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Sexual size dimorphism (SSD) can vary drastically across environments, demonstrating pronounced sex‐specific plasticity. In insects, females are usually the larger and more plastic sex. However, the shortage of taxa with male‐biased SSD hampers the assessment of whether the greater plasticity in females is driven by selection on size or represents an effect of the female reproductive role. Here, we specifically address the role of sex‐specific plasticity of body size in the evolution of SSD reversals to disentangle sex and size effects. We first investigate sex‐specific body size plasticity in Sepsis punctum and Sepsis neocynipsea as two independent cases of intraspecific SSD reversals in sepsid flies. In both species, directional variation in SSD between populations is driven by stronger sexual selection on male size. Using controlled laboratory breeding, we find evidence for sex‐specific plasticity and increased condition dependence of male size in populations with male‐biased SSD, but not of female size in populations with female‐biased SSD. To extend the comparative scope, we next estimate sex‐specific body size plasticity in eight additional fly species that differ in the direction of SSD under laboratory conditions. In all species with male‐biased SSD we find males to be the more plastic sex, while this was only rarely the case in species with female‐biased SSD, thus suggesting a more general trend in Diptera. To examine the generality of this pattern in holometabolous insects, we combine our data with data from the literature in a meta‐analysis. Again, male body size tends to be more plastic than female size when males are the larger sex, though female size is now also generally more plastic when females are larger. Our findings indicate that primarily selection on size, rather than the reproductive role per se, drives the evolution of sex‐specific body size plasticity. However, sepsid flies, and possibly Diptera in general, show a clear sexual asymmetry with greater male than female plasticity related to SSD, likely driven by strong sexual selection on males. Although further research controlling for phylogenetic and ecological confounding effects is needed, our findings are congruent with theory in suggesting that condition dependence plays a pivotal role in the evolution of sexual size dimorphism. A plain language summary is available for this article. Plain Language Summary

Single male sexually selected traits have been found to exhibit substantial genetic variance, even though natural and sexual selection are predicted to deplete genetic variance in these traits. We tested whether genetic variance in multiple male display traits of Drosophila serrata was maintained under field conditions. A breeding design involving 300 field‐reared males and their laboratory‐reared offspring allowed the estimation of the genetic variance‐covariance matrix for six male cuticular hydrocarbons (CHCs) under field conditions. Despite individual CHCs displaying substantial genetic variance under field conditions, the vast majority of genetic variance in CHCs was not closely associated with the direction of sexual selection measured on field phenotypes. Relative concentrations of three CHCs correlated positively with body size in the field, but not under laboratory conditions, suggesting condition‐dependent expression of CHCs under field conditions. Therefore condition dependence may not maintain genetic variance in preferred combinations of male CHCs under field conditions, suggesting that the large mutational target supplied by the evolution of condition dependence may not provide a solution to the lek paradox in this species. Sustained sexual selection may be adequate to deplete genetic variance in the direction of selection, perhaps as a consequence of the low rate of favorable mutations expected in multiple trait systems.

Theory predicts that costly sexual displays should evolve condition dependence if the marginal fitness gain from trait exaggeration is greater for high- than for low-condition individuals and that the strength of condition dependence should increase with the strength of directional selection. While there is substantial support for the first prediction, evidence for the latter is much weaker. We undertook a quantitative test of this prediction for a multivariate sexual display consisting of a suite of contact pheromones termed \"cuticular hydrocarbons\" (CHCs) in Drosophila serrata. We performed a dietary manipulation of condition (i.e., the pool of metabolic resources available for allocation to fitness-enhancing traits) within a half-sibling breeding design, thereby also providing insight into the genetic basis of condition dependence. As predicted, the linear combination of CHCs under the strongest sexual selection from female mate preferences was unusually condition dependent relative to other CHC combinations within the population (). A significant positive correlation also existed between the strengths of condition dependence and sexual selection among different CHC blends (, ). Finally, sires varied in their response to the dietary manipulation, demonstrating significant genetic variance in condition dependence. Our results are consistent with the evolution of heightened condition dependence of sexual displays in response to persistent sexual selection.

