Geographical gradients in leaky sex expression and reproductive effort in a dioecious plant are consistent with selection during range expansion

Range expansion involves repeated dispersal and the establishment of new populations through colonization. Natural selection is therefore expected to favour traits that enhance dispersal and enable uniparental reproduction when mates are scarce. It is known that range-edge populations may evolve increased dispersal and, in hermaphroditic species, an enhanced capacity for self-fertilization. Here, we report results from a large common-garden experiment showing that males and females of the dioecious annual herb Mercurialis annua are more likely to show 'leaky' or inconstant sex expression towards the recently colonized edge of its geographical distribution in Europe than those from the eastern Mediterranean Basin, from where the species expanded its range. Range-edge populations also had greater reproductive effort (RE). Leaky sex expression allows otherwise unisexual individuals of M. annua to produce progeny by self-fertilization, a trait that may have been selected to increase reproductive assurance during the range expansion. High RE likely facilitated both colonization and subsequent population establishment. Our results show that selection during range expansions may modify reproductive traits towards range margins, extending this notion to the phenomenon of leaky sex expression in dioecious species. Previous work has shown that leaky sex expression in M. annua is strongly heritable; our results now further suggest that has been enhanced by selection for reproductive assurance towards range margins and confirm, in a natural setting, that the trait is not just an expression of developmental instability during floral development or a relic of an incomplete transition to dioecy.