Right‐handed penises of the earwig Labidura riparia (Insecta, Dermaptera, Labiduridae): Evolutionary relationships between structural and behavioral asymmetries

Abstract

The number of penises vary in the insect suborder Forficulina (order Dermaptera; earwigs). Males of the families Diplatyidae, Pigidicranidae, Anisolabididae, Apachyidae, and Labiduridae have two penises (right and left), while those of the Spongipohridae, Chelisochidae, and Forficulidae have a single penis. The proposed phylogenetic relationships among these families suggest that the single-penis families evolved from an ancestor possessing two penises. To date, examinations of double-penis earwig species have found that only a single penis is used per single copulation. These diversities in structural and behavioral aspects of genitalia raises the following intriguing questions: How are the two penises used? Why did a penis degenerate in several earwig families, and which one was lost? To address these questions, structural and behavioral asymmetries were examined in detail for a representative species Labidura riparia (Labiduridae). Although there was no detectable morphological differentiation between the right and left penises, male L. riparia predominantly used the right one for insemination. This significant "right-handedness" developed without any experience of mating and was also manifested in the resting postures of the two penises when not engaged in copulation. However, surgical ablation of the right penis did not influence the insemination capacity of males. In wild-caught males, only about 10% were left-handed; within this group, abnormalities were frequently observed in the right penis. These lines of evidence indicate that the left penis is merely a spare intromittent organ, which most L. riparia males are likely never to use. Additional observations of five species of single-penis families revealed that the left penis degenerated in the common ancestor of this group. Considering the proposed sister relationship between the Labiduridae and the single-penis families, it is possible that such behavioral asymmetries in penis' use, as observed in L. riparia, are parental to the evolutionary degeneration of the infrequently used left penis.