A phylogenetic test of the size-advantage model: evolutionary changes in mating behavior influence the loss of sex change in a fish lineage.

The size-advantage model asserts that mating behavior influences the incidence and direction of sex change in animals. Selection for protogyny (female to male sex change) occurs in mating systems in which large males monopolize and pair spawn with females; however, gonochorism (no sex change) is favored when adults spawn in groups and sperm competition is present. Despite widespread empirical and theoretical support for the model, these predictions have not been tested within a phylogenetic context. Here we show that the loss of sex change within a lineage of reef fishes is influenced by evolutionary changes in two traits related to their mating behavior: mating group structure and sperm competition intensity. Phylogenetic reconstructions of the reproductive evolution of groupers (Epinephelidae) indicate that protogyny and paired spawning are the ancestral conditions for the lineage; both gonochorism and group spawning evolved independently at least four times in three different genera. Evolutionary transformations from protogyny to gonochorism (loss of sex change) are associated with equivalent transformations in mating group structure from paired to group spawning, and sperm competition is considerably higher in gonochoric species than in protogynous species. These results provide explicit phylogenetic support for predictions of the size-advantage model, demonstrating that selection for protogynous sex change decreases as mating group size and sperm competition intensity increase.