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.

Coevolution between Male and Female Genitalia in the Drosophila melanogaster Species Subgroup

“…However, Drosophila copulation anatomy has recently been investigated in detail, and a general pattern seems to emerge, with male genitalia causing copulatory wounds to the female tract, mainly via phallic auxiliary organs known as posterior parameres or inner paraphyses [24], [25] or via phallic spikes [26]. Whether these wounds reduce survival of mated females is unknown, although they were shown to trigger a localized immune response [27]. In D. melanogaster , a few harmful seminal proteins such as the sex peptide are known to enter the female hemolymph through the intima of the anterior margin of the vagina [28], [29] where the mating wounds form [25].…”

Copulatory Wounding and Traumatic Insemination

“…In ground beetles (Sota and Kubota 1998) and Drosophila (Kamimura 2012), interspecific matings resulted in more severe CW than intraspecific mating crosses, but in both cases, asymmetrically in only one direction. Remarkably, the risk of foreign, bacteria-sized particles to invade the copulatory wound was increased in both interspecific pairings (Kamimura 2012). This points toward the possibility that infection, in addition to CW itself, may generate a hybridization barrier.…”

“…Correspondingly, interspecific matings between the sister species Drosophila santomea and Drosophila yakuba resulted in more damaging CW than in intraspecific matings (Kamimura 2012).…”

“…Costs of this anchorage to females are unknown, but may arise from infection (Kamimura 2012). For instance, the female immune system in D. melanogaster responds to seminal fluids (Peng et al 2005;Domanitskaya et al 2007), but not to bacteria (Gendrin et al 2009) introduced to the reproductive tract (Kamimura 2012).…”

“…After CW, external male or female surfacedwelling or sexually transmitted microbes may enter the wound (Eke 2002;Mehta et al 2009Mehta et al , 2010Mehta et al , 2012Otti et al 2009Otti et al , 2013Kamimura 2012;and references therein). This elicits a series of responses.…”