Frequent origins of traumatic insemination involve convergent shifts in sperm and genital morphology

Abstract

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 malefemale 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.

Evolution and co-evolution of the suck behaviour, a postcopulatory female resistance trait that manipulates received ejaculate

“…Moreover, this interpretation is also supported by the finding that there are multiple origins of hypodermic insemination in the genus Macrostomum (Brand et al, 2022b;Singh & Schärer, 2021). There are at least nine independent shifts from reciprocal mating to hypodermic insemination in Macrostomum, while no transition is observed in the converse direction (Brand et al, 2022b).…”

“…We found a significant evolutionary correlation between the presence of reciprocal mating and the suck behaviour (Figure 5a). In reciprocally-mating species, ejaculate is deposited in the female antrum allowing its removal during the suck behaviour, while in hypodermically-inseminating species, sperm is injected potentially anywhere in the body (Schärer et al ., 2011; Brand et al ., 2022b). Given that the function of the suck behaviour indeed appears to be the removal of ejaculate, we do not expect to see the suck behaviour in hypodermically-inseminating species.…”

“…if it takes longer to insert and remove more complex male genitalia, and to suck out ejaculate from more complex female antra. Interestingly in Macrostomum , male and female genital complexity are indeed correlated (Brand et al ., 2022b). Moreover, a positive correlation between reciprocal mating and suck could also appear, if some species do not do well under our laboratory conditions, leading to an overall low behaviour frequency.…”

“…Following Brand et al (2022b), 38 of a total of 64 species Macrostomum included in the current study were classified as exhibiting the reciprocal inferred mating syndrome, because they had a blunt tip of the stylet (the male intromittent organ), and of these all but one had received sperm in the antrum. A further 6 species with a sharp stylet were also classified as exhibiting the reciprocal inferred mating syndrome because they had complex sperm with lateral bristles and we observed sperm in the antrum (Figure 2).…”

Refutation of traumatic insemination in the Drosophila bipectinata species complex

“…This extraordinary behaviour is distinguished from other forms of 'traumatic mating', where only non-sperm components of the ejaculate, or no ejaculate at all, transfer to the female through the male-inflicted wounds [1][2][3][4]. Though rare, TI has arisen independently in a number of animal groups [3,5], and the evolutionary drivers of this unusual form of insemination are the focus of ongoing debate [1,[5][6][7][8][9].…”