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Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments

One of the central goals of evolutionary biology is to explain and predict the molecular basis of adaptive evolution. We studied the evolution of genetic networks in Saccharomyces cerevisiae (budding yeast) populations propagated for more than 200 generations in different nitrogen-limiting condition...

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Autores principales: Hong, Jungeui, Gresham, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3886903/
https://www.ncbi.nlm.nih.gov/pubmed/24415948
http://dx.doi.org/10.1371/journal.pgen.1004041
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author Hong, Jungeui
Gresham, David
author_facet Hong, Jungeui
Gresham, David
author_sort Hong, Jungeui
collection PubMed
description One of the central goals of evolutionary biology is to explain and predict the molecular basis of adaptive evolution. We studied the evolution of genetic networks in Saccharomyces cerevisiae (budding yeast) populations propagated for more than 200 generations in different nitrogen-limiting conditions. We find that rapid adaptive evolution in nitrogen-poor environments is dominated by the de novo generation and selection of copy number variants (CNVs), a large fraction of which contain genes encoding specific nitrogen transporters including PUT4, DUR3 and DAL4. The large fitness increases associated with these alleles limits the genetic heterogeneity of adapting populations even in environments with multiple nitrogen sources. Complete identification of acquired point mutations, in individual lineages and entire populations, identified heterogeneity at the level of genetic loci but common themes at the level of functional modules, including genes controlling phosphatidylinositol-3-phosphate metabolism and vacuole biogenesis. Adaptive strategies shared with other nutrient-limited environments point to selection of genetic variation in the TORC1 and Ras/PKA signaling pathways as a general mechanism underlying improved growth in nutrient-limited environments. Within a single population we observed the repeated independent selection of a multi-locus genotype, comprised of the functionally related genes GAT1, MEP2 and LST4. By studying the fitness of individual alleles, and their combination, as well as the evolutionary history of the evolving population, we find that the order in which these mutations are acquired is constrained by epistasis. The identification of repeatedly selected variation at functionally related loci that interact epistatically suggests that gene network polymorphisms (GNPs) may be a frequent outcome of adaptive evolution. Our results provide insight into the mechanistic basis by which cells adapt to nutrient-limited environments and suggest that knowledge of the selective environment and the regulatory mechanisms important for growth and survival in that environment greatly increase the predictability of adaptive evolution.
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spelling pubmed-38869032014-01-10 Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments Hong, Jungeui Gresham, David PLoS Genet Research Article One of the central goals of evolutionary biology is to explain and predict the molecular basis of adaptive evolution. We studied the evolution of genetic networks in Saccharomyces cerevisiae (budding yeast) populations propagated for more than 200 generations in different nitrogen-limiting conditions. We find that rapid adaptive evolution in nitrogen-poor environments is dominated by the de novo generation and selection of copy number variants (CNVs), a large fraction of which contain genes encoding specific nitrogen transporters including PUT4, DUR3 and DAL4. The large fitness increases associated with these alleles limits the genetic heterogeneity of adapting populations even in environments with multiple nitrogen sources. Complete identification of acquired point mutations, in individual lineages and entire populations, identified heterogeneity at the level of genetic loci but common themes at the level of functional modules, including genes controlling phosphatidylinositol-3-phosphate metabolism and vacuole biogenesis. Adaptive strategies shared with other nutrient-limited environments point to selection of genetic variation in the TORC1 and Ras/PKA signaling pathways as a general mechanism underlying improved growth in nutrient-limited environments. Within a single population we observed the repeated independent selection of a multi-locus genotype, comprised of the functionally related genes GAT1, MEP2 and LST4. By studying the fitness of individual alleles, and their combination, as well as the evolutionary history of the evolving population, we find that the order in which these mutations are acquired is constrained by epistasis. The identification of repeatedly selected variation at functionally related loci that interact epistatically suggests that gene network polymorphisms (GNPs) may be a frequent outcome of adaptive evolution. Our results provide insight into the mechanistic basis by which cells adapt to nutrient-limited environments and suggest that knowledge of the selective environment and the regulatory mechanisms important for growth and survival in that environment greatly increase the predictability of adaptive evolution. Public Library of Science 2014-01-09 /pmc/articles/PMC3886903/ /pubmed/24415948 http://dx.doi.org/10.1371/journal.pgen.1004041 Text en © 2014 Hong, Gresham http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Hong, Jungeui
Gresham, David
Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments
title Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments
title_full Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments
title_fullStr Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments
title_full_unstemmed Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments
title_short Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments
title_sort molecular specificity, convergence and constraint shape adaptive evolution in nutrient-poor environments
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3886903/
https://www.ncbi.nlm.nih.gov/pubmed/24415948
http://dx.doi.org/10.1371/journal.pgen.1004041
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