Trait variation in yeast is defined by population history.

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...

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Main Authors: Jonas Warringer, Enikö Zörgö, Francisco A Cubillos, Amin Zia, Arne Gjuvsland, Jared T Simpson, Annabelle Forsmark, Richard Durbin, Stig W Omholt, Edward J Louis, Gianni Liti, Alan Moses, Anders Blomberg
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-06-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1002111&type=printable
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author Jonas Warringer
Enikö Zörgö
Francisco A Cubillos
Amin Zia
Arne Gjuvsland
Jared T Simpson
Annabelle Forsmark
Richard Durbin
Stig W Omholt
Edward J Louis
Gianni Liti
Alan Moses
Anders Blomberg
author_facet Jonas Warringer
Enikö Zörgö
Francisco A Cubillos
Amin Zia
Arne Gjuvsland
Jared T Simpson
Annabelle Forsmark
Richard Durbin
Stig W Omholt
Edward J Louis
Gianni Liti
Alan Moses
Anders Blomberg
author_sort Jonas Warringer
collection DOAJ
description 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.
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spelling doaj-art-18cf6777a2f248a09bcb40ef762065762025-08-20T02:05:38ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042011-06-0176e100211110.1371/journal.pgen.1002111Trait variation in yeast is defined by population history.Jonas WarringerEnikö ZörgöFrancisco A CubillosAmin ZiaArne GjuvslandJared T SimpsonAnnabelle ForsmarkRichard DurbinStig W OmholtEdward J LouisGianni LitiAlan MosesAnders BlombergA 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.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1002111&type=printable
spellingShingle Jonas Warringer
Enikö Zörgö
Francisco A Cubillos
Amin Zia
Arne Gjuvsland
Jared T Simpson
Annabelle Forsmark
Richard Durbin
Stig W Omholt
Edward J Louis
Gianni Liti
Alan Moses
Anders Blomberg
Trait variation in yeast is defined by population history.
PLoS Genetics
title Trait variation in yeast is defined by population history.
title_full Trait variation in yeast is defined by population history.
title_fullStr Trait variation in yeast is defined by population history.
title_full_unstemmed Trait variation in yeast is defined by population history.
title_short Trait variation in yeast is defined by population history.
title_sort trait variation in yeast is defined by population history
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1002111&type=printable
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