Evolutionary responses to increased opportunity for sexual selection in yeast

Sexual selection contributes to biodiversity and the costs and benefits of sexual reproduction. In organisms where sex is infrequent, these impacts of sexual selection are likely to be limited. An increased frequency of obligate sex would increase the opportunity for sexual selection, which could promote the evolution of sexual traits and sexual differentiation. To study these dynamics, we conducted experimental evolution in the yeast Saccharomyces cerevisiae, which is predominantly asexual, with two isogamous mating types. We used selectable markers to impose frequent obligate sex in 96 populations. We manipulated the opportunity for sexual selection by imposing skewed mating-type ratios and by altering the degree to which mating occurred by selfing versus outcrossing. After just ten sexual cycles, we observed evolution in growth, cell size, pheromone production, and mating, with the mating types responding asymmetrically, but little evolutionary change in sporulation rate. Mating type dimorphism increased, with evident trade-offs between growth, attractiveness, and cell size. Genome sequences from a subset of populations revealed many mutations affecting sex-related genes. Unexpectedly, the selfing populations evolved to become sporulation-competent haploids, unlinking meiosis from ploidy change. Our results illustrate that sexual differentiation can evolve rapidly in response to an increased opportunity for sexual selection.