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Data from: Dietary stress does not strengthen selection against single deleterious mutations in Drosophila melanogaster
Rundle, Howard D.; MacLellan, Kelsie; Kwan, Lucia; Whitlock, Michael C. — 2011-06-13 Stress is generally thought to increase the strength of selection, although empirical results are mixed and general conclusions are difficult because data are limited. Here we compare the fitness effects of nine independent recessive mutations in Drosophila melanogaster in a high- and low-dietary-stress environment, estimating the strength of selection on these mutations arising from both a competitive measure of male reproductive success and productivity (female fecundity and the subsequent survival to adulthood of her offspring). The effect of stress on male reproductive success has not been addressed previously for individual loci and is of particular interest with respect to the alignment of natural and sexual selection. Our results do not support the hypothesis that stress increases the efficacy of selection arising from either fitness component. Results concerning the alignment of natural and sexual selection were mixed, although data are limited. In the low-stress environment, selection on mating success and productivity were concordant for five of nine mutations (four out of four when restricted to those with significant or near-significant productivity effects), whereas in the high-stress environment, selection aligned for seven of nine mutations (two out of two when restricted to those having significant productivity effects). General conclusions as to the effects of stress on the strength of selection and the alignment of natural and sexual selection await data from additional mutations, fitness components and stressors.
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Data from: Quantitative genetics of female mate preferences in an ancestral and a novel environment
Delcourt, Matthieu; Blows, Mark W.; Rundle, Howard D. — 2012-01-10 A female’s mate preference is a potentially complex function relating variation in multiple male phenotypes with her probability of accepting individual males as a mate. Estimating the quantitative genetic basis of preference functions within a population is empirically challenging yet key to understanding preference evolution. We employed a recently described approach that uses random-coefficient mixed models in the analysis of function-valued traits. Using a half-sibling breeding design in a laboratory-adapted Drosophila serrata population, we estimated the genetic (co)variance function of female preference for male sexual displays composed of nine contact pheromones. The breeding design was performed across two environments: the food to which the population was well adapted and a novel food that reduced average female productivity by 35%. Significant genetic variance in female preference was detected and the majority (64.2%) was attributable to a single genetic dimension (eigenfunction), suggesting that preferences for different pheromones are not genetically independent. The second eigenfunction, accounting for 24% of the total genetic variance, approached significance in a conservative test, suggesting the existence of a second, independent genetic dimension. There was no evidence that the genetic basis of female preference differed between the two environments, suggesting the absence of genotype-by-environment interactions and hence a lack of condition-dependent preference expression.
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Data from: Reduced genetic variance among high fitness individuals: inferring stabilizing selection on male sexual displays in D. serrata
Sztepanacz, Jacqueline L.; Rundle, Howard D. — 2012-03-23 Directional selection is prevalent in nature yet phenotypes tend to remain relatively constant, suggesting a limit to trait evolution. However, the genetic basis of this limit is unresolved. Given widespread pleiotropy, opposing selection on a trait may arise from the effects of the underlying alleles on other traits under selection, generating net stabilizing selection on trait genetic variance. These pleiotropic costs of trait exaggeration may arise through any number of other traits, making them hard to detect in phenotypic analyses. Stabilizing selection can be inferred, however, if genetic variance is greater among low compared to high fitness individuals. We extend a recently suggested approach to provide a direct test of a difference in genetic variance for a suite of cuticular hydrocarbons (CHCs) in Drosophila serrata. Despite strong directional sexual selection on these traits, genetic variance differed between high and low fitness individuals and was greater among the low fitness males for seven of eight CHCs, significantly more than expected by chance. Univariate tests of a difference in genetic variance were non-significant but likely have low power. Our results suggest that further CHC exaggeration in D. serrata in response to sexual selection is limited by pleiotropic costs mediated through other traits.
