Divergent ecological selection causes reproductive isolation and vast genomic instability in hybrids between experimentally evolved yeast population

Populations evolving independently in divergent environments accumulate genetic differences and potentially evolve reproductive isolation (RI) as a by-product of divergence. The speed and mechanisms underlying this process are difficult to investigate because we rarely get the opportunity to witness them in natural settings. In addition, histories of selection and gene flow between populations are often unknown. Here, we used experimental evolution with yeast across 1000 generations of evolution in both divergent and parallel environments and measured their phenotypic divergence. At regular time points during experimental evolution, we made crosses between parallel- and divergent-evolving populations to measure RI (F2 spore viability). We used whole genome population sequencing to determine mutational load, the number and types of structural variation (a measure of genomic stability), and other genomic features in the parent, F1 and F2 hybrid populations. We found that populations evolving in different environments diverged phenotypically over time and produced hybrid offspring with lower viability, causing up to 50% reproductive isolation. Notably, no hybrid breakdown was observed between parallel-selected populations. We further found that F2 hybrid genomes contained vast genomic instability, i.e. new structural variants (especially insertions and deletions) that were not observed in parent and F1 populations, likely as a result of chromosome missegregation and recombination errors in F1 hybrid meiosis. Our results suggest that RI can evolve rapidly as a consequence of adaptation to divergent environments in sexual microbes, consistent with predictions of ecological speciation theory.