Females are frequently harassed and harmed by males attempting to obtain matings. When these males are also “choosy” with their courtship, there may be negative consequences to the species' ability to adaptively evolve.

Whether the changes brought about by sexual selection are, on the whole, congruent or incongruent with the changes favored by natural selection is a fundamentally important question in evolutionary biology. Although a number of theoretical models have assumed that sexual selection reinforces natural selection [1, 2], others assume these forces are in opposition [3-5]. Empirical results have been mixed (see reviews in [1, 6-8]) and the reasons for the differences among studies are unclear. Variable outcomes are expected if populations differ in their evolutionary histories and therefore harbor different amounts and types of segregating genetic variation. Here, we constructed populations of Drosophila melanogaster that differed in this regard to directly test this hypothesis. In well-adapted populations, sexually successful males sired unfit daughters, indicating sexual and natural selection are in conflict. However, in populations containing an influx of maladaptive alleles, attractive males sired offspring of high fitness, suggesting that sexual selection reinforces natural selection. Taken together, these results emphasize the importance of evolutionary history on the outcome of sexual selection. Consequently, studies based on laboratory populations, cultured for prolonged periods under homogeneous conditions, may provide a skewed perspective on the relationship between sexual and natural selection.

The strongest form of intralocus sexual conflict occurs when two conditions are met: (i) there is a positive intersexual genetic correlation for a trait and (ii) the selection gradients on the trait in the two sexes are in opposite directions. Intralocus sexual conflict can constrain the adaptive evolution of both sexes and thereby contribute to a species' 'gender load'. Previous studies of adult lifetime fitness of the same sets of genes expressed in both males and females have established that there is substantial intralocus conflict in the LH M laboratory-adapted population of Drosophila melanogaster. Here, we investigated whether a highly dimorphic trait-adult locomotory activity-contributed substantially to the established intralocus sexual conflict. To measure the selection gradient on activity level, both this trait and adult lifetime fitness were measured under the same environmental conditions to which the flies were adapted. We found significant phenotypic variation in both sexes for adult locomotory activity, and that the selection gradients on this variation were large and in opposite directions in the two sexes. Using hemiclonal analysis to screen 99% of the entire genome, we found abundant genetic variation for adult locomotory activity and showed that this variation occurs on both the X and autosomes. We also established that there is a strong positive intersexual genetic correlation for locomotory activity. These assays revealed that, despite the strong, extant sexual dimorphism for the trait, locomotory activity continues to contribute strongly to intralocus sexual conflict in this population.

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