Correlated evolutionary changes in Drosophila female genitalia reduce the possible infection risk caused by male copulatory wounding

Abstract

Male and female genitalia often show corresponding morphologies indicating coevolutionary processes, but ongoing debate exists as to the driving mechanisms of such coevolution between the sexes. Using interspecific matings between Drosophila santomea and Drosophila yakuba, this study provides evidence that micron-scale differences in male and female genital morphology and resultant mismatches between them during copulation cause wounding and infection risk to females. Male D. yakuba possesses a pair of sclerotized spikes (ventral branches of the basal processes) on the aedeagus, while these projections are much more rounded in D. santomea. D. yakuba females possess a pair of cavities with sclerotized platelets that receive the male genital spikes during copulation, whereas D. santomea females lack these cavities. The pointed genital spikes cause wounding in almost all females of D. santomea mating with male D. yakuba. Furthermore, when fluorescent-labeled microbeads were applied to male genitalia, they invaded the female hemocoel through the copulatory wounds significantly more frequently in heterospecific matings. Although the sclerotized platelets in the genital cavities prevented precise quantification of the extent of wounding in D. yakuba females, a similarly enhanced risk of microbial invasion was detected for the reciprocal heterospecific cross. All beads detected in the female hemocoel were immobilized by hemolymph clotting, indicating an effective immune response. The observed enhanced mating costs due to genital mismatch support the view that corresponding morphologies in female genitalia represent counteradaptations to harmful male behaviors, instead of being evolutionary adaptations to discriminate the species or genetic quality of male mates.