Resource-mediated condition dependence in sexually dichromatic butterfly wing coloration

Theory predicts that traits subject to strong sexual selection should evolve to be more exaggerated and developmentally integrated than nonsexual traits, thus leading to heightened condition dependence. Until recently, however, efforts to evaluate this prediction have suffered from either a purely correlational (nonmanipulative) approach, or from using manipulations of doubtful ecological relevance. Here I address these issues by integrating observation and manipulation to study condition- and sex-related color variation in a butterfly. The focal species, Eurema hecabe (Pieridae), possesses three sexually homologous and morphogenetically discrete dorsal wing color elements-coherently scattered ultraviolet (UV), pteridine yellow, and melaninic black. The UV is most strongly sexually selected, and is also the only color element with restricted distribution across female wings. Condition dependence and sexual dichromatism were pervasive, characterizing all color traits except the melanic black, and acting such that low condition males resembled high condition females. Although female coloration tended to exhibit greater phenotypic variation, size-scaled UV was more variable and condition dependent in males. Importantly, manipulation of larval resources was sufficient to closely reconstruct the extent and patterns of field-observed phenotypic variation in condition, and color trait expression, which implicates larval resource acquisition as a primary driver of condition dependence. These results support theories regarding phenotypic variation in sexually selected traits.     

Condition‐dependent expression of pre‐ and postcopulatory sexual traits in guppies

Female choice can impose persistent directional selection on male sexually selected traits, yet such traits often exhibit high levels of phenotypic variation. One explanation for this paradox is that if sexually selected traits are costly, only the fittest males are able to acquire and allocate the resources required for their expression. Furthermore, because male condition is dependent on resource allocation, condition dependence in sexual traits is expected to underlie trade‐offs between reproduction and other life‐history functions. In this study we test these ideas by experimentally manipulating diet quality (carotenoid levels) and quantity in the guppy (Poecilia reticulata), a livebearing freshwater fish that is an important model for understanding relationships between pre‐ and post‐copulatory sexually selected traits. Specifically, we test for condition dependence in the expression of pre‐ and postcopulatory sexual traits (behavior, ornamentation, sperm traits) and determine whether diet manipulation mediates relationships among these traits. Consistent with prior work we found a significant effect of diet quantity on the expression of both pre‐ and postcopulatory male traits; diet‐restricted males performed fewer sexual behaviors and exhibited significant reductions in color ornamentation, sperm quality, sperm number, and sperm length than those fed ad libitum. However, contrary to our expectations, we found no significant effect of carotenoid manipulation on the expression of any of these traits, and no evidence for a trade‐off in resource allocation between pre‐ and postcopulatory episodes of sexual selection. Our results further underscore the sensitivity of behavioral, ornamental, and ejaculate traits to dietary stress, and highlight the important role of condition dependence in maintaining the high variability in male sexual traits.     

Condition dependence and the maintenance of genetic variance in a sexually dimorphic black scavenger fly

The maintenance of genetic variation in traits under strong sexual selection is a longstanding problem in evolutionary biology. The genic capture model proposes that this problem can be explained by the evolution of condition dependence in exaggerated male traits. We tested the predictions that condition dependence should be more pronounced in male sexual traits and that genetic variance in expression of these traits should increase under stress as among‐genotype variation in overall condition is exposed. Genetic variance in female and nonsexual traits should, by contrast, be similar across environments as a result of stabilizing selection on trait expression. The relationship between the degree of sexual dimorphism, condition dependence and additive genetic variance (V_a) was assessed for two morphological traits (body size and relative fore femur width) affecting male mating success in the black scavenger fly Sepsis punctum (Diptera: Sepsidae) and for development time (a nonsexual trait often correlated with body size). We compared trait expression between the sexes for two cross‐continental populations that differ in degree of sexual dimorphism (Ottawa and Zurich). Condition dependence was indeed most pronounced in males of the strongly dimorphic Zurich population (males larger), and V_a was similar for males and females unless the trait was strongly sex specific and condition dependent. Contrary to prediction, however, V_a primarily increased under food limitation in both sexes, and genetic variance in fore femur width was low to nil, perhaps depleted by putatively strong sexual selection. Solely for body size of Zurich males, V_a increased more in males than females at limited food, in accordance with the predictions of the genic capture model. Overall therefore, quantitative genetic evidence in support of the model was inconsistent and weak at best.     

