Significance of precise genital coupling for female Drosophila fruit flies: why do females appear to cooperate with males by accepting harmful traumatic matings? (#247)
Male and female genitalia often exhibit corresponding morphologies indicating coevolutionary processes, but the driving mechanisms of such coevolution are still debated. In Drosophila melanogaster and its allied congeners, male genitalia often bear multiple ornaments (spines etc.) that inflict wounds on female genitalia during mating. Except for the D. bipectinata species complex, in which males are known to inject ejaculates into the female vagina through wounds, wounds may have unknown functions or may represent a byproduct of secure mate-holding. Female genitalia usually bear membranous pouches (‘pockets’) or hardened plates at the location where males inflict wounds. Because the soft pockets do not prevent male organs from inflicting wounds, some authors suggest that females ‘cooperate’ with males by preparing ‘niches’ for the wound-making organs, instead of developing counteradaptations to harmful male behaviors. Here I review studies on Drosophila spp., including unpublished ones, to explore whether precisely matched genital couplings reduce mating costs for females. Studies using interspecific crosses or crosses between genetic introgression lines provide evidence that micron-scale differences in male and female genital morphology and resultant mismatches during mating result in an elevated risk of wounding and infection for females. Furthermore, genital mismatches between female D. santomea and male D. yakuba frequently result in failed insertion of the male sperm-transferring organ, leading to leakage of the ejaculate and a prolonged struggle to separate pairs glued together by the ejaculate. Manipulative studies suggest that even small changes in male or female genital morphology (ablation of sensilla or ovipositor tips) strongly affect the latency to mating and insemination success. The dual functions of insect female genitalia, acquisition of sufficient sperm from males (at least one) and oviposition, likely constrain morphological evolution.