title: Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus.
abstract: Lager-style beers constitute the vast majority of the beer market, and yet, the genetic origin of the yeast strains that brew them has been shrouded in mystery and controversy. Unlike ale-style beers, which are generally brewed with Saccharomyces cerevisiae, lagers are brewed at colder temperatures with allopolyploid hybrids of Saccharomyces eubayanus x S. cerevisiae. Since the discovery of S. eubayanus in 2011, additional strains have been isolated from South America, North America, Australasia, and Asia, but only interspecies hybrids have been isolated in Europe. Here, using genome sequence data, we examine the relationships of these wild S. eubayanus strains to each other and to domesticated lager strains. Our results support the existence of a relatively low-diversity (π = 0.00197) lineage of S. eubayanus whose distribution stretches across the Holarctic ecozone and includes wild isolates from Tibet, new wild isolates from North America, and the S. eubayanus parents of lager yeasts. This Holarctic lineage is closely related to a population with higher diversity (π = 0.00275) that has been found primarily in South America but includes some widely distributed isolates. A second diverse South American population (π = 0.00354) and two early-diverging Asian subspecies are more distantly related. We further show that no single wild strain from the Holarctic lineage is the sole closest relative of lager yeasts. Instead, different parts of the genome portray different phylogenetic signals and ancestry, likely due to outcrossing and incomplete lineage sorting. Indeed, standing genetic variation within this wild Holarctic lineage of S. eubayanus is responsible for genetic variation still segregating among modern lager-brewing hybrids. We conclude that the relationships among wild strains of S. eubayanus and their domesticated hybrids reflect complex biogeographical and genetic processes.
authors.affiliation: Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
authors.forename: David
authors.identifier: 0000-0001-9912-8802
authors.initials: D
authors.lastname: Peris
authors.affiliation: Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
authors.forename: Quinn K
authors.initials: QK
authors.lastname: Langdon
authors.affiliation: Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
authors.forename: Ryan V
authors.identifier: 0000-0001-7100-1906
authors.initials: RV
authors.lastname: Moriarty
authors.affiliation: Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
authors.forename: Kayla
authors.initials: K
authors.lastname: Sylvester
authors.affiliation: Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
authors.forename: Martin
authors.identifier: 0000-0003-3013-6155
authors.initials: M
authors.lastname: Bontrager
authors.affiliation: Institut de Biologie Intégrative et des Systèmes (IBIS), Département de Biologie, PROTEO, Pavillon Charles-Eugène-Marchand, Université Laval, Québec City, Québec, Canada.
authors.forename: Guillaume
authors.initials: G
authors.lastname: Charron
authors.affiliation: Institut de Biologie Intégrative et des Systèmes (IBIS), Département de Biologie, PROTEO, Pavillon Charles-Eugène-Marchand, Université Laval, Québec City, Québec, Canada.
authors.forename: Jean-Baptiste
authors.initials: JB
authors.lastname: Leducq
authors.affiliation: Institut de Biologie Intégrative et des Systèmes (IBIS), Département de Biologie, PROTEO, Pavillon Charles-Eugène-Marchand, Université Laval, Québec City, Québec, Canada.
authors.forename: Christian R
authors.initials: CR
authors.lastname: Landry
authors.affiliation: Laboratorio de Microbiología Aplicada, Biotecnología y Bioinformática, Instituto Andino Patagonico de Tecnologías Biológicas y Geoambientales, IPATEC (CONICET-UNComahue), Centro Regional Universitario Bariloche, Bariloche, Río Negro, Argentina.
authors.forename: Diego
authors.initials: D
authors.lastname: Libkind
authors.affiliation: Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
authors.forename: Chris Todd
authors.initials: CT
authors.lastname: Hittinger
mesh_terms: D001515:Beer / Q000145:classification / Q000382:microbiology*; D005060:Europe; D005285:Fermentation; D014644:Genetic Variation; D016681:Genome, Fungal; D006824:Hybridization, Genetic; D009656:North America; D010802:Phylogeny; D012440:Saccharomyces / Q000235:genetics* / Q000378:metabolism; D012441:Saccharomyces cerevisiae / Q000235:genetics; D013020:South America; D018609:Tibet