Social effects for locomotion vary between environments in Drosophila melanogaster females

Despite strong purifying or directional selection, variation is ubiquitous in populations. One mechanism for the maintenance of variation is indirect genetic effects (IGEs), as the fitness of a given genotype will depend somewhat on the genes of its social partners. IGEs describe the effect of genes in social partners on the expression of the phenotype of a focal individual. Here, we ask what effect IGEs, and variation in IGEs between abiotic environments, has on locomotion in Drosophila. This trait is known to be subject to intralocus sexually antagonistic selection. We estimate the coefficient of interaction, Ψ, using six inbred lines of Drosophila. We found that Ψ varied between abiotic environments, and that it may vary across among male genotypes in an abiotic environment specific manner. We also found evidence that social effects of males alter the value of a sexually dimorphic trait in females, highlighting an interesting avenue for future research into sexual antagonism. We conclude that IGEs are an important component of social and sexual interactions and that they vary between individuals and abiotic environments in complex ways, with the potential to promote the maintenance of phenotypic variation.     

Condition dependence of sexually dimorphic colouration and longevity in the ambush bug Phymata americana

Sexually selected traits that are costly are predicted to be more condition dependent than nonsexually selected traits. Assuming resource limitation, increased allocation to a sexually selected trait may also come at a cost to other fitness components. To test these predictions, we varied adult food ration to manipulate condition in the colour dimorphic bug, Phymata americana. We compared the degree of condition dependence in a sexually selected trait expressed in males to a nonsexually selected trait expressed in males and females. We also evaluated the effects of condition on longevity of both sexes. We found that the expression of these colour pattern traits was strongly influenced by both diet and age. As expected, the strength of condition dependence was much more pronounced in the sexually selected, male-limited trait but the nonsexual trait also exhibited significant condition dependence in both sexes. The sexually selected male trait also exhibited a higher coefficient of phenotypic variation than the nonsexually selected trait in males and females. Diet had contrasting effects on male and female longevity; increased food availability had positive effects on female lifespan but these effects were not detected in males, suggesting that males allocated limited resources preferentially to sexually selected traits. These results are consistent with the expectation that optimal allocation to various fitness components differs between the sexes.     

Parasitism and the expression of sexual dimorphism

Although a negative covariance between parasite load and sexually selected trait expression is a requirement of few sexual selection models, such a covariance may be a general result of life‐history allocation trade‐offs. If both allocation to sexually selected traits and to somatic maintenance (immunocompetence) are condition dependent, then in populations where individuals vary in condition, a positive covariance between trait expression and immunocompetence, and thus a negative covariance between trait and parasite load, is expected. We test the prediction that parasite load is generally related to the expression of sexual dimorphism across two breeding seasons in a wild salamander population and show that males have higher trematode parasite loads for their body size than females and that a key sexually selected trait covaries negatively with parasite load in males. We found evidence of a weaker negative relationship between the analogous female trait and parasite infection. These results underscore that parasite infection may covary with expression of sexually selected traits, both within and among species, regardless of the model of sexual selection, and also suggest that the evolution of condition dependence in males may affect the evolution of female trait expression.     

Stronger condition dependence in female size explains altitudinal variation in sexual size dimorphism of a Tibetan frog

The present study investigated altitudinal variation in sexual size dimorphism of a Tibetan frog Nanorana parkeri. Size dimorphism was female‐biased in all populations, although this bias became less at higher altitudes because of a steeper altitudinal decrease in female size than male size. Operational sex ratios, an indicator of the opportunity for sexual selection on larger males, changed independently of altitude. Clutch volume, an indicator of the strength of fecundity selection on larger females, was positively with female size, and tended to decrease approaching high altitudes. Females lived longer and grew more slowly than males, and the mean age in both sexes increased and growth rate decreased altitudinally, although the changes were more rapid in females than males. These results suggest that, relative to males, females (i.e. the sex that typically bears greater reproductive costs and experiences stronger directional selection for larger size to take fecundity advantages) should be more sensitive to environments, attaining a larger size via enhancing growth under favourable lower‐latitude conditions but a smaller size as a result of retarding growth when conditions become harsher at higher altitudes. This supports the condition‐dependence hypothesis with respect to intraspecific variation in sexual size dimorphism. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 558–565.     

