title: Concerted evolution of life stage performances signals recent selection on yeast nitrogen use.
abstract: Exposing natural selection driving phenotypic and genotypic adaptive differentiation is an extraordinary challenge. Given that an organism's life stages are exposed to the same environmental variations, we reasoned that fitness components, such as the lag, rate, and efficiency of growth, directly reflecting performance in these life stages, should often be selected in concert. We therefore conjectured that correlations between fitness components over natural isolates, in a particular environmental context, would constitute a robust signal of recent selection. Critically, this test for selection requires fitness components to be determined by different genetic loci. To explore our conjecture, we exhaustively evaluated the lag, rate, and efficiency of asexual population growth of natural isolates of the model yeast Saccharomyces cerevisiae in a large variety of nitrogen-limited environments. Overall, fitness components were well correlated under nitrogen restriction. Yeast isolates were further crossed in all pairwise combinations and coinheritance of each fitness component and genetic markers were traced. Trait variations tended to map to quantitative trait loci (QTL) that were private to a single fitness component. We further traced QTLs down to single-nucleotide resolution and uncovered loss-of-function mutations in RIM15, PUT4, DAL1, and DAL4 as the genetic basis for nitrogen source use variations. Effects of SNPs were unique for a single fitness component, strongly arguing against pleiotropy between lag, rate, and efficiency of reproduction under nitrogen restriction. The strong correlations between life stage performances that cannot be explained by pleiotropy compellingly support adaptive differentiation of yeast nitrogen source use and suggest a generic approach for detecting selection.
authors.affiliation: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
authors.forename: Sebastian
authors.initials: S
authors.lastname: Ibstedt
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences (UMB), Ås, Norway.
authors.forename: Simon
authors.initials: S
authors.lastname: Stenberg
authors.affiliation: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
authors.forename: Sara
authors.initials: S
authors.lastname: Bagés
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences (UMB), Ås, Norway.
authors.forename: Arne B
authors.initials: AB
authors.lastname: Gjuvsland
authors.affiliation: IRCAN, CNRS UMR 6267, INSERM U998, University of Nice, Nice, France.
authors.forename: Francisco
authors.initials: F
authors.lastname: Salinas
authors.affiliation: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
authors.forename: Olga
authors.initials: O
authors.lastname: Kourtchenko
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences (UMB), Ås, Norway.
authors.forename: Jeevan K A
authors.initials: JK
authors.lastname: Samy
authors.affiliation: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
authors.forename: Anders
authors.initials: A
authors.lastname: Blomberg
authors.affiliation: Department of Biotechnology, Faculty of Natural Sciences and Technology, Norwegian University of Science and Technology, Trondheim, Norway.
authors.forename: Stig W
authors.initials: SW
authors.lastname: Omholt
authors.affiliation: IRCAN, CNRS UMR 6267, INSERM U998, University of Nice, Nice, France.
authors.forename: Gianni
authors.initials: G
authors.lastname: Liti
authors.affiliation: Department of Biochemistry and Biotechnology, Universitat Rovira i Virgili, Tarragona, Spain.
authors.forename: Gemma
authors.initials: G
authors.lastname: Beltran
authors.affiliation: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences (UMB), Ås, Norway jonas.warringer@cmb.gu.se.
authors.forename: Jonas
authors.initials: J
authors.lastname: Warringer
mesh_terms: D000581:Amidohydrolases / Q000235:genetics / Q000378:metabolism; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D056084:Genetic Fitness; D005838:Genotype; D008565:Membrane Proteins / Q000235:genetics / Q000378:metabolism; D026901:Membrane Transport Proteins / Q000235:genetics / Q000378:metabolism; D009584:Nitrogen / Q000378:metabolism*; D010641:Phenotype; D020641:Polymorphism, Single Nucleotide; D011494:Protein Kinases / Q000235:genetics / Q000378:metabolism; D040641:Quantitative Trait Loci; D012441:Saccharomyces cerevisiae / Q000235:genetics / Q000254:growth & development* / Q000378:metabolism; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics / Q000378:metabolism; D012641:Selection, Genetic
chemical_list: D001426:Bacterial Proteins; C503298:DAL4 protein, S cerevisiae; D008565:Membrane Proteins; D026901:Membrane Transport Proteins; C080683:PutA protein, Bacteria; D029701:Saccharomyces cerevisiae Proteins; D011494:Protein Kinases; C410736:Rim15 protein, S cerevisiae; D000581:Amidohydrolases; C492138:DAL1 protein, S cerevisiae; D009584:Nitrogen
keywords: adaptation; life history; metabolism; nitrogen; selection; yeast