Rapid evolution of pollen and pistil traits as a response to sexual selection in the post-pollination phase of mating

Abstract

Sexual selection is the basis of some of the most striking phenotypic variation in nature.1,2 In animals, sexual selection in males can act on traits that improve access to mates prior to copulation,3-8 but also on sperm traits filtered by sperm competition,9-14 or female choice expressed simply by the morphology and physiology of genital tracts.14-16 Although long overlooked as a mode of selection on plant traits, sexual selection should act on land plants too because they are anisogamous: males produce more, and smaller, gametes than females.17-19 Numerical asymmetry in gamete production is thought to play a central role in selection on traits that affect pollen transfer to mates,20,21 but very little is known about how pollen competition or cryptic female choice might affect the evolution of traits expressed after pollination.22,23 Here, we report the divergence of pollen and pistil traits of the dioecious wind-pollinated annual herb Mercurialis annua during evolution over three generations between populations at low versus high plant density, corresponding to low versus higher levels of polyandry;24 we expected selection under higher polyandry to strengthen competition among pollen donors for fertilizing ovules. We found that populations at high density evolved faster-growing pollen tubes (an equivalent of greater sperm velocity), greater expression of pollen proteins involved in pollen growth, and larger stigmas (a trait likely enhancing the number of pollen donors and thus competition for ovules). Our results identify the post-pollination phase of plant mating as an important arena for the action of sexual selection.