Sexual dimorphism accounts for a large fraction of intraspecific diversity. However, not all traits are equally sexually dimorphic; instead, individuals are mosaics of tissues that vary in their ability to exhibit dimorphism. Furthermore, the degree of a trait's sexual dimorphism is frequently environment‐dependent, with elaborate sexual dimorphism commonly being restricted to high nutritional conditions. Understanding the developmental basis and evolution of condition‐dependent sexual dimorphism can be critically informed by determining – across tissues and nutritional conditions – what sex‐biased genes are deployed and how they interact and translate into functional processes. Indeed, key theories concerning the evolution of condition‐dependent sexually dimorphic traits rest on assumptions regarding their developmental genetic underpinnings, yet, have largely gone unexamined by empirical studies. Here, we provide such evidence by investigating the transcriptomic basis of tissue‐ and nutrition‐dependent sexual dimorphism in the bull‐headed dung beetle Onthophagus taurus. Our findings suggest (1) that generating morphological sexual dimorphism requires sex‐biased gene expression in and developmental remodeling of both sexes, regardless of which sex exhibits externally visible trait exaggeration, (2) that although sexually dimorphic phenotypes are comprised of traits underlain by independent repertoires of sex‐biased gene expression, they act similarly at a functional level, and (3) that sexual dimorphism and condition‐dependence share common genetic underpinnings specifically in sexually‐selected traits. Sexual dimorphism represents one of the phylogenetically most widespread and striking patterns of diversity. In our study, we assess sex‐biased gene expression patterns across body regions and under different nutritional conditions and reveal how they are (1) unique to or shared across tissues; (2) how they are integrated at a functional level; and (3) how they diverge or are shared with genes whose expression contributes specifically to nutrition dependence.

Despite limitations on offspring production, almost all multicellular species use sex to reproduce. Sex gives rise to sexual selection, a widespread force operating through competition and choice within reproduction, however, it remains unclear whether sexual selection is beneficial for total lineage fitness, or if it acts as a constraint. Sexual selection could be a positive force because of selection on improved individual condition and purging of mutation load, summing into lineages with superior fitness. On the other hand, sexual selection could negate potential net fitness through the actions of sexual conflict, or because of tensions between investment in sexually selected and naturally selected traits. Here, we explore these ideas using a multigenerational invasion challenge to measure consequences of sexual selection for the overall net fitness of a lineage. After applying experimental evolution under strong versus weak regimes of sexual selection for 77 generations with the flour beetle Tribolium castaneum, we measured the overall ability of introductions from either regime to invade into conspecific competitor populations across eight generations. Results showed that populations from stronger sexual selection backgrounds had superior net fitness, invading more rapidly and completely than counterparts from weak sexual selection backgrounds. Despite comprising only 10% of each population at the start of the invasion experiment, colonizations from strong sexual selection histories eventually achieved near‐total introgression, almost completely eliminating the original competitor genotype. Population genetic simulations using the design and parameters of our experiment indicate that this invasion superiority could be explained if strong sexual selection had improved both juvenile and adult fitness, in both sexes. Using a combination of empirical and modeling approaches, our findings therefore reveal positive and wide‐reaching impacts of sexual selection for net population fitness when facing the broad challenge of invading competitor populations across multiple generations.

