Enhanced leaky sex expression is an adaptive plastic response to pollen limitation in the dioecious plant Mercurialis annua

Phenotypic plasticity is almost ubiquitous across the tree of life, but clear demonstrations that it is adaptive are rare. In dioecious plants, males and females frequently show ‘leaky’ sex expression, with individuals occasionally producing flowers of the opposite sex. Here, we demonstrate that leaky sex expression in the wind-pollinated dioecious herb Mercurialis annua is plastically responsive to its mating context. We compared experimental populations of females growing either with or without males. Females growing in the absence of males were leakier in their sex expression than controls with males, producing more than twice as many male flowers. Moreover, because greater leakiness was more highly represented in the population’s progeny, we conclude that enhanced leakiness in sex expression is adaptive in M. annua. We discuss differences in the degree of plasticity between ploidal races of Mercurialis annua in terms of likely differences in the reliability of the signal plants may perceive for the presence of males in their populations. Our results provide a striking instance of adaptive plasticity in the reproductive behavior of plants and draw attention to possible constraints on plasticity when the environmental signals that individuals receive are unreliable.