Traumatic insemination and female counter-adaptation in Strepsiptera (Insecta)

In a few insect groups, males pierce the female’s integument with their penis during copulation to transfer sperm. This so-called traumatic insemination was previously confirmed for Strepsiptera but only in species with free-living females. The more derived endoparasitic groups (Stylopidia) were suggested to exhibit brood canal mating. Further, it was assumed that females mate once and that pheromone production ceases immediately thereafter. Here we examined Stylops ovinae to provide details of the mating behaviour within Stylopidia. By using μCT imaging of Stylops in copula, we observed traumatic insemination and not, as previously suggested, brood canal mating. The penis is inserted in an invagination of the female cephalothorax and perforates its cuticle. Further we show that female Stylops are polyandrous and that males detect the mating status of the females. Compared to other strepsipterans the copulation is distinctly prolonged. This may reduce the competition between sperm of the first mating male with sperm from others. We describe a novel paragenital organ of Stylops females, the cephalothoracic invagination, which we suggest to reduce the cost of injuries. In contrast to previous interpretations we postulate that the original mode of traumatic insemination was maintained after the transition from free-living to endoparasitic strepsipteran females.