Abstract

Population‐level sampling and whole‐genome sequences of different individuals allow one to identify signatures of hybridization, gene flow and potential molecular mechanisms of environmental responses. Here, we report the isolation of 160 Saccharomyces eubayanus strains, the cryotolerant ancestor of lager yeast, from ten sampling sites in Patagonia along 2,000 km of Nothofagus forests. Frequency of S. eubayanus isolates was higher towards southern and colder regions, demonstrating the cryotolerant nature of the species. We sequenced the genome of 82 strains and, together with 23 available genomes, performed a comprehensive phylogenetic analysis. Our results revealed the presence of five different lineages together with dozens of admixed strains. Various analytical methods reveal evidence of gene flow and historical admixture between lineages from Patagonia and Holarctic regions, suggesting the co-occurrence of these ancestral populations. Analysis of the genetic contribution to the admixed genomes revealed a Patagonian genetic origin of the admixed strains, even for those located in the North Hemisphere. Overall, the Patagonian lineages, particularly the southern populations, showed a greater global genetic diversity compared to Holarctic and Chinese lineages, in agreement with a higher abundance in Patagonia. Thus, our results are consistent with a likely colonization of the species from peripheral glacial refugia from South Patagonia. Furthermore, fermentative capacity and maltose consumption resulted negatively correlated with latitude, indicating better fermentative performance in northern populations. Our genome analysis, together with previous reports in the sister species S. uvarum suggests that a S. eubayanus ancestor was adapted to the harsh environmental conditions of Patagonia, a region that provides the ecological conditions for the diversification of these ancestral lineages.

Highlights

  • The identification of admixed and/or hybrid individuals in nature together with the geographic distribution of ecologically relevant traits is crucial for the understanding of how new lineages diversify in a given climate/region/environment [1]

  • The recent isolation of S. eubayanus, the lager yeast ancestor, represents an unprecedented opportunity to extend our knowledge on yeast phylogeography and the origins of the S. pastorianus lager hybrid

  • Our work demonstrates that S. eubayanus isolates from Patagonia have the greatest genetic diversity, comprising the largest number of lineages within a single geographic region and experienced ancestral and recent admixture between lineages, likely suggesting co-occurrence in Patagonia

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Summary

Introduction

The identification of admixed and/or hybrid individuals in nature together with the geographic distribution of ecologically relevant traits is crucial for the understanding of how new lineages diversify in a given climate/region/environment [1]. Studies addressing admixture in fungi are still uncommon. In this context, the utilization of population-level sampling and whole-genome sequences involving large sets of individuals allows studying genetic correlations by exploring patterns of genomic variation across lineages and identifying signatures of gene flow, revealing potential mechanisms of physiological adjustment to the environment [2]. Given the economic importance of this clade, as well as the wealth of genomic information that has been produced in the past decade, for the model organism S. cerevisiae [5,6,7,8,9,10], natural populations of Saccharomyces are excellent models for understanding genome evolution in the wild

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