whole-body energy use, or converge on similar rates through different physiological mechanisms. Yet many studies that measure the relationship between metabolic rate and body size only pay attention to a single sex (more often males), or do not distinguish between sexes. We present four reasons why explicit attention to energy-use between the sexes can yield insight into the physiological mechanisms that shape broader patterns of metabolic scaling in nature. First, the sexes often differ considerably in their relative investment in reproduction, which shapes much of life-history and rates of energy use. Second, males and females share a majority of their genome but may experience different selective pressures. Sex-specific energy profiles can reveal how the energetic needs of individuals are met despite the challenge of within-species genetic constraints. Third, sexual selection often pushes growth and behavior to physiological extremes. Exaggerated sexually selected traits are often most prominent in one sex, can comprise up to 50% of body mass, and thus provide opportunities to uncover energetic constraints of trait growth and maintenance. Finally, sex-differences in behavior such as mating-displays, long-distance dispersal, and courtship can lead to drastically different energy allocation among the sexes; the physiology to support this behavior can shape patterns of metabolic scaling. The mechanisms underlying metabolic scaling in females, males, and hermaphroditic animals can provide opportunities to develop testable predictions that enhance our understanding of energetic scaling patterns in nature. 

Abstract When individuals engage in fights with conspecifics over access to resources, injuries can occur. Most theoretical models suggest that the costs associated with these injuries should influence an individual’s decision to retreat from a fight. Thus, damage from intraspecific combat is frequently noted and quantified. However, the fitness-related costs associated with this damage are not. Quantifying the cost of fighting-related damage is important because most theoretical models assume that it is the cost associated with the damage (not the damage itself) that should influence an individual’s decision to retreat. Here, we quantified the cost of fighting-related injuries in the giant mesquite bug, Thasus neocalifornicus. We demonstrate that experimentally simulated fighting injuries result in metabolic costs and costs to flight performance. We also show that flight costs are more severe when the injuries are larger. Overall, our results provide empirical support for the fundamental assumption that damage acquired during intraspecific combat is costly. 

Abstract Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g., basal, resting, field, and maximally active). The scaling of metabolism is usually highly correlated with the scaling of many life-history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to (a) lower contents of expensive tissues (brains, liver, and kidneys), and (b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. An additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include (1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries; (2) studies linking scaling to ecological or phylogenetic context; (3) studies that consider multiple, possibly interacting hypotheses; and (4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate, and reproduction.