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Data from: Remating and sperm competition in replicate populations of Drosophila melanogaster adapted to alternative environments
Arbuthnott, Devin; Agrawal, Aneil F.; Rundle, Howard D. — 2015-01-31 The prevalence of sexual conflict in nature, as well as the supposedly arbitrary direction of the resulting coevolutionary trajectories, suggests that it may be an important driver of phenotypic divergence even in a constant environment. However, natural selection has long been central to the operation of sexual conflict within populations and may therefore constrain or otherwise direct divergence among populations. Ecological context may therefore matter with respect to the diversification of traits involved in sexual conflict, and if natural selection is sufficiently strong, such traits may evolve in correlation with environment, generating a pattern of ecologically-dependent parallel evolution. In this study we assess among-population divergence both within and between environments for several traits involved in sexual conflict. Using eight replicate populations of Drosophila melanogaster from a long-term evolution experiment, we measured remating rates and subsequent offspring production of females when housed with two separate males in sequence. We found no evidence of any variation in male reproductive traits (offense or defense). However, the propensity of females to remate diverged significantly among the eight populations with no evidence of any environmental effect, consistent with sexual conflict promoting diversification even in the absence of ecological differences. On the other hand, females adapted to one environment (ethanol) tended to produce a higher proportion of offspring sired by their first mate as compared to those adapted to the other (cadmium) environment, suggesting ecologically-based divergence of this conflict phenotype. Because we find evidence for both stochastic population divergence operating outside of an ecological context and environment-dependent divergence of traits under sexual conflict, the interaction of these two processes is an important topic for future work.
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Data from: Sexually antagonistic genetic variance for fitness in an ancestral and a novel environment
Delcourt, Matthieu; Blows, Mark W.; Rundle, Howard D. — 2012-01-10 The intersex genetic correlation for fitness (rwfm), a standardized measure of the degree to which male and female fitness covary genetically, has consequences for important evolutionary processes, but few estimates are available and none have explored how it changes with environment. Using a half-sibling breeding design, we estimated the genetic (co)variance matrix (G) for male and female fitness, and the resulting rwfm,in Drosophila serrata. Our estimates were performed in two environments: the laboratory yeast food to which the population was well adapted and a novel corn food. The major axis of genetic variation for fitness in the two environments, accounting for 51.3 per cent of the total genetic variation, was significant and revealed a strong signal of sexual antagonism, loading negatively in both environments on males but positively on females. Consequently, estimates of rwfm were negative in both environments (-0.34 and -0.73, respectively), indicating that the majority of genetic variance segregating in this population has contrasting effects on male and female fitness. The possible strengthening of the negative rwfm in this novel environment may be a consequence of no history of selection for amelioration of sexual conflict. Additional studies from a diverse range of novel environments will be needed to determine the generality of this finding.
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On male harm: How it is measured and how it evolves in different environments
Rundle, Howard D.; Yun, Li; Agrawal, Aneil F. — 2021-04-29 <p>Males can harm the females they interact with, but populations/species vary widely in the occurrence and extent of harm. We consider the merits and limitations of two common approaches to investigating male harm and apply these to an experimental study of divergence in harm. Different physical environments can affect how the sexes interact, causing plastic and/or evolved changes in harm. If harmful male phenotypes are less likely to evolve in situations where females have more control over sexual interactions, populations evolving in environments in which females have greater control should have less harmful males. We test this idea using experimental populations of <em>Drosophila melanogaster</em> that have evolved in either of two environments that vary in the extent to which females can avoid males, or in a third environment without mate competition (i.e., enforced monogamy). We demonstrate an evolved reduction in harm in the absence of mate competition and also in a mate competition environment in which females have greater control. We also show a plastic effect in that otherwise harmful males are no longer so when tested in the environment in which females have greater control. Our results reveal the different perspectives provided by the two methods of studying harm.</p>
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Data from: Environmental complexity and the purging of deleterious alleles
Singh, Amardeep; Agrawal, Aneil F.; Rundle, Howard D. — 2017-07-31 Sexual interactions among adults can generate selection on both males and females with genome-wide consequences. Sexual selection through males is one component of this selection that has been argued to play an important role in purging deleterious alleles. A common technique to assess the influence of sexual selection is by a comparison of experimental evolution under enforced monogamy vs. polygamy. Mixed results from past studies may be due to the use of highly simplified lab conditions that alter the nature of sexual interactions. Here we examine the rate of purging of 22 gene disruption mutations in experimental polygamous populations of Drosophila melanogaster in each of two mating environments: a simple, high density environment (i.e., typical fly vials) and a lower density, more spatially complex environment. Based on past work, we expect sexual interactions in the latter environment to result in stronger selection in both sexes. Consistent with this, we find that mutations tend to be purged more quickly in populations evolving in complex environments. We discuss possible mechanisms by which environmental complexity might modulate the rate at which deleterious alleles are purged and putatively ascribe a role for sexual interactions in explaining the treatment differences in our experiment.
