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Traumatic insemination is a mating behavior during which the (sperm) donor uses a traumatic intromittent organ to inject an ejaculate through the epidermis of the (sperm) recipient, thereby frequently circumventing the female genitalia. Traumatic insemination occurs widely across animals, but the frequency of its evolution, the intermediate stages via which it originates, and the morphological changes that such shifts involve remain poorly understood. Based on observations in 145 species of the free‐living flatworm genus Macrostomum, we identify at least nine independent evolutionary origins of traumatic insemination from reciprocal copulation, but no clear indication of reversals. These origins involve convergent shifts in multivariate morphospace of male and female reproductive traits, suggesting that traumatic insemination has a canalizing effect on morphology. We also observed sperm in both the sperm receiving organ and within the body tissue of two species. These species had intermediate trait values indicating that traumatic insemination evolves through initial internal wounding during copulation. Finally, signatures of male‐female coevolution of genitalia across the genus indicate that sexual selection and sexual conflict drive the evolution of traumatic insemination, because it allows donors to bypass postcopulatory control mechanisms of recipients. [ABSTRACT FROM AUTHOR]

In species with multiple mating, intense sexual selection may occur both before and after copulation. However, comparing the strength of pre- and postcopulatory selection is challenging, because (i) postcopulatory processes are generally difficult to observe and (ii) the often-used opportunity for selection ( I ) metric contains both deterministic and stochastic components. Here, we quantified pre- and postcopulatory male fitness components of the simultaneously hermaphroditic flatworm, Macrostomum lignano . We did this by tracking fluorescent sperm-using transgenics-through the transparent body of sperm recipients, enabling to observe postcopulatory processes in vivo . Moreover, we sequentially exposed focal worms to three independent mating groups, and in each assessed their mating success, sperm-transfer efficiency, sperm fertilizing efficiency, and partner fecundity. Based on these multiple measures, we could, for each fitness component, combine the variance ( I ) with the repeatability ( R ) in individual success to assess the amount of repeatable variance in individual success-a measure we call the repeatable opportunity for selection ( I R ). We found higher repeatable opportunity for selection in sperm-transfer efficiency and sperm fertilizing efficiency compared to mating success, which clearly suggests that postcopulatory selection is stronger than precopulatory selection. Our study demonstrates that the opportunity for selection contains a repeatable deterministic component, which can be assessed and disentangled from the often large stochastic component, to provide a better estimate of the strength of selection., Competing Interests: The authors declare no conflict of interest., (© 2020 The Authors. Evolution Letters published by Wiley Periodicals, LLC on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB).)