Misalignment of natural and sexual selection among divergently adapted Drosophila melanogaster populations

The effect of sexual selection on nonsexual fitness is a major unanswered question in evolutionary biology that may have important implications for adaptation, diversification and the evolution of mate preferences. If reproductive success is condition dependent, the resulting sexual selection will tend to align with natural selection, promoting adaptation. One prediction under such a scenario is that adaptation to a novel environment should increase male mating success and hence sexual fitness. Environmentally induced plasticity in mate preferences could also contribute to an alignment of natural and sexual selection if the changes cause females to prefer locally adapted males as mates. We tested for both forms of alignment using a set of 10 independent populations of Drosophila melanogaster that were adapted to one of two environments. Competitive mating trials were performed between pairs of populations adapted to these two environments, with the trials designed to separate the effects of local adaptation on male mating success from plasticity of female mate preferences in response to these environments. Contrary to expectations under an alignment of natural and sexual selection, males did not have higher mating success when competing in the environment to which they were adapted. Furthermore, there was no evidence that females altered their mate choice based on their rearing environment, indicating the absence of any adaptive plasticity in mate preferences. Overall, despite previous evidence of reciprocal adaptation to these different environments, increased nonsexual fitness did not translate into higher mating success, indicating a lack of any alignment with natural selection of this component of male sexual fitness.