title: Ancient evolutionary trade-offs between yeast ploidy states.
abstract: The number of chromosome sets contained within the nucleus of eukaryotic organisms is a fundamental yet evolutionarily poorly characterized genetic variable of life. Here, we mapped the impact of ploidy on the mitotic fitness of baker's yeast and its never domesticated relative Saccharomyces paradoxus across wide swaths of their natural genotypic and phenotypic space. Surprisingly, environment-specific influences of ploidy on reproduction were found to be the rule rather than the exception. These ploidy-environment interactions were well conserved across the 2 billion generations separating the two species, suggesting that they are the products of strong selection. Previous hypotheses of generalizable advantages of haploidy or diploidy in ecological contexts imposing nutrient restriction, toxin exposure, and elevated mutational loads were rejected in favor of more fine-grained models of the interplay between ecology and ploidy. On a molecular level, cell size and mating type locus composition had equal, but limited, explanatory power, each explaining 12.5%-17% of ploidy-environment interactions. The mechanism of the cell size-based superior reproductive efficiency of haploids during Li(+) exposure was traced to the Li(+) exporter ENA. Removal of the Ena transporters, forcing dependence on the Nha1 extrusion system, completely altered the effects of ploidy on Li(+) tolerance and evoked a strong diploid superiority, demonstrating how genetic variation at a single locus can completely reverse the relative merits of haploidy and diploidy. Taken together, our findings unmasked a dynamic interplay between ploidy and ecology that was of unpredicted evolutionary importance and had multiple molecular roots.
authors.affiliation: Centre for Integrative Genetics, Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, UMB, Ås, Norway.
authors.forename: Enikö
authors.initials: E
authors.lastname: Zörgö
authors.forename: Karolina
authors.initials: K
authors.lastname: Chwialkowska
authors.forename: Arne B
authors.initials: AB
authors.lastname: Gjuvsland
authors.forename: Elena
authors.initials: E
authors.lastname: Garré
authors.forename: Per
authors.initials: P
authors.lastname: Sunnerhagen
authors.forename: Gianni
authors.initials: G
authors.lastname: Liti
authors.forename: Anders
authors.initials: A
authors.lastname: Blomberg
authors.forename: Stig W
authors.initials: SW
authors.lastname: Omholt
authors.forename: Jonas
authors.initials: J
authors.lastname: Warringer
mesh_terms: D005075:Biological Evolution; D048429:Cell Size / Q000187:drug effects; D002875:Chromosomes / Q000187:drug effects / Q000235:genetics; D003300:Copper / Q000633:toxicity; D004171:Diploidy; D004463:Ecology; D019143:Evolution, Molecular; D059647:Gene-Environment Interaction; D049770:Genes, Mating Type, Fungal / Q000187:drug effects / Q000235:genetics; D005838:Genotype; D006238:Haploidy; D008094:Lithium / Q000633:toxicity; D012098:Reproduction / Q000187:drug effects / Q000235:genetics; D012441:Saccharomyces cerevisiae / Q000235:genetics*
chemical_list: D003300:Copper; D008094:Lithium
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