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.

The pdm3 Locus Is a Hotspot for Recurrent Evolution of Female-Limited Color Dimorphism in Drosophila.

Sex-limited polymorphisms are an intriguing form of sexual dimorphism that offer unique opportunities to reconstruct the evolutionary changes that decouple male and female traits encoded by a shared genome. We investigated the genetic basis of a Mendelian female-limited color dimorphism (FLCD) that segregates in natural populations of more than 20 species of the Drosophila montium subgroup. In these species, females have alternative abdominal color morphs, light and dark, whereas males have only one color morph in each species. A comprehensive molecular phylogeny of the montium subgroup supports multiple origins of FLCD. Despite this, we mapped FLCD to the same locus in four distantly related species-the transcription factor POU domain motif 3 (pdm3), which acts as a repressor of abdominal pigmentation in D. melanogaster. In D. serrata, FLCD maps to a structural variant in the first intron of pdm3; however, this variant is not found in the three other species-D. kikkawai, D. leontia, and D. burlai-and sequence analysis strongly suggests the pdm3 alleles responsible for FLCD originated independently at least three times. We propose that cis-regulatory changes in pdm3 form sexually dimorphic and monomorphic alleles that segregate within species and are preserved, at least in one species, by structural variation. Surprisingly, pdm3 has not been implicated in the evolution of sex-specific pigmentation outside the montium subgroup, suggesting that the genetic paths to sexual dimorphism may be constrained within a clade but variable across clades.

Genomic Evidence that Sexual Selection Impedes Adaptation to a Novel Environment.

Sexual selection is widely appreciated for generating remarkable phenotypic diversity, but its contribution to adaptation and the purging of deleterious mutations is unresolved. To provide insight into the impact of sexual selection on naturally segregating polymorphisms across the genome, we previously evolved 12 populations of Drosophila serrata in a novel environment employing a factorial manipulation of the opportunities for natural and sexual selection. Here, we genotype more than 1,400 SNPs in the evolved populations and reveal that sexual selection affected many of the same genomic regions as natural selection, aligning with it as often as opposing it. Intriguingly, more than half of the 80 SNPs showing treatment effects revealed an interaction between natural and sexual selection. For these SNPs, while sexual selection alone often caused a change in allele frequency in the same direction as natural selection alone, when natural and sexual selection occurred together, changes in allele frequency were greatly reduced or even reversed. This suggests an antagonism between natural and sexual selection arising from male-induced harm to females. Behavioral experiments showed that males preferentially courted and mated with high-fitness females, and that the harm associated with this increased male attention eliminated the female fitness advantage. During our experiment, females carrying otherwise adaptive alleles may therefore have disproportionally suffered male-induced harm due to their increased sexual attractiveness. These results suggest that a class of otherwise adaptive mutations may not contribute to adaptation when mating systems involve sexual conflict and male mate preferences.