Dioecy in a wind-pollinated herb explained by disruptive selection on sex allocation via inbreeding avoidance

The evolution of dioecy from hermaphroditism is widely thought to be a response to disruptive selection favoring males and females, driven by advantages of inbreeding avoidance, sexual specialization, or both. It has hitherto been difficult to uncouple the importance of these two hypotheses. We use phenotypes produced by experimental evolution to test the inbreeding avoidance hypothesis in populations from which sexual specialization can be effectively ruled out. We estimate the selfing rate and the shape of fitness gain curves under scenarios with and without inbreeding depression in experimental populations of wind-pollinated Mercurialis annua with high variation in sex allocation. Our results confirm a phenotypic trade-off between male and female allocation in M. annua. Individual selfing rates increased with pollen production. This dependence led to strong disruptive selection on sex allocation due to its interaction with the mating system under the scenario of high inbreeding depression, especially for plants of medium and large sizes. Taken together, our results demonstrate that inbreeding avoidance on its own can lead to disruptive selection on sex allocation, favoring the selection and maintenance of dioecy under wind pollination without associated benefits of sexual specialization.