Male Adaptive Plasticity Can Explain the Evolution of Sexual Perception Costs

Sensory perception of environmental cues has been shown to trigger plastic responses that can induce important fitness costs, including the dramatic modulation of aging across distant taxa. For example, male Drosophila melanogaster suffer a marked decrease in fitness, characterized by faster reproductive and actuarial aging, if they perceive female cues but fail to mate shortly after (aging via sexual perception). While this has been a breakthrough for our understanding of the mechanisms of aging, it raises the question of why such plastic responses evolved. Here, we used D. melanogaster to ask whether sexual perception costs may be a by-product of adaptive plastic responses to female cues. We found that (a) short-term perception (1 day) of female cues before mating opportunities increases male relative lifetime reproductive success in a competitive environment, (b) medium-term perception (3–7 days) is neutral, and (c) long-term perception (15 days) leads to reproductive costs. We then ran mathematical simulations under a wide range of sociosexual and demographic scenarios to show that such plastic male responses can be adaptive whenever mating rates fluctuate within the range experienced by D. melanogaster and other insects in the wild, suggesting that this may be a widespread strategy in nature. Finally, we show that, because the short-term benefits of plastic responses will be acquired mostly by high-quality males while long-term costs will be paid mostly by low-quality males, sexual perception can significantly magnify sexual selection (15%–27% average increase in the opportunity for selection).