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

Quinn K Langdon,Dana A Opulente,María E Rodríguez,Juan I Eizaguirre,Chris Todd Hittinger,Martin Jarzyna,David Peris,Christian A Lopes,Kayla Sylvester,Diego Libkind,Kelly V Buh

doi:10.1371/journal.pgen.1008680

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.

Highlights

In microbial population genomics, the interplay of human association and natural variation is still poorly understood
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
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

Summary

Introduction

The interplay of human association and natural variation is still poorly understood. The genus Saccharomyces is an optimal model to address these questions for eukaryotic microbes, as it contains both partly human-associated species (i.e. Saccharomyces cerevisiae) and mostly wild species (e.g. Saccharomyces paradoxus) These two examples illustrate the complexity of studying yeast population genomics. Other hybrids with contributions from S. eubayanus have been isolated from industrial environments [11,12,13,14], indicating that this species has long been playing a role in shaping many fermented products This association with both natural and domesticated environments makes S. eubayanus an excellent model where both wild diversity and domestication can be investigated

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Discussion

Conclusion