The contribution of mutation and selection to multivariate quantitative genetic variance in an outbred population of Drosophila serrata.

Genetic variance is not equal for all multivariate combinations of traits. This inequality, in which some combinations of traits have abundant genetic variation while others have very little, biases the rate and direction of multivariate phenotypic evolution. However, we still understand little about what causes genetic variance to differ among trait combinations. Here, we investigate the relative roles of mutation and selection in determining the genetic variance of multivariate phenotypes. We accumulated mutations in an outbred population of Drosophila serrata and analyzed wing shape and size traits for over 35,000 flies to simultaneously estimate the additive genetic and additive mutational (co)variances. This experimental design allowed us to gain insight into the phenotypic effects of mutation as they arise and come under selection in naturally outbred populations. Multivariate phenotypes associated with more (less) genetic variance were also associated with more (less) mutational variance, suggesting that differences in mutational input contribute to differences in genetic variance. However, mutational correlations between traits were stronger than genetic correlations, and most mutational variance was associated with only one multivariate trait combination, while genetic variance was relatively more equal across multivariate traits. Therefore, selection is implicated in breaking down trait covariance and resulting in a different pattern of genetic variance among multivariate combinations of traits than that predicted by mutation and drift. Overall, while low mutational input might slow evolution of some multivariate phenotypes, stabilizing selection appears to reduce the strength of evolutionary bias introduced by pleiotropic mutation.

Using inbreeding to test the contribution of non-additive genetic effects to additive genetic variance: a case study in Drosophila serrata.

Additive genetic variance, VA, is the key parameter for predicting adaptive and neutral phenotypic evolution. Changes in demography (e.g. increased close-relative inbreeding) can alter VA, but how they do so depends on the (typically unknown) gene action and allele frequencies across many loci. For example, VA increases proportionally with the inbreeding coefficient when allelic effects are additive, but smaller (or larger) increases can occur when allele frequencies are unequal at causal loci with dominance effects. Here, we describe an experimental approach to assess the potential for dominance effects to deflate VA under inbreeding. Applying a powerful paired pedigree design in Drosophila serrata, we measured 11 wing traits on half-sibling families bred via either random or sibling mating, differing only in homozygosity (not allele frequency). Despite close inbreeding and substantial power to detect small VA, we detected no deviation from the expected additive effect of inbreeding on genetic (co)variances. Our results suggest the average dominance coefficient is very small relative to the additive effect, or that allele frequencies are relatively equal at loci affecting wing traits. We outline the further opportunities for this paired pedigree approach to reveal the characteristics of VA, providing insight into historical selection and future evolutionary potential.

Experimental evidence for accelerated adaptation to desiccation through sexual selection on males.

The impact of sexual selection on the adaptive process remains unclear. On the one hand, sexual selection might hinder adaptation by favouring costly traits and preferences that reduce nonsexual fitness. On the other hand, condition dependence of success in sexual selection may accelerate adaptation. Here, we used replicate populations of Drosophila melanogaster to artificially select on male desiccation resistance while manipulating the opportunity for precopulatory sexual selection in a factorial design. Following five generations of artificial selection, we measured the desiccation resistance of males and females to test whether the addition of sexual selection accelerated adaptation. We found a significant interaction between the effects of natural selection and sexual selection: desiccation resistance was highest in populations where sexual selection was allowed to operate. Despite only selecting on males, we also found a correlated response in females. These results provide empirical support for the idea that sexual selection can accelerate the rate of adaptation.

Evaluating the genetic architecture of quantitative traits via selection followed by inbreeding.

The deleterious mutation model proposes that quantitative trait variation should be dominated by rare, partially recessive, deleterious mutations. Following artificial selection on a focal trait, the ratio of the difference in inbreeding effects between control and selected populations (ΔB), to the difference in trait means caused by directional selection (ΔM), can inform the extent to which deleterious mutations cause quantitative trait variation. Here, we apply the ΔB/ΔM ratio test to two quantitative traits (male mating success and body size) in Drosophila melanogaster. For both traits, ΔB/ΔM ratios suggested that intermediate-frequency alleles, rather than rare, partially recessive alleles (i.e. deleterious mutations), caused quantitative trait variation. We discuss these results in relation to viability data, exploring how differences between regimens in segregating (measured through inbreeding) and fixed (measured through population crosses) mutational load could affect the ratio test. Finally, we present simulations that test the statistical power of the ratio test, providing guidelines for future research.

Environmental dependence of mutational (co)variances of adaptive traits.

Standing genetic variation, and capacity to adapt to environment change, will ultimately depend on the fitness effects of mutations across the range of environments experienced by contemporary, panmictic, populations. We investigated how mild perturbations in diet and temperature affect mutational (co)variances of traits that evolve under climatic adaptation, and contribute to individual fitness in Drosophila serrata. We assessed egg-to-adult viability, development time and wing size of 64 lines that had diverged from one another via spontaneous mutation over 30 generations of brother-sister mating. Our results suggested most mutations have directionally concordant (i.e., synergistic) effects in all environments and both sexes. However, elevated mutational variance under reduced macronutrient conditions suggested environment-dependent variation in mutational effect sizes for development time. We also observed evidence for antagonistic effects under standard versus reduced macronutrient conditions, where these effects were further contingent on temperature (for development time) or sex (for size). Diet also influenced the magnitude and sign of mutational correlations between traits, although this result was largely due to a single genotype (line), which may reflect a rare, large effect mutation. Overall, our results suggest environmental heterogeneity and environment-dependency of mutational effects could contribute to the maintenance of genetic variance.

Molecular evidence supports a genic capture resolution of the lek paradox.

The genic capture hypothesis, where sexually selected traits capture genetic variation in condition and the condition reflects genome-wide mutation load, stands to explain the presence of abundant genetic variation underlying sexually selected traits. Here we test this hypothesis by applying bidirectional selection to male mating success for 14 generations in replicate populations of Drosophila melanogaster. We then resequenced the genomes of flies from each population. Consistent with the central predictions of the genic capture hypothesis, we show that genetic variance decreased with success selection and increased with failure selection, providing evidence for purifying sexual selection. This pattern was distributed across the genome and no consistent molecular pathways were associated with divergence, consistent with condition being the target of selection. Together, our results provide molecular evidence suggesting that strong sexual selection erodes genetic variation, and that genome-wide mutation-selection balance contributes to its maintenance.

Evolutionary divergence in competitive mating success through female mating bias for good genes.

Despite heritable variation for univariate sexually selected traits, recent analyses exploring multivariate traits find evidence consistent with the lek paradox in showing no genetic variation available to choosy females, and therefore no genetic benefits of choice. We used the preferences of Drosophila melanogaster females to exert bidirectional selection on competitive male mating success to test for the presence and nature of genetic variation underlying this multivariate trait. Male mating success diverged between selection regimens, and flies from success-selected lines had a smaller burden of deleterious, recessive mutations that affect egg-to-adult viability, were better sperm competitors (sperm offence), and did not demonstrate reduced desiccation resistance or components of female fitness (traits thought to trade off with attractiveness) relative to flies from failure-selected populations. Mating success remained subject to inbreeding depression in success-selected lines, suggesting that variation in mating success remains, thanks to numerous genes of small effect. Together, our results provide unique evidence for the evolutionary divergence in male mating success, demonstrating that genetic variation is not exhausted along the axis of precopulatory sexual selection and that female mating biases align with the avoidance of bad genes.