title: Trait variation in yeast is defined by population history.
abstract: A fundamental goal in biology is to achieve a mechanistic understanding of how and to what extent ecological variation imposes selection for distinct traits and favors the fixation of specific genetic variants. Key to such an understanding is the detailed mapping of the natural genomic and phenomic space and a bridging of the gap that separates these worlds. Here we chart a high-resolution map of natural trait variation in one of the most important genetic model organisms, the budding yeast Saccharomyces cerevisiae, and its closest wild relatives and trace the genetic basis and timing of major phenotype changing events in its recent history. We show that natural trait variation in S. cerevisiae exceeds that of its relatives, despite limited genetic variation, and follows the population history rather than the source environment. In particular, the West African population is phenotypically unique, with an extreme abundance of low-performance alleles, notably a premature translational termination signal in GAL3 that cause inability to utilize galactose. Our observations suggest that many S. cerevisiae traits may be the consequence of genetic drift rather than selection, in line with the assumption that natural yeast lineages are remnants of recent population bottlenecks. Disconcertingly, the universal type strain S288C was found to be highly atypical, highlighting the danger of extrapolating gene-trait connections obtained in mosaic, lab-domesticated lineages to the species as a whole. Overall, this study represents a step towards an in-depth understanding of the causal relationship between co-variation in ecology, selection pressure, natural traits, molecular mechanism, and alleles in a key model organism.
authors.affiliation: Department of Cell and Molecular Biology, University of Gothenburg, Gothenburg, Sweden. Jonas.Warringer@cmb.gu.se
authors.forename: Jonas
authors.initials: J
authors.lastname: Warringer
authors.forename: Enikö
authors.initials: E
authors.lastname: Zörgö
authors.forename: Francisco A
authors.initials: FA
authors.lastname: Cubillos
authors.forename: Amin
authors.initials: A
authors.lastname: Zia
authors.forename: Arne
authors.initials: A
authors.lastname: Gjuvsland
authors.forename: Jared T
authors.initials: JT
authors.lastname: Simpson
authors.forename: Annabelle
authors.initials: A
authors.lastname: Forsmark
authors.forename: Richard
authors.initials: R
authors.lastname: Durbin
authors.forename: Stig W
authors.initials: SW
authors.lastname: Omholt
authors.forename: Edward J
authors.initials: EJ
authors.lastname: Louis
authors.forename: Gianni
authors.initials: G
authors.lastname: Liti
authors.forename: Alan
authors.initials: A
authors.lastname: Moses
authors.forename: Anders
authors.initials: A
authors.lastname: Blomberg
mesh_terms: D000354:Africa, Western; D000483:Alleles; D005075:Biological Evolution; D049109:Cell Proliferation; D004463:Ecology; D005656:Fungal Proteins / Q000235:genetics / Q000378:metabolism; D005690:Galactose / Q000378:metabolism; D014644:Genetic Variation; D053858:Metabolic Networks and Pathways / Q000235:genetics; D010641:Phenotype; D040641:Quantitative Trait Loci / Q000235:genetics; D012440:Saccharomyces / Q000166:cytology / Q000235:genetics* / Q000378:metabolism; D012441:Saccharomyces cerevisiae / Q000166:cytology / Q000235:genetics / Q000378:metabolism; D012641:Selection, Genetic; D013045:Species Specificity
chemical_list: D005656:Fungal Proteins; D005690:Galactose