The joint evolution of separate sexes and sexual dimorphism

Abstract Dioecious plants are frequently sexually dimorphic. Such dimorphism, which reflects responses to selection acting in opposite directions for male and female components of fitness, is commonly thought to emerge after separate sexes evolved from hermaphroditism. But associations between allocation to male and female function and traits under sexual conflict could also begin to evolve in hermaphroditic ancestors, and fuel transitions to dioecy. Here, we show that variation in sex allocation and a trait under sexual conflict inevitably generates an advantage to sexual specialisation. In the absence of constraints, this leads to the joint evolution of separate sexes and sexual dimorphism through the build up of an association between sex allocation and the conflict trait, such that eventually the population consists of unisexuals expressing their sex-specific trait optima. We then investigate how such association might materialise genetically, either via recombination suppression or via sex-dependent expression, and show that the genetic architecture of sex allocation and the conflict trait readily evolves to produce the association favoured by selection. Finally, we demonstrate that limited dispersal and self-fertilisation, which are pervasive ecological characteristics of flowering plants, can offset the advantage of sexual specialisation generated by a jointly evolving trait under sexual conflict and maintain hermaphroditism, in agreement with previous theory where sex allocation evolves alone. Taken together, our results indicate that advantages to sexual specialisation are inevitable when there is conflict between sexual functions in hermaphrodites, but can be counterbalanced by ecological benefits of hermaphroditism, underscoring the importance of ecology for sexual system evolution.