From Oak to Wine: Evolution, Admixture, and Adaptation of California and British Columbia Saccharomyces cerevisiae Wine Strains

Abstract

Population admixture is a frequent outcome of range expansion among plants, animals, and fungi, and drives rapid genome diversification and adaptation. The globalization of winemaking has introduced domesticated European Saccharomyces cerevisiae wine strains into North America, promoting admixture between distantly related lineages. However, the degree that admixture has shaped biological diversity and adaptation within S. cerevisiae remains unclear. Here, we integrate population genetics, high-throughput phenotyping, and gene-trait mapping to characterize the evolutionary impact of S. cerevisiae admixture in North American wine regions. Whole-genome surveys of wine and oak-associated S. cerevisiae strains isolated from California reveal regional diversification of wine strains, with a subset clustering within the Pacific West Coast Wine (PWCW) clade. The PWCW clade is an admixed population derived from Wine/European and North American oak strains first described in Canada. Phylogenetic analyses further suggest that admixture within the PWCW clade has been driven by recent east-west dispersal of a North American Oak lineage into California. Solid-agar phenotyping revealed key wine and oak-associated traits selected for within PWCW clade strains, including stress resistance, nitrogen utilization, and temperature tolerance, while high-throughput microvinifications showed strong association between phylogenetic placement, fermentation completeness, and metabolite production. Genome-wide association identified loci underlying adaptive phenotypes, including copy number variation and chromosomal rearrangements linked to key stress resistance traits. Collectively, these results uncover ongoing adaptation and admixing between North American S. cerevisiae strains, as driven by winemaking practices, and advance our understanding into how admixture influences genome evolution and adaptation.