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 events and the establishment of new populations through colonisation. Natural selection is therefore expected to favour traits that enhance dispersal and enable uniparental reproduction when mates are scarce. There is substantial evidence that range-edge populations evolve both increased dispersal ability and, in hermaphroditic species, an enhanced capacity for self-fertilisation. By contrast, the evolution of a greater capacity for uniparental production has not yet been demonstrated for dioecious plants. Here, we report results from a large common-garden experiment to assess the life history and sex expression of males and females of the dioecious annual herb Mercurialis annua sampled from across its European range. We found that plants from range-edge populations in central and western Europe not only tend to have smaller seeds and greater reproductive effort (RE) than populations from the eastern Mediterranean Basin, from where the species expanded its range, but also that males and females have an increased incidence of leaky sex expression (the production of flowers of the opposite sex). Small seeds and high RE are associated with dispersal, and the colonisation of new populations, and leaky sex expression allows otherwise unisexual individuals to produce progeny by self-fertilisation. Our results suggest that leaky sex expression in this species has been enhanced by selection for reproductive assurance, rather than representing a by-product of developmental instability during floral development or a relic of an incomplete transition to dioecy, as has been proposed for other dioecious species exhibiting leaky sex expression.