Impacts of diet quality on life‐history and reproductive traits in male and female armed beetle,Gnatocerus cornutus

1. The energy available for reproduction is usually limited by resource acquisition (i.e. condition). Because condition is known to be strongly affected by environmental factors, reproductive investments also vary across heterogeneous environments. 2. Although the condition dependence of reproductive investment is common to both sexes, reproductive traits may exhibit sexually different responses to environmental fluctuation due to sex‐specific life‐history strategies. However, few direct experimental studies have investigated the condition dependence of reproductive investments in both sexes. 3. We investigated the condition dependence of life‐history and reproductive traits of males and females in the beetle Gnatocerus cornutus Fabricus by manipulating larval and adult diet quality. We found that male and female life‐history traits exhibited similar responses to environmental fluctuations. 4. By contrast, the sexes exhibit different patterns of condition dependence in reproductive traits (i.e. the adult nutritional environment has a strong impact on the female lifetime reproductive success, whereas larval nutritional environment strongly affects the secondary sexual trait in males). 5. This difference in the plasticity of reproductive traits may lead to different selection pressures for each sex, even if both sexes develop and/or live in the same environment.     

The evolution of condition-dependent sexual dimorphism

Theory suggests that the net benefit of allocating resources to a sexual trait depends both on the strength of sexual selection on that trait and on individual condition. This predicts a tight coevolution between sexual dimorphism and condition dependence and suggests that these patterns of within-sex and between-sex variation may share a common genetic and developmental basis. Although condition-dependent expression of sexual traits is widely documented, the extent of covariation between condition dependence and sexual dimorphism remains poorly known. I investigated the effects of condition (larval diet quality) on multivariate sexual dimorphism in the fly Telostylinus angusticollis (Neriidae). Condition determined the direction of sexual size dimorphism and modulated sexual shape dimorphism by affecting allometric slopes and/or intercepts of sexually homologous traits in both sexes. Although the greatest responses to condition manipulation were observed in male sexual traits, both sexual and nonsexual traits exhibited substantial variation in the nature and magnitude of condition effects. Nonetheless, condition dependence and sexual dimorphism were remarkably congruent: variation in the strength of condition effects on male traits explained more than 90% of the variation in the magnitude of sexual dimorphism, whether quantified in terms of trait size or allometric slope. The genetic mechanisms that give rise to multivariate sexual dimorphism in body shape thus function in a strongly condition-dependent manner in this species, suggesting a common genetic basis for body shape variation within and between sexes.     

Condition dependence of developmental stability in the sexually dimorphic fly Telostylinus angusticollis (Diptera: Neriidae)

Developmental stability is widely regarded as a condition‐dependent trait, but its relation to genotype and environment, and extent of developmental integration, remain contentious. In Telostylinus angusticollis, the dorsocentral bristles exhibit striking variation in developmental stability, manifested as fluctuating asymmetry (FA) in bristle position (‘positional FA’) and failure to develop some bristles (‘bristle loss’), in natural and laboratory populations. To determine whether this variation reflects condition, I tested for effects of genotype and environment (larval diet quality), and examined covariation with condition‐dependent traits. Positional FA was not affected by genotype or environment. However, positional FA covaried negatively with secondary sexual trait expression in males, and with sexual dimorphism in body shape, but covaried positively with body size in females. Bristle loss reflected both genotype and larval diet. Flies reared on poor‐quality diet exhibited a similar rate of bristle loss as wild flies. Both positional FA and bristle loss were greater in males. These results suggest that the relation between developmental stability and condition is complex and sex dependent.     

