Adaptive benefits of hybridization in Saccharomyces yeast are constrained by genomic background and depend on...

Climate change urges us to better understand and predict evolutionary responses to temperature shifts. Hybridization, by increasing genetic variation, can widen the range of adaptive responses and genetic mechanisms available to survive temperature changes. However, genomic data on the long-term effect of hybridization on adaptation is rare, and the molecular mechanisms usually remain unclear. Here, we hybridized two divergent species of Saccharomyces yeast. We experimentally evolved both hybrid and parental populations for 200 generations under hot (30 °C), cold (16 °C), and fluctuating (16-30 °C) temperature regimes. Most hybrids showed intermediate growth, but the large variance produced by hybridization also led to thermally transgressive hybrids with high performance. Across regimes, response to selection scaled negatively with ancestral growth, consistent with diminishing-returns epistasis. Analysis of genes with identified mutations revealed enrichment in multiple shared annotation terms between populations evolved in cold and fluctuating environments, such as cell wall functions. Evolved hybrid populations, across all evolution regimes, accumulated significantly more de novo copy number variants than both parental species, indicating extensive genome restructuring in hybrids. This increased structural variation may provide a substrate for selection and adaptive divergence among hybrid lineages. Our results suggest that hybridization can lead to increased growth, especially in hot and thermally unstable environments, by capitalizing on the genomic content inherited from one or the other parental species.