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Animal genitalia have changed substantially and rapidly during evolution, and functionally interacting anatomical structures complementarily match between the sexes. Several hypotheses have been proposed to explain how such structure-matching evolved. A test of these hypotheses would require a detailed analysis of male and female genitalia among closely related species and a comparison of the functional aspects of the interacting structures between the sexes. Therefore, here we document genital coupling and copulatory wounds in the four species of the Drosophila auraria complex. The position of the protrusion of the median gonocoxite of males relative to the female terminalia differed among the species, which may reflect differences in protrusion morphology. Species-specific female structures were discovered on the membrane between the genitalia and analia and on the vaginal wall. The former makes contact with the protrusion, and the latter makes contact with appendages of the aedeagus. Copulatory wounds, which are produced during copulation, were seen at three locations on females: depressions near the genital orifice, the membrane between the genitalia and analia, and the vaginal wall. Some of the copulatory wounds were located at sites that could potentially make contact with the species-specific structures that we identified. We speculate that the female structures that differ between species of the D. auraria complex evolved in concert with the genitalia of male conspecifics.

Animals can show bias in their use of laterally paired organs that do not have any conspicuous anatomical differentiation between the right and left organs. Like right handedness in humans, males of the giant earwig Labidura riparia (Labiduridae: Labidurinae) preferentially (~90%) use the right one of their laterally paired penises for copulation. To elucidate the evolutionary origin of this lateralization, patterns of penis use were examined for the related species of the genus Nala (Labiduridae: Nalinae). In multiple populations and broods of both Nala lividipes and Nala nepalensis, males that were ready to use the right or left penis were equally frequent, providing a striking contrast to Labidura. Surgical ablation of one of the two penises revealed that both penises are functionally competent in N. lividipes. Nevertheless, each male almost consistently used only one of the paired penises, either the right or the left one. Changes in penis use were estimated to occur only once per 64–143 days per male. The present study is the first report of individual-level lateralization for animal genitalia that do not show any conspicuous anatomical differentiation between the right and left organs. Possible advantages of lateralization are discussed in relationship to co-evolution of the genitalia between the sexes.

Ovoviviparity or viviparity has evolved independently in animals and involves adaptations in females to accommodate developing embryos for a prolonged duration in their bodies, a condition which has likely to have influenced the evolution of the male genitalia. We aimed to ascertain whether the elongated male genitalia of the ovoviviparous free-living earwig species Marava arachidis (Dermaptera: Spongiphoridae) delivers sperm directly to the female ovaries where fertilization occurs. Males mated coercively with females by grabbing the female antenna with their mouth parts. Although females resisted the mating attempts, pairs mated 3.3 times on average over 15 h. The elongated intromittent organ, known as a virga, was inserted into the long-tubed spermatheca during insemination. Surgical ectomy of the spermatheca confirmed that sperm migrated from here to the ovaries with a variable delay. A pair of sclerites in the male genitalia frequently inflicted wounds near the spermathecal opening, while the single, thin virga sometimes broke off during mating. However, unlike earwigs bearing a ‘spare’ virga, damage was restricted to the tip of the virga, without which the males could still inseminate the females. We discuss the evolution of the genitalia in this insect in the light of sexual selection and sexual conflict over mating and fertilization.

Male genitalia show several evolutionary characteristics, including rapid morphological divergence between closely related species and low within-species phenotypic variability. In addition, genital asymmetry is widespread despite the essentially bilaterally symmetric external morphology of insects. Several hypotheses, such as sexual selection and lock-and-key hypotheses, have been proposed to explain these characteristics of genital evolution. Although these hypotheses provide different predictions about the genetic basis of variation in genitalia, detailed quantitative genetic studies have been conducted in only three insect taxa: heteropterans, dung beetles (Scarabaeidae), and drosophilid flies. For an anisolabidid earwig, Euborellia plebeja, characterized by paired elongated intromittent organs, we estimated the heritabilities and genetic correlations of genital laterality, size of genitalia, and body size. No statistically significant additive genetic, dominance, maternal, or common environmental effects were detected for genital laterality (readiness to use either the left or the right intromittent organ). This result lends further support to the general rule that the direction of antisymmetric variations is randomly determined by non-genetic factors. Irrespective of the restricted phenotypic variation in genitalia compared with body size (allometric slope