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

Jungeui Hong, David Gresham

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish (US)
Article numbere1004041
JournalPLoS Genetics
Volume10
Issue number1
DOIs
StatePublished - Jan 2014

Fingerprint

Food
nutrient
nutrients
Nitrogen
gene
Gene Regulatory Networks
nitrogen
Population
loci
mutation
allele
fitness
Alleles
alleles
epistasis
Saccharomycetales
Genetic Loci
Genetic Heterogeneity
Molecular Evolution
evolutionary biology

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics
  • Cancer Research
  • Genetics(clinical)

Cite this

Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments. / Hong, Jungeui; Gresham, David.

In: PLoS Genetics, Vol. 10, No. 1, e1004041, 01.2014.

Research output: Contribution to journalArticle

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