In Drosophila, where females mate multiply, sperm competition contributes strongly to fitness variability among males. Males transfer “Acp” seminal proteins to females during mating, and these proteins influence the outcome of sperm competition. Because Acps function within the female, male proteins can directly interact with female molecules in a manner that affects reproductive fitness. Here we begin to dissect the genetic architecture of male × female interactions underlying reproductive phenotypes important to sperm competition. By utilizing chromosome extraction lines, we demonstrate that the third and X chromosomes each have large effects on fertility phenotypes, female remating rate, and the sperm competition parameter, P1. Strikingly, the third and X chromosomes harbor genetic variation that gives rise to strong male × female interactions that modulate female remating rate and P1. Encoded on these chromosomes are, respectively, sex peptide (SP) and sex peptide receptor (SPR), the only pair of physically interacting male Acp and female receptor known. We identified several intriguing allelic interactions between SP and SPR. The results of this study begin to elucidate the complex genetic architecture of reproductive and sperm competition phenotypes and have significant implications for the evolution of male and female characters.
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