Why sex has evolved and is maintained is an open question in evolutionary biology. The Red Queen hypothesis predicts that host lineages subjected to more intense parasite pressure should invest more in sexual reproduction to continuously create novel defences against their rapidly evolving natural enemies. In this comparative study across the angiosperms, we show that hermaphrodite plant species associated with higher species richness of insect herbivores evolved flowers with higher biomass allocation towards the male sex, an indication of their greater outcrossing effort. This pattern remained robust after controlling for key vegetative, reproductive and biogeographical traits, suggesting that long-term herbivory pressure is a key factor driving the selfing-outcrossing gradient of higher plants. Although flower evolution is frequently associated with mutualistic pollinators, our findings support the Red Queen hypothesis and suggest that insect herbivores drive the sexual strategies of flowering plants and their genetic diversity.
Keywords: Red Queen hypothesis; coevolution; flowering plant; functional trait; herbivory; male-male competition; outcrossing; pollinator; sex evolution; sexual selection.
© 2022 John Wiley & Sons Ltd.