Plasticity of size and allometry in multiple sexually selected traits in an armed beetle <Emphasis Type="Italic">Gnatocerus cornutus</Emphasis>

Male-male competition frequently results in the evolution of sexually selected traits used as weapons and ornaments. The expression of these traits often depends on male condition, i.e., condition dependence. Although males often have multiple sexually selected traits, to date many studies have focused on the morphological analysis of one sexual trait whilst ignoring the others. We here report phenotypic plasticity for multiple sexual traits, by manipulating larval diet quality and density, in the broad-horned flour beetle Gnatocerus cornutus. The male beetles possess enlarged mandibles, developed genae and a pair of small horns, but females lack these completely. Larval density significantly affected overall body size but not relative investment in each sexual trait. In contrast, diet quality had no effect on body size but had a significant effect on relative investment in the mandibles and genae. These results indicate that the allometric intercepts of the mandible and genae alter in response to diet quality, i.e., allometric plasticity. However, diet quality had no effect on the growth of the horn. Thus, multiple sexual traits exhibited differences in plasticity as a result of larval nutrient condition in G. cornutus males.     

The tale of the shrinking weapon: seasonal changes in nutrition affect weapon size and sexual dimorphism,but not contemporary evolution

Sexually selected traits are often highly variable in size within populations due to their close link with the physical condition of individuals. Nutrition has a large impact on physical condition, and thus, any seasonal changes in nutritional quality are predicted to alter the average size of sexually selected traits as well as the degree of sexual dimorphism in populations. However, although traits affected by mate choice are well studied, we have a surprising lack of knowledge of how natural variation in nutrition affects the expression of sexually selected weapons and sexual dimorphism. Further, few studies explicitly test for differences in the heritability and mean‐scaled evolvability of sexually selected traits across conditions. We studied Narnia femorata (Hemiptera: Coreidae), an insect where males use their hind legs as weapons and the femurs are enlarged, to understand the extent to which weapon expression, sexual dimorphism and evolvability change across the actual range of nutrition available in the wild. We found that insects raised on a poor diet (cactus without fruit) are nearly monomorphic, whereas those raised on a high‐quality diet (cactus with ripe fruit) are distinctly sexually dimorphic via the expression of large hind leg weapons in males. Contrary to our expectations, we found little evidence of a potential for evolutionary change for any trait measured. Thus, although we show weapons are highly condition dependent, and changes in weapon expression and dimorphism could alter evolutionary dynamics, our populations are unlikely to experience further evolutionary changes under current conditions.     

FLUCTUATING ASYMMETRY IS NONGENETICALLY RELATED TO MATING SUCCESS IN DROSOPHILA BUZZATII

Abstract To date, there is still no consensus on the real significance of fluctuating asymmetry (FA) in evolutionary biology. Some studies have established links between FA and Darwinian fitness, and in a number of cases intermediate heritabilities for FA have been reported. However, many claims have been raised against the generality of these findings. I therefore tested if FA of a sexually selected trait (wing length) is indeed related to male mating success in Drosophila buzzatii from field and laboratory samples and whether FA has detectable heritability. Single, unsuccessful males had greater asymmetry for wing length than their mating counterparts both in nature and under nonoptimal rearing environments, but the higher FA in single males is most likely due to a poorer average phenotypic condition because there was no evidence of a genetic basis for this trait. Further evidence of an increase in FA under larval food stress is suggested when comparing the magnitude of the FA levels between stressful and optimal environments. On methodological grounds, a linear model is suggested that allows directional asymmetry (DA) and any genetic variation of DA that may be present to be statistically eliminated from estimates of FA.     

Fluctuating asymmetry,body size and sexual selection in the dung fly Sepsis cynipsea — testing the good genes assumptions and predictions

