Multiple sexual selection pressures drive the rapid evolution of complex morphology in a male secondary genital structure

The genitalia of internally fertilizing taxa represent a striking example of rapid morphological evolution. Although sexual selection can shape variation in genital morphology, it has been difficult to test whether multiple sexual selection pressures combine to drive the rapid evolution of individual genital structures. Here, we test the hypothesis that both pre- and postcopulatory sexual selection can act in concert to shape complex structural variation in secondary genital morphology. We genetically modified the size and shape of the posterior lobes of Drosophila melanogaster males and tested the consequences of morphological variation on several reproductive measures. We found that the posterior lobes are necessary for genital coupling and that they are also the targets of multiple postcopulatory processes that shape quantitative variation in morphology, even though these structures make no direct contact with the external female genitalia or internal reproductive organs during mating. We also found that males with smaller and less structurally complex posterior lobes suffer substantial fitness costs in competitive fertilization experiments. Our results show that sexual selection mechanisms can combine to shape the morphology of a single genital structure and that the posterior lobes of D. melanogaster are the targets of multiple postcopulatory selection pressures.