Dermaptera (earwigs) shows much diversity in the genital structures, the presence of either one or two male intromittent organs (penes) being one striking aspect. The members of several groups (Karschiellidae, Eudermaptera, Arixeniina, and Hemimerina) possess a single functional penis, while others have a pair of penes. The latter condition is considered to be plesiomorphic in Dermaptera. Despite its importance for inferring the phylogeny of Dermaptera, it is presently unclear how the ancestor of earwigs acquired paired penes. To estimate the mode of mating and sperm transfer in the common ancestor of extant earwigs, this study examines the mating behavior and genital coupling of the primitive earwig species Echinosoma denticulatum Hincks, 1959 as a representative of Pygidicranidae, one of the basal-most assemblages of earwigs. Staged mating experiments, including surgical manipulation of male penes revealed the following characteristics for this species: (1) males use only one of the paired penes for a single genital coupling; (2) both penes are likely functional; (3) there are no consistent biases in usage of the penes; (4) laterality of the penis-use pattern is not related to the direction of rotation of the male abdomen to establish genital coupling; (5) sperm are transferred directly into the spermatheca, a female sperm storage organ; (6) the spined area of the penis inflicts wounds on the vagina around the spermathecal opening, which bears many setae, during copulation. Characteristics (1)–(4) are considered to be plesiomorphic and may represent the condition of the common ancestor. Traumatic penetration during copulation is reported for earwigs for the first time. Together with intermittent acceptance of courting males by females only after a certain interval, these results suggest sexual conflict over mating in this species.

Evolution of laterally paired structures, dermapteran phylogeny, Pygidicranidae, genital evolution, mating behavior, insemination process, traumatic mating