Climate-driven adaptive microevolution in wild yeasts

Environmental variation imposes strong selection on microbial populations, yet linking ecological gradients to genomic and phenotypic diversification remains challenging due to limited sampling of wild microbes. Here, we leveraged the exceptional abundance of the cold-adapted yeast Saccharomyces eubayanus throughout Patagonian Nothofagus forests to investigate how climatic gradients shape natural microbial diversity. Using systematic sampling across ~1,000 km of Chilean Patagonia, spanning multiple seasons, altitudes, and thermal regimes, we integrated environmental, genomic, and phenotypic analyses of wild populations inhabiting Nothofagus forests. Whole-genome sequencing of 117 isolates identified three major Patagonian lineages that show strong latitudinal structuring and contrasting levels of nucleotide diversity, with colder, wetter southern populations harboring the greatest diversity. Multivariate and permutation-based analyses consistently identified latitude, temperature, and precipitation as the primary correlates of genomic variation, together explaining over half of the observed patterns of nucleotide diversity. Notably, S. eubayanus exhibited an inverse latitudinal diversity gradient, contrasting with patterns commonly reported in Northern Hemisphere populations. Climatic structuring was mirrored by pronounced phenotypic differentiation: Southern populations exhibited lower thermal optima, enhanced cold fitness, and increased sporulation capacity, whereas northern populations displayed greater growth performance under nutrient-rich and hyperosmotic conditions. Sporulation capacity closely paralleled nucleotide diversity along the same environmental gradient, linking climate, reproductive investment, and population diversification. Together, our results indicate that climatic gradients simultaneously shape demographic history, physiological performance, metabolic strategies, and life-history traits in natural yeast populations. More broadly, Patagonia emerges as a powerful natural system for understanding how environmental heterogeneity drives microbial diversification across heterogeneous landscapes.