The Red Queen unveils the sexual and mating strategies of flowers

Abstract The Red Queen Hypothesis states that sex evolved as an adaptation of hosts against their parasites, allowing them to produce offspring protected by rare combinations of defence genes. It has been hypothesized that plant species under higher pressure by short‐lived natural enemies should invest more heavily in outcrossing. Here, we test the interspecific prediction that plant species associated with a higher species richness of insect herbivores—used as a proxy for a higher, more diverse and consistent herbivory pressure over geographic space and evolutionary time—should exhibit sexual and mating traits leading to outcrossing. We predict that plant species associated with a richer insect fauna will have a higher probability to be auto‐incompatible, dichogamous, heterostylous, dimorphic, dioecious and allogamous. Furthermore, they are predicted to exhibit a higher pollen–ovule ratio, to be more dependent on pollinators or wind for cross‐fertilization, and to rely mostly on sexually generated seeds for reproduction rather than on asexual reproduction. In order to perform such comparative tests, we assembled published insect–plant interaction records and information on key reproductive floral traits linked to the inbreeding–outcrossing gradient for 1884 native angiosperm species from Germany. The analyses were performed with generalized linear models and phylogenetic models using species richness of insect herbivores as the single explanatory variable, but also with plant geographic range size and plant height as covariates. We showed that plant species consumed by a higher species richness of insect herbivores have a higher probability to be auto‐incompatible, dichogamous, dimorphic, dioecious and allogamous. In addition, they had a higher pollen–ovule ratio, were more dependent on pollinators or wind for cross‐fertilization, and relied mostly on sexually generated seeds for reproduction rather than also use asexual reproduction. Model fitting improved considerably after taking into consideration the phylogenetic structure of the data and the results remained relatively consistent after controlling for geographic range size and plant height. Synthesis . Although the conventional wisdom is that floral traits of plants evolved in concert with their mutualistic pollinators, here we showed that several key sexual and mating traits of plants, which modulate their outcrossing strategy, evolved in response to the pressure exerted by their antagonistic insect herbivores. The Red Queen Hypothesis emerges as a unifying theory which helps to explain the sexual diversity of angiosperms, with consequences for genetic and phylogenetic diversity, animal–plant network structures, and plant‐based ecosystem services.