A model for the gradual evolution of dioecy and heterogametic sex determination

Abstract

In plants with separate sexes, the development of an individual as male or female is controlled by a dominant allele at a sex-determining locus - the fundamental basis of XY and ZW systems. The many independent transitions from hermaphroditism to dioecy that have taken place in flowering plants must therefore often have entailed the emergence of such a locus. One proposition is that this evolution occurs in two steps, with the initial invasion of a male-sterility mutation at one locus followed by mutations causing female sterility at a second closely linked locus. Here, we show how dioecy with heterogametic sex determination can also emerge in a gradual adaptive process, involving the co-evolution of resource allocation to different sexual functions jointly with its genetic architecture. Our model reveals that whether an XY or a ZW system evolves depends on the mating system of the ancestral hermaphrodites as well as the trade-off they face between allocation to male and female functions. In particular, the evolution of dioecy in response to selection to avoid selfing and inbreeding depression favours the emergence of XY systems, which characterise the vast majority of dioecious flowering plants. Selection favouring female specialisation also favours XY over ZW sex determination. Taken together, our results throw new light on the possible origins of dioecy from hermaphroditism by revealing a hitherto unrecognised link between the ecology and economics of sex allocation and the genetic basis of sex determination.