Perceptive Costs of Reproduction Drive Aging and Physiology in Male Drosophila

Costs of reproduction are thought to result from natural selection optimizing organismal fitness within putative physiological constraints. Phenotypic and population genetic studies of reproductive costs are plentiful across taxa, but an understanding of their mechanistic basis would provide important insight into the diversity in life history traits, including reproductive effort and aging. Here we dissect the causes and consequences of specific costs of reproduction in male Drosophila melanogaster. We find that key survival and physiological costs of reproduction arise from perception of the opposite sex, and they are reversed by the act of mating. In the absence of pheromone perception, males are free from reproductive costs on longevity, stress resistance, and fat storage. Both the costs of perception and the benefits of mating are mediated by evolutionarily conserved neuropeptidergic signaling molecules, as well as the transcription factor dFoxo. These results provide a molecular framework in which certain costs of reproduction arise as a result of self-imposed ‘decisions’ in response to perceptive neural circuits, which then orchestrate the control of life-history traits independent of physical or energetic effects associated with mating itself.