Reduction of female copulatory damage by resilin represents evidence for tolerance in sexual conflict

Abstract

Intergenomic evolutionary conflicts increase biological diversity. In sexual conflict, female defence against males is generally assumed to be resistance, which, however, often leads to trait exaggeration but not diversification. Here, we address whether tolerance, a female defence mechanism known from interspecific conflicts, exists in sexual conflict. We examined the traumatic insemination of female bed bugs via cuticle penetration by males, a textbook example of sexual conflict. Confocal laser scanning microscopy revealed large proportions of the soft and elastic protein resilin in the cuticle of the spermalege, the female defence organ. Reduced tissue damage and haemolymph loss were identified as adaptive female benefits from resilin. These did not arise from resistance because microindentation showed that the penetration force necessary to breach the cuticle was significantly lower at the resilin-rich spermalege than at other cuticle sites. Furthermore, a male survival analysis indicated that the spermalege did not impose antagonistic selection on males. Our findings suggest that the specific spermalege material composition evolved to tolerate the traumatic cuticle penetration. They demonstrate the importance of tolerance in sexual conflict and genitalia evolution, extend fundamental coevolution and speciation models and contribute to explaining the evolution of complexity. We propose that tolerance can drive trait diversity.