The rapid dissolution of dioecy by experimental evolution

Evolutionary transitions from hermaphroditism to dioecy have been common in flowering plants,^1,2 but recent analysis also points to frequent reversions from dioecy to hermaphroditism.^2-4 Here, we use experimental evolution to expose a mechanism for such reversions, validating an explanation for the scattered phylogenetic distribution of dioecy. We removed males from dioecious populations of the wind-pollinated plant Mercurialis annua and allowed natural selection to act on the remaining females that occasionally produced male flowers; such "leaky" sex expression is common in both males and females of dioecious plants.⁵ Over the course of four generations, females evolved a 23-fold increase in average male flower production. This phenotypic masculinization of females coincided with the evolution of partial self-fertilization, high average seed set in the continued absence of males, and a capacity to sire progeny when males were re-introduced into their populations. Our study thus validates a mechanism for the rapid dissolution of dioecy and the evolution of functional hermaphroditism under conditions that may frequently occur during periods of low population density, repeated colonization, or range expansion.^6,7 Our results illustrate the power of natural selection, acting in replicated experimental populations, to bring about transitions in the mating behavior of plants.