In the dung fly Sepsis cynipsea large and more symmetric males have been shown to enjoy a mating advantage, but we still do not know which mechanism of sexual selection is responsible. Here we test several assumptions and predictions relating to the hypothesis that either trait is indicative of ‘good genes’. We tested for good genes by regressing fitness in good and bad environments (no and high larval competition, respectively) on the family mean for size or asymmetry as expressed in the good environment, separately for both sexes. Body size (hind tibia length or head width) was positively correlated with female fecundity, growth rate of both sexes and larval survivorship for males, but only in the good environment. The corresponding evidence for asymmetry is more equivocal. Mean standardised asymmetry was weakly associated with lower survivorship in the good environment, while growth rates and female fecundity were not. As predicted by sexual selection theory, fore tibia length showed greater asymmetry than other, presumably not sexually selected traits, and asymmetry in fore tibia length was greater for males than females. However, a negative correlation between trait size and asymmetry was only evident for male seta length but not for fore tibia length, fore femur length, or any composite measure of asymmetry. Most crucially, asymmetry was heritable for some female morphological traits (hind tibia length: h² = 0.15; fore femur length: h² = 0.16; mean of all measured traits: h² = 0.27), but not for any male trait. Also, asymmetry of the various traits measured was not correlated within males and only weakly so within females. The crucial assumption that asymmetry of sexually selected traits reflects overall, heritable developmental stability of an individual is thus only partly substantiated by our data. In contrast, large body size is heritable, associated with high fitness and consequently could be indicative of good genes. Fore leg asymmetry may influence male mating success by simply mechanically constraining his ability to hold on to the female.     

An assessment of Putative Sexually Antagonistic Traits in a Freshwater Amphipod Species

Sexual conflict can result in an ‘evolutionary arms race’ between males and females, with the evolution of sexual antagonistic traits used to resolve the conflict in favor of one sex over the other. We assessed the resolution of sexual conflict in a Hyalella amphipod species by manipulating putative sexually antagonistic traits in males and females and used mate‐guarding duration as our metric of conflict resolution. We discovered that large male posterior gnathopod size increased mate‐guarding duration, which suggests that it is a sexually antagonistic trait in this species. In contrast, female and male body size did not significantly affect mate‐guarding duration. Given that male posterior gnathopods show heightened condition dependence, future investigations should explore the interactive effects of sexual conflict and ecological context on trait evolution, phenotypic divergence, and speciation to elucidate the complex mechanisms involved in the evolution of biological diversity.     

CONDITION DEPENDENCE OF A SEXUALLY SELECTED TRAIT IN A CRUSTACEAN SPECIES COMPLEX: IMPORTANCE OF THE ECOLOGICAL CONTEXT

The genic capture model offers a promising solution to the lek paradox. Heightened condition dependency of sexually selected traits is a prerequisite of this model. Condition dependency is empirically inferred by the sensitivity of traits to stressors. The magnitude of ecological stress (e.g., competition and predation) experienced by populations varies considerably. Thus, condition dependence should manifest more in populations experiencing higher levels of stress. We experimentally assessed the sensitivity of a sexually selected trait (posterior gnathopod) to food resource stress in an amphipod species. We found that gnathopod size variation was 59% higher under food stress, with no corresponding effect on nonsexually selected traits. In addition, we assessed levels of gnathopod variation and the allometry of gnathopods for males sampled from natural populations for two amphipod species that experience different levels of stress (driven by contrasting size‐selective predation and associated life‐history trade‐offs). Populations that experience higher resource stress had both steeper allometries and greater gnathopod size variation. These results suggest that the magnitude of ecological stress experienced by natural populations strongly impacts condition dependency of sexually selected traits, and could play an important role in shaping trait variation and thus the opportunity for sexual selection.     

Heightened Condition Dependence of a Sexually Selected Signal in Male Polistes dominulus Paper Wasps

Sexually selected signals are theoretically expected to exhibit heightened condition dependence compared to non‐signaling traits. This link to condition enables sexual signals to provide information regarding individual quality and also provides a mechanism that allows animals to develop signals that accurately reflect their abilities. Most previous work on sexual signal condition dependence has focused on signals that have clear developmental costs, while less is known about the development of other types of quality signals. Male Polistes dominulus paper wasps have yellow‐on‐black abdominal spots that are important signals during female choice and male–male competition. These signals lack obvious production costs, as males are covered in yellow and black patterns composed of the same pigments. Here, we assess signal condition dependence by testing whether larval diet has a stronger influence on the development of male spots than on the development of control traits composed of the same pigments. Males reared on ad libitum diets developed elliptical spots similar to those seen on dominant, attractive males, while males reared on restricted diets developed irregularly shaped spots similar to those seen on subordinate, unattractive males. Remarkably, the development of a control trait composed of the same yellow and black pigments was not influenced by larval diet. Therefore, sexually selected signals can be developmentally decoupled from traits comprised of the same pigments. Condition dependence of sexually selected signals is likely to be a widespread solution to the challenge of developing sexually selected signals that accurately convey information about individual quality.     

