The distribution of beneficial mutational effects between two sister yeast species poorly explains natural outcomes of vineyard adaptation

Abstract

AbstractDomesticated strains ofSaccharomyces cerevisiaehave adapted to resist copper and sulfite, two chemical stressors commonly used in winemaking.S. paradoxus, has not adapted to these chemicals despite being consistently present in sympatry withS. cerevisiaein vineyards. This contrast represents a case of apparent evolutionary constraints favoring greater adaptive capacity inS. cerevisiae. In this study, we used a comparative mutagenesis approach to test whetherS. paradoxusis mutationally constrained with respect to acquiring greater copper and sulfite resistance. For both species, we assayed the rate, effect size, and pleiotropic costs of resistance mutations and sequenced a subset of 150 mutants isolated from our screen. We found that the distributions of mutational effects displayed by the two species were very similar and poorly explained the natural pattern. We also found that chromosome VIII aneuploidy and loss of function mutations inPMA1confer copper resistance in both species, whereas loss of function mutations inREG1were only a viable route to copper resistance inS. cerevisiae. We also observed a singlede novoduplication of theCUP1gene inS. paradoxusbut none inS. cerevisiae. For sulfite, loss of function mutations inRTS1andKSP1confer resistance in both species, but mutations inRTS1have larger average effects inS. paradoxus. Our results show that even when the distributions of mutational effects are largely similar, species can differ in the adaptive paths available to them. They also demonstrate that assays of the distribution of mutational effects may lack predictive insight concerning adaptive outcomes.