Spore germination determines yeast inbreeding according to fitness in the local environment

Gene combinations conferring local fitness may be destroyed by mating with individuals that are adapted to a different environment. This form of outbreeding depression provides an evolutionary incentive for self-fertilization. We show that the yeast Saccharomyces paradoxus tends to self-fertilize when it is well adapted to its local environment but tends to outcross when it is poorly adapted. This behavior could preserve combinations of genes when they are beneficial and break them up when they are not, thereby helping adaptation. Haploid spores must germinate before mating, and we found that fitter spores had higher rates of germination across a 24-hour period, increasing the probability that they mate with germinated spores from the same meiotic tetrad. The ability of yeast spores to detect local conditions before germinating and mating suggests the novel possibility that these gametes directly sense their own adaptation and plastically adjust their breeding strategy accordingly.