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 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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Public Library of Science
2020-04-06
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Subjects: | Phylogeography, Species diversity, South America, Saccharomyces cerevisiae, Europe, Nucleotide sequencing, Saccharomyces, |
Online Access: | http://hdl.handle.net/10261/208424 http://dx.doi.org/10.13039/100000001 http://dx.doi.org/10.13039/100005825 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100006668 |
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Phylogeography Species diversity South America Saccharomyces cerevisiae Europe Nucleotide sequencing Saccharomyces Phylogeography Species diversity South America Saccharomyces cerevisiae Europe Nucleotide sequencing Saccharomyces |
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Phylogeography Species diversity South America Saccharomyces cerevisiae Europe Nucleotide sequencing Saccharomyces Phylogeography Species diversity South America Saccharomyces cerevisiae Europe Nucleotide sequencing Saccharomyces Langdon, Quinn K. Peris, David Eizaguirre, Juan I. Opulente, Dana Buh, Kelly V. Sylvester, Kayla Jarzyna, Martin Rodríguez, María E. Lopes, Christian A. Libkind, Diego Hittinger, Chris Todd Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids |
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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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National Science Foundation (US) |
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National Science Foundation (US) Langdon, Quinn K. Peris, David Eizaguirre, Juan I. Opulente, Dana Buh, Kelly V. Sylvester, Kayla Jarzyna, Martin Rodríguez, María E. Lopes, Christian A. Libkind, Diego Hittinger, Chris Todd |
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Phylogeography Species diversity South America Saccharomyces cerevisiae Europe Nucleotide sequencing Saccharomyces |
author |
Langdon, Quinn K. Peris, David Eizaguirre, Juan I. Opulente, Dana Buh, Kelly V. Sylvester, Kayla Jarzyna, Martin Rodríguez, María E. Lopes, Christian A. Libkind, Diego Hittinger, Chris Todd |
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Langdon, Quinn K. |
title |
Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids |
title_short |
Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids |
title_full |
Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids |
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Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids |
title_full_unstemmed |
Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids |
title_sort |
postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids |
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Public Library of Science |
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2020-04-06 |
url |
http://hdl.handle.net/10261/208424 http://dx.doi.org/10.13039/100000001 http://dx.doi.org/10.13039/100005825 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100006668 |
work_keys_str_mv |
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dig-iata-es-10261-2084242021-12-27T15:31:40Z Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids Langdon, Quinn K. Peris, David Eizaguirre, Juan I. Opulente, Dana Buh, Kelly V. Sylvester, Kayla Jarzyna, Martin Rodríguez, María E. Lopes, Christian A. Libkind, Diego Hittinger, Chris Todd National Science Foundation (US) National Institute of Food and Agriculture (US) European Commission Fondo para la Investigación Científica y Tecnológica (Argentina) Universidad Nacional del Comahue Phylogeography Species diversity South America Saccharomyces cerevisiae Europe Nucleotide sequencing Saccharomyces 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. This material is based upon work supported by the National Science Foundation (https://www.nsf.gov) under Grant Nos. DEB-1253634 (to CTH) and DGE-1256259 (Graduate Research Fellowship to QKL), the USDA National Institute of Food and Agriculture (https://www.nifa.usda.gov) Hatch Project Nos. 1003258 and 1020204 to CTH, and in part by the DOE Great Lakes Bioenergy Research Center (DOE BER Office of Science (https://www.energy.gov/science/office-science) Nos. DE-SC0018409 and DE-FC02-07ER64494 to Timothy J. Donohue). QKL was also supported by the Predoctoral Training Program in Genetics, funded by the National Institutes of Health (5T32GM007133, https://www.nih.gov). DP is a Marie Sklodowska-Curie fellow of the European Union’s Horizon 2020 (https://ec.europa.eu/programmes/horizon2020/en) research and innovation program (Grant Agreement No. 747775). DL was supported by CONICET (PIP11220130100392CO, https://www.conicet.gov.ar), FONCyT (PICT 3677, PICT 2542, https://www.argentina.gob.ar/ciencia/agencia/fondo-para-la-investigacion-cientifica-y-tecnologica-foncyt), Universidad Nacional del Comahue (B199, https://www.uncoma.edu.ar), and NSF-CONICET grant (https://www.conicet.gov.ar). CTH is a Pew Scholar in the Biomedical Sciences and H. I. Romnes Faculty Fellow, supported by the Pew Charitable Trusts (https://www.pewtrusts.org/en) and Office of the Vice Chancellor for Research and Graduate Education (https://research.wisc.edu) with funding from the Wisconsin Alumni Research Foundation (WARF, https://www.warf.org), respectively. Peer reviewed 2020-04-21T10:46:22Z 2020-04-21T10:46:22Z 2020-04-06 artículo http://purl.org/coar/resource_type/c_6501 PLoS Genetics 16(4): e1008680 (2020) http://hdl.handle.net/10261/208424 10.1371/journal.pgen.1008680 1553-7404 http://dx.doi.org/10.13039/100000001 http://dx.doi.org/10.13039/100005825 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100006668 32251477 en #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/H2020/747775 Publisher's version https://doi.org/10.1371/journal.pgen.1008680 Sí open Public Library of Science |