Sexual selection and population divergence I: The influence of socially flexible cuticular hydrocarbon expression in male field crickets (Teleogryllus oceanicus)

Debates about how coevolution of sexual traits and preferences might promote evolutionary diversification have permeated speciation research for over a century. Recent work demonstrates that the expression of such traits can be sensitive to variation in the social environment. Here, we examined social flexibility in a sexually selected male trait—cuticular hydrocarbon (CHC) profiles—in the field cricket Teleogryllus oceanicus and tested whether population genetic divergence predicts the extent or direction of social flexibility in allopatric populations. We manipulated male crickets’ social environments during rearing and then characterized CHC profiles. CHC signatures varied considerably across populations and also in response to the social environment, but our prediction that increased social flexibility would be selected in more recently founded populations exposed to fluctuating demographic environments was unsupported. Furthermore, models examining the influence of drift and selection failed to support a role of sexual selection in driving population divergence in CHC profiles. Variation in social environments might alter the dynamics of sexual selection, but our results align with theoretical predictions that the role social flexibility plays in modulating evolutionary divergence depends critically on whether responses to variation in the social environment are homogeneous across populations, or whether gene by social environment interactions occur.     

Maintenance of variation in sexually selected traits in females: a case study using intrasexual aggression in tree swallows Tachycineta bicolor

A fundamental question in evolutionary biology is how phenotypic variation is maintained in the face of selection that ought to deplete that variation. Much research has investigated this question in traits favored via sexual selection in males, with a common solution implicating the condition dependence of sexually selected phenotypes. Despite growing interest in sexual selection on females, it is not clear if the same mechanisms maintain variation in female ornaments, weaponry or other female behaviors targeted by sexual selection. An important step in testing condition dependence in females is thus to identify whether sexually selected female phenotypes are associated with condition and also with potential costs. Here, I examine these two components of condition dependence for a sexually selected behavior, intrasexual aggression, in female tree swallows Tachycineta bicolor. I asked whether high levels of intrasexual aggression map onto natural variation in female condition and whether aggression is associated with one potential behavioral cost: performance in a vertically challenging test of flight. More aggressive females were heavier for their body size, heavier for their wing size and showed decreased flight ability, relative to less aggressive females. These findings are consistent with condition dependence, where only females in better condition are able to be highly aggressive. The association between high aggression and reduced flight ability may result from the additional lift required to power these relatively heavier birds. These associations between natural variation in aggressive behavior, morphology and flight ability are consistent with condition dependence because they confirm two basic assumptions of condition dependence: a link between aggression and condition, and a link between aggression and a behavioral cost, the speed of escape flight. As the first study to examine these assumptions for a conspicuous behavior favored by intrasexual selection in females, this study suggests broad relevance of condition dependence.     

The juvenile social environment introduces variation in the choice and expression of sexually selected traits

The juvenile environment provides numerous cues of the intensity of competition and the availability of mates in the near environment. As research demonstrates that the developing individuals can use these cues to alter their developmental trajectories, and therefore, adult phenotypes, we examined whether social cues available during development can affect the expression and the preference of sexually selected traits. To examine this, we used the Australian black field cricket (Telogryllus commodus), a species where condition at maturity is known to affect both male calling effort and female choice. We mimicked different social environments by rearing juveniles in two different densities crossed with three different calling environments. We demonstrate that the social environment affected female response speed but not preference, and male age-specific calling effort (especially the rate of senescence in calling effort) but not the structural/temporal parameters of calls. These results demonstrate that the social environment can introduce variation in sexually selected traits by modifying the behavioral components of male production and female choice, suggesting that the social environment may be an overlooked source of phenotypic variation. We discuss the plasticity of trait expression and preference in reference to estimations of male quality and the concept of condition dependence.