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Data from: Evolutionary optimum for male sexual traits characterized using the multivariate Robertson–Price Identity
Delcourt, Matthieu; Blows, Mark W.; Aguirre, J. David; Rundle, Howard D. — 2012-12-10 Phenotypes tend to remain relatively constant in natural populations, suggesting a limit to trait evolution. Although stationary phenotypes suggest stabilizing selection, directional selection is more commonly reported. However, selection on phenotypes will have no evolutionary consequence if the traits do not genetically covary with fitness, a covariance known as the Robertson–Price Identity. The nature of this genetic covariance determines if phenotypes will evolve directionally or whether they reside at an evolutionary optimum. Here, we show how a set of traits can be shown to be under net stabilizing selection through an application of the multivariate Robertson–Price Identity. We characterize how a suite of male sexual displays genetically covaries with fitness in a population of Drosophila serrata. Despite strong directional sexual selection on these phenotypes directly and significant genetic variance in them, little genetic covariance was detected with overall fitness. Instead, genetic analysis of trait deviations showed substantial stabilizing selection on the genetic variance of these traits with respect to overall fitness, indicating that they reside at an evolutionary optimum. In the presence of widespread pleiotropy, stabilizing selection on focal traits will arise through the net effects of selection on other, often unmeasured, traits and will tend to be stronger on trait combinations than single traits. Such selection may be difficult to detect in phenotypic analyses if the environmental covariance between the traits and fitness obscures the underlying genetic associations. The genetic analysis of trait deviations provides a way of detecting the missing stabilizing selection inferred by recent metaanalyses.
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Data from: Competition for mates and the improvement of nonsexual fitness
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Yun, Li; Chen, Patrick J.; Kwok, Kevin E.; Angell, Christopher S.; Rundle, Howard D.; Agrawal, Aneil F. — 2019-05-25 Competition for mates can be a major source of selection, not just on secondary sexual traits but across the genome. Mate competition strengthens selection on males via sexual selection, which typically favours healthy, vigorous individuals and, thus, all genetic variants that increase overall quality. However, recent studies suggest another major effect of mate competition that could influence genome-wide selection: sexual harassment by males can drastically weaken selection on quality in females. Because of these conflicting effects, the net effect of mate competition is uncertain, though perhaps not entirely unpredictable. We propose that the environment in which mate competition occurs mediates the importance of sexual selection relative to sexual conflict, and hence the net effect of mate competition on nonsexual fitness. To test this, we performed experimental evolution with 63 fruit fly populations adapting to novel larval conditions where each population was maintained with or without mate competition. In half the populations with mate competition, adults interacted in simple, high-density environments. In the remainder, adults interacted in more spatially complex environments in which male-induced harm is reduced. Populations evolving with mate competition in the complex environment adapted faster to novel larval environments than did populations evolving without mate competition or with mate competition in the simple environment. Moreover, mate competition in the complex environment caused a substantial reduction in inbreeding depression in egg-to-adult viability relative to the other two mating treatments. These results demonstrate that the mating environment has a substantial and predictable effect on nonsexual fitness through adaptation and purging.
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Data from: Comparing the intersex genetic correlation for fitness across novel environments in the fruit fly, Drosophila serrata
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Punzalan, David; Delcourt, Matthieu; Rundle, Howard D. — 2013-08-08 Sexually antagonistic genetic variation can pose limits to the independent evolution and adaptation of the sexes. The extent of sexually antagonistic variation is reflected in the intersex genetic correlation for fitness (rwFM). Previous estimates of this correlation have been mostly limited to populations in environments to which they are already well adapted, making it difficult to gauge the importance of sexually antagonistic genetic variance during the early stages of adaptation, such as that occurring following abrupt environmental change or upon the colonization of new habitat. Here we assayed male and female lifetime fitness in a population of Drosophila serrata in four novel laboratory environments. We found that rwFM varied significantly across environments, with point estimates ranging from positive to negative values of considerable magnitude. We also found that the variability among estimates was because, at least in part, of significant differences among environments in the genetic variances of both male and female fitness, with no evidence of any significant changes in the intersex covariance itself, although standard errors of these estimates were large. Our results illustrate the unpredictable nature of rwFM in novel environments and suggest that, although sexually antagonistic genetic variance can be pronounced in some novel environments, it may have little effect in constraining the early stages of adaptation in others.
