Ancient and recent origins of shared polymorphisms in yeast

Abstract Shared genetic polymorphisms between populations and species can be ascribed to ancestral variation or to more recent gene flow. Here, we mapped shared polymorphisms in Saccharomyces cerevisiae and its sister species Saccharomyces paradoxus, which diverged 4-6 million years ago. We used a dense map of diagnostic markers (mean distance 15.6 bp) in 1,673 sequenced S. cerevisiae isolates to catalogue 3,852 introgressed blocks (≥ 5 consecutive markers) from S. paradoxus, with the majority being recent and clade-specific. The highly diverged wild Chinese S. cerevisiae lineages were depleted of introgressed blocks, but retained an excess of individual ancestral polymorphisms derived from incomplete lineage sorting, perhaps due to less dramatic population bottlenecks. In the non-Chinese S. cerevisiae lineages, we inferred major hybridisation events and detected cases of overlapping introgressed blocks across distinct clades due to either shared histories or convergent evolution. We experimentally engineered, in otherwise isogenic backgrounds, the introgressed PAD1-FDC1 gene-pair that independently arose in two S. cerevisiae clades and revealed that it potentiates resistance against diverse antifungal drugs and ferulic acid. Overall, our study retraces histories of divergence and secondary contacts across S. cerevisiae and S. paradoxus populations and unveil a functional outcome.