Harmful self-pollination drives gynodioecy in European chestnut, a self-incompatible tree

Gynodioecy is a rare sexual system in which two genders, cosexuals and females, coexist. It provides the opportunity to compare individuals having both sexual functions with individuals lacking the male function, an ideal situation to understand how sexes interact within individual plants. We report gynodioecy in the European chestnut, an outcrossing self-incompatible Fagaceae tree species. This finding was unexpected because gynodioecy is often interpreted as an outbreeding mechanism. To understand how female chestnuts compensate for their lack of siring capacity, we compared key female fitness components between genders and performed emasculation experiments. Genders have similar basal area and number of flowers but different fruit set. Following the removal of nectar-producing catkins on branches or entire trees, fruit set increased in cosexual trees but decreased in female trees. These results show that self-pollination impairs fruit set in cosexual trees, a likely effect of self-pollen interference caused by late-acting self-incompatibility and by early inbreeding depression. Female trees escape from self-pollen interference but continue to attract pollinators thanks to their sterile but rewarding male catkins, resulting in a much higher fruit set than cosexuals. This demonstrates that even entirely outcrossed plants can benefit from the cessation of self-pollination.