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.

An Out-of-Patagonia migration explains the worldwide diversity and distribution of Saccharomyces eubayanus lineages

“…However, the widespread distribution and higher abundance of N. pumilio in Tierra del Fuego compared to northern areas may facilitate the survival, range distribution, and habitat colonization of S. eubayanus [31], thus increasing its population size and genetic diversity. The isolation frequency of S. eubayanus in Patagonia was three times higher than that reported in China and North America, where a similar number of bark samples and sampling sites were surveyed [23][24][25]. Our results are also in agreement with those reported for S. eubayanus in Argentina, where high isolation rates in N. pumilio trees were also found [20].…”

“…Subsequently, a step-wise wave of dispersion-colonization of Nothofagus in a westward direction reached South America. This scenario is consistent with a colonization of the S. eubayanus and S. uvarum ancestor across the South Hemisphere [23,32].…”

“…This initial assessment of admixture allowed us to determine that strains isolated from Karukinka (SoAm-3) likely originated from the same admixture event between PB-1 and PB-3 lineages, as 92% of their bins were assigned to the same lineage ( Fig 4A). A common origin is also predicted for the North American admixed strains (NoAm) as previously reported [22,23,25], where a PB-1 origin contributes to the genome of all isolates.…”

“…The phylogenomic analysis presented here of wild S. eubayanus (Fig 2) reveals a higher genetic diversity for the PB South American lineages than that reported for S. eubayanus in the Northern Hemisphere [23,25]. Indeed, our results resemble those obtained in the sister species for S. uvarum, where similar sequence divergence among S. uvarum populations was described [13], whereas in Chinese S. cerevisiae, a much higher genetic diversity is observed compared to other regions of the world [33].…”

“…Despite the industrial importance of S. pastorianus, much of the natural history of this hybrid remains obscure, largely because the S. eubayanus parental species was only recently isolated [19]. S. eubayanus was originally isolated from Nothofagus trees in the Argentinian Patagonia [19,20] and since then it has been isolated in New Zealand [21], North America [22,23] and East Asia [24]. However, the evolutionary origin of S. eubayanus is still controversial.…”