The rapid dissolution of dioecy by experimental evolution

• DOI: 10.1016/j.cub.2020.12.028
• Publication Date: 2021-01-19T15:35:29Z
• Authors: Guillaume G. Cossard; Jörn F. Gerchen; Xinji Li; Yves Cuenot; John R. Pannell
• Keywords: 0106 biological sciences; Magnoliopsida; Solubility; Reproduction; Hermaphroditic Organisms; Biological Evolution; 01 natural sciences; Phylogeny

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.