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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.

SUBMITTER: Warringer J

PROVIDER: S-EPMC3116910 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Developing population models for assessing risks to terrestrial plant species listed as threatened or endangered under the Endangered Species Act (ESA) is challenging given a paucity of data on their life histories. The purpose of this study was to develop a novel approach for identifying relatively data-rich nonlisted species that could serve as representatives for species listed under the ESA in the development of population models to inform risk assessments. We used the USDA PLANTS Database, which provides data on plants present in the US territories, to create a list of herbaceous plants. A total of 8742 species was obtained, of which 344 were listed under the ESA. Using the most up-to-date phylogeny for vascular plants in combination with a database of matrix population models for plants (COMPADRE) and cluster analyses, we investigated how listed species were distributed across the plant phylogeny, grouped listed and nonlisted species according to their life history, and identified the traits distinguishing the clusters. We performed elasticity analyses to determine the relative sensitivity of population growth rate to perturbations of species' survival, growth, and reproduction and compared these across clusters and between listed and nonlisted species. We found that listed species were distributed widely across the plant phylogeny as well as clusters, suggesting that listed species do not share a common evolution or life-history characteristics that would make them uniquely vulnerable. Lifespan and age at maturity were more important for distinguishing clusters than were reproductive traits. For clusters that were intermediate in their lifespan, listed and nonlisted species responded similarly to perturbations of their life histories. However, for clusters at either extreme of lifespan, the response to survival perturbations varied depending on conservation status. These results can be used to guide the choice of representative species for population model development in the context of ecological risk assessment. Integr Environ Assess Manag 2023;19:213-223. © 2022 The Authors. Integrated Environmental Assessment and Management published by Wiley Periodicals LLC on behalf of Society of Environmental Toxicology & Chemistry (SETAC).

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Trait variation in yeast is defined by population history.

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