Female penis, male vagina, and their correlated evolution in a cave insect

Abstract

Sex-specific elaborations are common in animals and have attracted the attention of many biologists, including Darwin [ 1 ]. It is accepted that sexual selection promotes the evolution of sex-specific elaborations. Due to the faster replenishment rate of gametes, males generally have higher potential reproductive and optimal mating rates than females. Therefore, sexual selection acts strongly on males [ 2 ], leading to the rapid evolution and diversification of male genitalia [ 3 ]. Male genitalia are sometimes used as devices for coercive holding of females as a result of sexual conflict over mating [ 4, 5 ]. In contrast, female genitalia are usually simple. Here we report the reversal of intromittent organs in the insect genus Neotrogla (Psocodea: Prionoglarididae) from Brazilian caves. Females have a highly elaborate, penis-like structure, the gynosome, while males lack an intromittent organ. The gynosome has species-specific elaborations, such as numerous spines that fit species-specific pouches in the simple male genital chamber. During prolonged copulation (∼40–70 hr), a large and potentially nutritious ejaculate is transferred from the male via the gynosome. The correlated genital evolution in Neotrogla is probably driven by reversed sexual selection with females competing for seminal gifts. Nothing similar is known among sex-role reversed animals.