Traumatic insemination is a bizarre form of mating practiced by some invertebrates in which males use hypodermic genitalia to penetrate their partner's body wall during copulation, frequently bypassing the female genital tract and ejaculating into their blood system. The requirements for traumatic insemination to evolve are stringent, yet surprisingly it has arisen multiple times within invertebrates. In terrestrial arthropods traumatic insemination is most prevalent in the true bug infraorder Cimicomorpha, where it has evolved independently at least three times. Traumatic insemination is thought to occur in the Strepsiptera and has recently been recorded in fruit fly and spider lineages. We review the putative selective pressures that may have led to the evolution of traumatic insemination across these lineages, as well as the pressures that continue to drive divergence in male and female reproductive morphology and behavior. Traumatic insemination mechanisms and attributes are compared across independent lineages.

In traumatic insemination, males pierce females with hypodermic genitalia and ejaculate into the body cavity rather than into the genital tract. This has resulted in the evolution of female counter-adaptations in the form of paragenitalia to reduce the direct physical costs of mating. While rare in the animal kingdom, traumatic insemination is oddly prevalent in the true bug infraorder Cimicomorpha (Heteroptera), where it occurs in six families and is thought to have arisen twice. Here, we report the discovery of traumatic insemination and elaborate paragenital development in the plant bug genus Coridromius (Miridae), representing a third, independent emergence of traumatic insemination in this infraorder.

Sexual conflict has recently been proposed as a driving force behind the rapid diversification of genitalia among sexually reproducing organisms. In traumatically inseminating insects, males stab females in the side of the body with needle‐like genitalia, ejaculating into their body cavity. Such mating is costly to females and has led to the evolution of cost‐reducing ‘paragenitalia’ in some species. Whereas some consider this evidence of sexually antagonistic coevolution, others remain unconvinced. Variation in the reproductive morphology of both sexes – particularly males – is alleged to be negligible, contradicting the expectations of a coevolutionary arms race. Here, we use a phylogeny of the traumatically inseminating plant bug genus Coridromius to show that external female paragenitalia have evolved multiply across the genus and are correlated with changes in male genital shape. This pattern is characteristic of an evolutionary arms race driven by sexual conflict.