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Abstract

Sex with another species can be disastrous, especially for organisms that mate only once, like yeast [1, 2 and 3]. Courtship signals, including pheromones, often differ between species and can provide a basis for distinguishing between reproductively compatible and incompatible partners [4, 5 and 6]. Remarkably, we show that the baker’s yeast Saccharomyces cerevisiae does not reject mates engineered to produce pheromones from highly diverged species, including species that have been reproductively isolated for up to 100 million years. To determine whether effective discrimination against mates producing pheromones from other species is possible, we experimentally evolved pheromone receptors under conditions that imposed high fitness costs on mating with cells producing diverged pheromones. Evolved receptors allowed both efficient mating with cells producing the S. cerevisiae pheromone and near-perfect discrimination against cells producing diverged pheromones. Sequencing evolved receptors revealed that each contained multiple mutations that altered the amino acid sequence. By isolating individual mutations, we identified specific amino acid changes that dramatically improved discrimination. However, the improved discrimination conferred by these individual mutations came at the cost of reduced mating efficiency with cells producing the S. cerevisiae pheromone, resulting in low fitness. This tradeoff could be overcome by simultaneous introduction of separate mutations that improved mating efficiency alongside those that improved discrimination. Thus, if mutations occur sequentially, the shape of the fitness landscape may prevent evolution of the optimal phenotype [ 7 and 8]—offering a possible explanation for the poor discrimination of receptors found in nature.