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Data from: Experimental evidence of condition-dependent sexual dimorphism in the weakly dimorphic antler fly, Protopiophila litigata (Diptera: Piophilidae)
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Oudin, Mathieu J.; Bonduriansky, Russell; Rundle, Howard D. — 2015-03-10 Sexually dimorphic traits have a history of directional selection for exaggeration in at least one sex. Theory suggests that traits targeted by persistent selection should evolve heightened condition dependence whereby their expression reflects the availability and processing efficiency of metabolic resources. This joint dependence of sexual dimorphism and condition dependence on directional selection should result in a positive correlation between the extent of sexual dimorphism and the strength of condition dependence. However, because direct phenotypic evidence is predominately from species with highly exaggerated male traits, it remains unclear whether condition-dependent sexual dimorphism is characteristic of species with more typical levels of dimorphism. We manipulated condition via larval diet and quantified sex-specific responses in adult body size and shape in a moderately dimorphic dipteran species, the antler fly Protopiophila litigata. While dimorphism did not increase with diet quality within any trait, among traits the extent of dimorphism was positively associated with the strength of condition dependence in males but not females, as previously reported for highly dimorphic species. This finding suggests that a shared developmental basis to condition dependence and sexual dimorphism can arise via sexual selection on males even in lineages lacking highly exaggerated male traits.
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Data from: Air-borne genotype by genotype indirect genetic effects are substantial in the filamentous fungus Aspergillus nidulans
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Rode, Nicolas O.; Soroye, Peter; Kassen, Rees; Rundle, Howard D. — 2017-01-30 Genotype by genotype indirect genetic effects (G × G IGEs) occur when the phenotype of an individual is influenced by an interaction between its own genotype and those of neighbour individuals. Little is known regarding the relative importance of G × G IGEs compared with other forms of direct and indirect genetic effects. We quantified the relative importance of IGEs in the filamentous fungus Aspergillus nidulans, a species in which IGEs are likely to be important as air-borne social interactions are known to affect growth. We used a collection of distantly related wild isolates, lab strains and a set of closely related mutation accumulation lines to estimate the contribution of direct and indirect genetic effects on mycelium growth rate, a key fitness component. We found that indirect genetic effects were dominated by G × G IGEs that occurred primarily between a focal genotype and its immediate neighbour within a vertical stack, and these accounted for 11% of phenotypic variation. These results indicate that G × G IGEs may be substantial, at least in some systems, and that the evolutionary importance of these interactions may be underappreciated, especially in microbes. We advocate for a wider use of the IGE framework in both applied (for example, choice of varietal mixtures in plant breeding) and evolutionary genetics (kin selection/kin competition studies).
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Data from: Reproductive character displacement of female mate preferences for male cuticular hydrocarbons in Drosophila subquinaria
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Rundle, Howard D.; Dyer, Kelly A. — 2015-08-17 Several lines of evidence implicate sexual isolation in both initiating and completing the speciation process. While its existence is straightforward to demonstrate, understanding the evolution of sexual isolation requires identifying the underlying phenotypes responsible so that we can determine how these have diverged. Here we study geographic variation in female mate preferences for male sexual displays in the fly Drosophila subquinaria. Female D. subquinaria that are sympatric with its sister species D. recens discriminate strongly against both D. recens and allopatric conspecific males, whereas females from allopatric populations do not. Furthermore, female mate preferences target at least in part a suite of cuticular hydrocarbons (CHCs) in males and geographic variation in CHCs mirrors the pattern of mate discrimination. In this study we quantify female mate preferences for male CHCs from populations that span the geographic range of D. subquinaria. We find that the direction of linear sexual selection varies significantly between populations that are sympatric vs. allopatric with D. recens in a pattern of reproductive character displacement. Differences in preference partially align with existing differences in CHCs and patterns of sexual isolation, although discrepancies remain that suggest the involvement of additional traits and/and more complex, nonlinear preference functions.
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Data from: Sexual selection is ineffectual or inhibits the purging of deleterious mutations in Drosophila melanogaster
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Arbuthnott, Devin; Rundle, Howard D. — 2012-01-19 The effects of sexual selection on population mean fitness are unclear and a subject of debate. Recent models propose that, because reproductive success may be condition-dependent, much of the genome may be a target of sexual selection. Under this scenario, mutations that reduce health, and thus non-sexual fitness, may also be deleterious with respect to reproductive success, meaning that sexual selection may contribute to the purging of deleterious alleles. We tested this hypothesis directly by subjecting replicate Drosophila melanogaster populations to two treatments that altered the opportunity for sexual selection and then tracked changes in the frequency of six separate deleterious alleles with recessive and visible phenotypic effects. While natural selection acted to decrease the frequency of all six mutations, the addition of sexual selection did not aid in the purging of any of them, and for three of them appears to have hampered it. Courtship and mating have harmful effects in this species and mate choice assays showed that males directed more courtship and mating behavior towards wild-type over mutant females, providing a likely explanation for sexual selection’s cost. Whether this cost extends to other mutations (e.g., those lacking visible phenotypic effects) is an important topic for future research.
