‘Stab, chase me, mate with me, seduce me’: how widespread is traumatic insemination in Strepsiptera?

Abstract

Abstract Traumatic insemination refers to mating in which males pierce the female’s integument with his penis for insemination. Strepsiptera are often listed as an example for this mode of copulation. However, while traumatic insemination in Mengenillidae with free-living females is undisputed, its occurrence in Stylopidia with permanent endoparasitic females – 97% of the known species of Strepsiptera – has remained unclear. Rather, observations from a single study on Xenos vesparum (Xenidae) that questioned traumatic insemination in this species became generalized for Stylopidia. Here we show that integration of data from various imaging methods provides convincing evidence for traumatic insemination being phylogenetically widespread in Strepsiptera. Specifically, we provide the first evidence of injury wounds from traumatic insemination in species of Mengenillidae, Corioxenidae, Elenchidae, Halictophagidae and Xenidae. Using three-dimensional models of copulating pairs of Stylops ovinae (Stylopidae) and X. vesparum, we visualize the physical piercing of the female’s integument by the male’s penis. Finally, we show in species of Mengenillidae, Xenidae and Stylopidae that traumatic mating is associated with the injection of sperm in the female’s haemocoel. Our results significantly alter the understanding of the reproductive biology of Strepsiptera and imply that traumatic insemination has been the ancestral mode of copulation and retained in most, if not all, extant families.