Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids
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 w...
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creator | Langdon, Quinn K Peris, David Eizaguirre, Juan I Opulente, Dana A Buh, Kelly V Sylvester, Kayla Jarzyna, Martin Rodríguez, María E Lopes, Christian A Libkind, Diego Hittinger, Chris Todd |
description | 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. |
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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.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1008680</identifier><identifier>PMID: 32251477</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>BASIC BIOLOGICAL SCIENCES ; biogeography ; Biology and Life Sciences ; Brewing ; Datasets ; Domestication ; Earth Sciences ; Ecology and Environmental Sciences ; Ecosystem ; Energy ; Europe ; Evolution ; Evolution, Molecular ; Funding ; Gene flow ; Genetic diversity ; Genome, Fungal ; Genomes ; Genomics ; Host plants ; Hybridization, Genetic ; Hybrids ; Innovations ; Laboratories ; Lager ; Nucleotide sequence ; nucleotide sequencing ; People and places ; Phylogeography ; Polymorphism, Genetic ; Population ; Population structure ; Principal components analysis ; Research and Analysis Methods ; Saccharomyces ; Saccharomyces - genetics ; Saccharomyces - physiology ; Saccharomyces cerevisiae ; Sibling species ; South America ; species diversity ; Studies ; Subpopulations ; Supervision ; Sympatric populations</subject><ispartof>PLoS genetics, 2020-04, Vol.16 (4), p.e1008680-e1008680</ispartof><rights>2020 Langdon et al. 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We conclude that this industrially relevant species has rich natural diversity with many factors contributing to its complex distribution and natural history.</description><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>biogeography</subject><subject>Biology and Life Sciences</subject><subject>Brewing</subject><subject>Datasets</subject><subject>Domestication</subject><subject>Earth Sciences</subject><subject>Ecology and Environmental Sciences</subject><subject>Ecosystem</subject><subject>Energy</subject><subject>Europe</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Funding</subject><subject>Gene flow</subject><subject>Genetic diversity</subject><subject>Genome, Fungal</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Host plants</subject><subject>Hybridization, Genetic</subject><subject>Hybrids</subject><subject>Innovations</subject><subject>Laboratories</subject><subject>Lager</subject><subject>Nucleotide 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migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids</title><author>Langdon, Quinn K ; Peris, David ; Eizaguirre, Juan I ; Opulente, Dana A ; Buh, Kelly V ; Sylvester, Kayla ; Jarzyna, Martin ; Rodríguez, María E ; Lopes, Christian A ; Libkind, Diego ; Hittinger, Chris Todd</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c553t-ec2b79d16a50b2f59ea37bb315a1a389ed3bfbf9f286aee8c58126faf46f537e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>biogeography</topic><topic>Biology and Life Sciences</topic><topic>Brewing</topic><topic>Datasets</topic><topic>Domestication</topic><topic>Earth Sciences</topic><topic>Ecology and Environmental Sciences</topic><topic>Ecosystem</topic><topic>Energy</topic><topic>Europe</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Funding</topic><topic>Gene flow</topic><topic>Genetic diversity</topic><topic>Genome, Fungal</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Host plants</topic><topic>Hybridization, Genetic</topic><topic>Hybrids</topic><topic>Innovations</topic><topic>Laboratories</topic><topic>Lager</topic><topic>Nucleotide sequence</topic><topic>nucleotide sequencing</topic><topic>People and places</topic><topic>Phylogeography</topic><topic>Polymorphism, Genetic</topic><topic>Population</topic><topic>Population structure</topic><topic>Principal components analysis</topic><topic>Research and Analysis Methods</topic><topic>Saccharomyces</topic><topic>Saccharomyces - genetics</topic><topic>Saccharomyces - physiology</topic><topic>Saccharomyces cerevisiae</topic><topic>Sibling species</topic><topic>South America</topic><topic>species diversity</topic><topic>Studies</topic><topic>Subpopulations</topic><topic>Supervision</topic><topic>Sympatric 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Diego</au><au>Hittinger, Chris Todd</au><aucorp>Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2020-04-01</date><risdate>2020</risdate><volume>16</volume><issue>4</issue><spage>e1008680</spage><epage>e1008680</epage><pages>e1008680-e1008680</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32251477</pmid><doi>10.1371/journal.pgen.1008680</doi><orcidid>https://orcid.org/0000-0003-3224-7510</orcidid><orcidid>https://orcid.org/0000-0003-4570-7432</orcidid><orcidid>https://orcid.org/0000-0001-9687-6186</orcidid><orcidid>https://orcid.org/0000-0001-9912-8802</orcidid><orcidid>https://orcid.org/0000-0003-0604-7208</orcidid><orcidid>https://orcid.org/0000-0002-3565-5811</orcidid><orcidid>https://orcid.org/0000-0002-2485-6589</orcidid><orcidid>https://orcid.org/0000-0001-5088-7461</orcidid><orcidid>https://orcid.org/0000000306047208</orcidid><orcidid>https://orcid.org/0000000224856589</orcidid><orcidid>https://orcid.org/0000000196876186</orcidid><orcidid>https://orcid.org/0000000199128802</orcidid><orcidid>https://orcid.org/0000000345707432</orcidid><orcidid>https://orcid.org/0000000150887461</orcidid><orcidid>https://orcid.org/0000000332247510</orcidid><orcidid>https://orcid.org/0000000235655811</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1553-7404 |
ispartof | PLoS genetics, 2020-04, Vol.16 (4), p.e1008680-e1008680 |
issn | 1553-7404 1553-7390 1553-7404 |
language | eng |
recordid | cdi_plos_journals_2403774498 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Public Library of Science (PLoS) |
subjects | BASIC BIOLOGICAL SCIENCES biogeography Biology and Life Sciences Brewing Datasets Domestication Earth Sciences Ecology and Environmental Sciences Ecosystem Energy Europe Evolution Evolution, Molecular Funding Gene flow Genetic diversity Genome, Fungal Genomes Genomics Host plants Hybridization, Genetic Hybrids Innovations Laboratories Lager Nucleotide sequence nucleotide sequencing People and places Phylogeography Polymorphism, Genetic Population Population structure Principal components analysis Research and Analysis Methods Saccharomyces Saccharomyces - genetics Saccharomyces - physiology Saccharomyces cerevisiae Sibling species South America species diversity Studies Subpopulations Supervision Sympatric populations |
title | Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids |
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