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Data from: Stronger convex (stabilizing) selection on homologous sexual display traits in females than in males: a multipopulation comparison in Drosophila serrata
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Rundle, Howard D.; Chenoweth, Stephen F. — 2011-02-18 Mutual mate choice for homologous sexual display traits has been demonstrated in Mutual mate choice for homologous sexual display traits has been demonstrated in several recent studies yet little attention has been given to quantitative comparison of the strength and form of mate preferences between the sexes. Such comparisons may provide important insight into the evolution of mate choice for honest signals. In particular, because females generally provide the majority of resources for initial offspring development, female displays may trade-off with fecundity, causing preference evolution to differ between the sexes. Recent theory suggests that adaptive male preferences for honest displays in females are possible under certain conditions and may result in preferences that are convex (i.e. stabilizing) in form. We compared sexual selection on a suite of contact pheromones arising from mutual mate choice using nine separate geographic populations of Drosophila serrata. We show that the convex selection is stronger on females than on males overall in these populations, and that convex selection is the predominate form of nonlinear selection on females but not males.
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Data from: Territory defense as a condition-dependent component of male reproductive success in Drosophila serrata
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White, Alison J.; Rundle, Howard D. — 2014-12-03 Sexual selection arises from both intrasexual competition and mate choice. With respect to the evolution of male traits, there is a vast literature documenting the existence of female choice and male-male competition, and both have been shown to co-occur in many species. Despite numerous studies of these two components of male reproductive success in isolation, few have investigated whether and how they interact to determine total sexual selection. To address this, we investigate male territoriality in Drosophila serrata, a species in which female preference for male sexual pheromones (cuticular hydrocarbons or CHCs) have been extensively studied. We demonstrate that territoriality occurs, that it involves direct male-male aggressive interactions, and that it contributes to variation in male mating success. Results from a phenotypic manipulation also indicate that territorial success is condition-dependent, although a genetic manipulation of condition, involving three generations of full-sib inbreeding, failed to find a significant effect. Finally, selection assays also suggest that territorial success depends on male body size but not on CHCs, whereas the opposite is true for mating success.
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Data from: The physical environment mediates male harm and its effect on selection in females
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Yun, Li; Chen, Patrick J.; Singh, Amardeep; Agrawal, Aneil F.; Rundle, Howard D. — 2017-06-01 Recent experiments indicate that male preferential harassment of high-quality females reduces the variance in female fitness, thereby weakening natural selection through females and hampering adaptation and purging. We propose that this phenomenon, which results from a combination of male choice and male-induced harm, should be mediated by the physical environment in which intersexual interactions occur. Using Drosophila melanogaster, we examined intersexual interactions in small and simple (standard fly vials) versus slightly more realistic (small cages with spatial structure) environments. We show that in these more realistic environments, sexual interactions are less frequent, are no longer biased towards high-quality females, and that overall male harm is reduced. Next, we examine the selective advantage of high- over low-quality females while manipulating the opportunity for male choice. Male choice weakens the viability advantage of high-quality females in the simple environment, consistent with previous work, but strengthens selection on females in the more realistic environment. Laboratory studies in simple environments have strongly shaped our understanding of sexual conflict but may provide biased insight. Our results suggest that the physical environment plays a key role in the evolutionary consequences of sexual interactions and ultimately the alignment of natural and sexual selection.
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Data from: The purging of deleterious mutations in simple and complex mating environments
Colpitts, Julie; Williscroft, Darla; Sekhon, Harmandeep; Rundle, Howard; Rundle, Howard D.; Sekhon, Harmandeep Singh — 2017-09-22 There is a general expectation that sexual selection should align with natural selection to aid the purging of deleterious mutations, yet experiments comparing purging under monogamy vs. polygamy have provided mixed results. Recent studies suggest that this may be because the simplified mating environments used in these studies reduces the benefit of sexual selection through males and hampers natural selection through females by increasing costs associated with sexual conflict. To test the effect of the physical mating environment on purging, we use experimental evolution in Drosophila melanogaster to track the frequency of four separate deleterious mutations in replicate populations that experience polygamy under either a simple or structurally complex mating arena while controlling for arena size. Consistent with past results suggesting a greater net benefit of polygamy in a complex environment, two of the mutations were purged significantly faster in this environment. The other two mutations showed no significant difference between environments.

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