Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids

Abstract

The wild, cold-adapted parent of hybrid lager-brewing yeasts, Saccharomyces eubayanus, has a complex and understudied natural history. The exploration of this diversity can be used both to develop new brewing applications and to enlighten our understanding of the dynamics of yeast evolution in the wild. Here, we integrate whole genome sequence and phenotypic data of 200 S. eubayanus strains, the largest collection known to date. S. eubayanus has a multilayered population structure, consisting of two major populations that are further structured into six subpopulations. Four of these subpopulations are found exclusively in the Patagonian region of South America; one is found predominantly in Patagonia and sparsely in Oceania and North America; and one is specific to the Holarctic ecozone. Plant host associations differed between subpopulations and between S. eubayanus and its sister species, Saccharomyces uvarum. S. eubayanus is most abundant and genetically diverse in northern Patagonia, where some locations harbor more genetic diversity than is found outside of South America, suggesting that northern Patagonia east of the Andes was a glacial refugium for this species. All but one subpopulation shows isolation-by-distance, and gene flow between subpopulations is low. However, there are strong signals of ancient and recent outcrossing, including two admixed lineages, one that is sympatric with and one that is mostly isolated from its parental populations. Using our extensive biogeographical data, we build a robust model that predicts all known and a handful of additional regions of the globe that are climatically suitable for S. eubayanus, including Europe where host accessibility and competitive exclusion by other Saccharomyces species may explain its continued elusiveness. We conclude that this industrially relevant species has rich natural diversity with many factors contributing to its complex distribution and natural history. The mysterious wild parent of hybrid-lager brewing yeasts, Saccharomyces eubayanus, has been known for less than 10 years. In this time, it has become clear that lager hybrids arose from a subpopulation that has only been isolated in Tibet and North Carolina, USA; but the global diversity of this species has been less explored. Here, we use whole genome sequencing data for 200 strains (174 newly sequenced) to investigate the genetic diversity and geographical distribution of S. eubayanus. We find that its extensive wild diversity is largely centered in northern Patagonia, which likely was a glacial refugium for this species as three of six subpopulations are endemic to this region. In contrast, S. eubayanus is rarely isolated outside of Patagonia. In North America, isolates are dominated by an invasive, near-clonal admixed lineage; the result of an outcrossing and migration event. All subpopulations are well-differentiated, with low gene flow between them. This genetic isolation of subpopulations could be due to ecological factors, such as plant host associations. With modeling, we find that many areas of the world are climatically suitable to S. eubayanus, including Europe, where it has never been isolated. We propose complex ancestries and rich ecologies underlie the global distribution and diversity of this elusive and industrially important species.