Single male sexually selected traits have been found to exhibit substantial genetic variance, even though natural and sexual selection are predicted to deplete genetic variance in these traits. We tested whether genetic variance in multiple male display traits of Drosophila serrata was maintained under field conditions. A breeding design involving 300 field-reared males and their laboratory-reared offspring allowed the estimation of the genetic variance-covariance matrix for six male cuticular hydrocarbons (CHCs) under field conditions. Despite individual CHCs displaying substantial genetic variance under field conditions, the vast majority of genetic variance in CHCs was not closely associated with the direction of sexual selection measured on field phenotypes. Relative concentrations of three CHCs correlated positively with body size in the field, but not under laboratory conditions, suggesting condition-dependent expression of CHCs under field conditions. Therefore condition dependence may not maintain genetic variance in preferred combinations of male CHCs under field conditions, suggesting that the large mutational target supplied by the evolution of condition dependence may not provide a solution to the lek paradox in this species. Sustained sexual selection may be adequate to deplete genetic variance in the direction of selection, perhaps as a consequence of the low rate of favorable mutations expected in multiple trait systems.

Sexually selected traits are predicted to show condition dependence by capturing the genetic quality of its bearer. In separate‐sexed organisms, this will ultimately translate into condition dependence of reproductive success of the sex that experiences sexual selection, which is typically the male. Such condition dependence of reproductive success is predicted to be higher in males than females under conditions promoting intense sexual selection. For simultaneous hermaphrodites, however, sex allocation theory predicts that individuals in poor condition channel relatively more resources into the male sex function at the expense of the female function. Thus, male reproductive success is expected to be less condition dependent than female reproductive success. We subjected individuals of the simultaneously hermaphroditic snail Physa acuta to two feeding treatments to test for condition dependence of male and female reproductive success under varying levels of male–male competition. Condition dependence was found for female, but not for male, reproductive success, meaning that selection on condition is relatively stronger through the female sex function. This effect was consistent over both male–male competition treatments. Decomposition of male and female reproductive performance revealed that individuals in poor condition copulated more in their male role, indicating an increased male allocation to mate acquisition. These findings suggest that sex‐specific condition dependence of reproductive success is at least partially driven by condition‐dependent sex allocation. We discuss the implications of condition‐dependent sex allocation for the evolution of sexually selected traits in simultaneous hermaphrodites.

The genic capture hypothesis implies that the expression of sexual ornaments largely depends on genes affecting resource acquisition and use. The ornaments should thus show high degree of directional dominance typical of life-history traits, and consequently, they should be severely affected by inbreeding. Here we investigated the effect of inbreeding on a sexual ornament (male eyespan) in stalk-eyed fly, Teleopsis dalmanni. For comparison, we also measured inbreeding depression in non-sexual morphological traits: female eyespan as well as wing and thorax lengths in both sexes. Both eyespan, and other morphological traits we measured, showed significant inbreeding depression. In accord with predictions of genic capture hypothesis, male eyespan did decrease under inbreeding significantly more than female eyespan. However, the decline in male eyespan was fully explained by overall decline in body length. Moreover, the magnitude of inbreeding depression in male eyespan was considerably lower than that typically observed for life-histories; in fact, it fitted within the range typically characterizing morphological traits. We therefore conclude that our results provide weak support for genic capture hypothesis.

In theory, females of many species choose mates based on traits that are indicators of male genetic quality. A fundamental question in evolutionary biology is why genetic variation for such indicator traits persists despite strong persistent selection imposed by female preference, which is known as the lek paradox. One potential solution to the lek paradox suggests that the traits that are targets of mate choice should evolve condition-dependent expression and that condition should have a large genetic variance. Condition is expected to exhibit high genetic variance because it is affected by a large number of physiological processes and hence, condition-dependent traits should 'capture' variation contributed by a large number of loci. We suggest that a potentially important cause of variation in condition is competition for limited resources. Here, we discuss a pair of models to analyze the evolutionary genetics of traits affected by success in social competition for resources. We show that competition can contribute to genetic variation of 'competition-dependent' traits that have fundamentally different evolutionary properties than other sources of variation. Competition dependence can make traits honest indicators of genetic quality by revealing the relative competitive ability of males, can provide a component of heritable variation that does not contribute to trait evolution, and can help maintain heritable variation under directional selection. Here we provide a general introduction to the concept of competition dependence and briefly introduce two models to demonstrate the potential evolutionary consequences of competition-dependent trait expression.