Shared Molecular Targets Confer Resistance over Short and Long Evolutionary Timescales

Mol Biol Evol. 2019 Apr 1;36(4):691-708. doi: 10.1093/molbev/msz006.

Abstract

Pre-existing and de novo genetic variants can both drive adaptation to environmental changes, but their relative contributions and interplay remain poorly understood. Here we investigated the evolutionary dynamics in drug-treated yeast populations with different levels of pre-existing variation by experimental evolution coupled with time-resolved sequencing and phenotyping. We found a doubling of pre-existing variation alone boosts the adaptation by 64.1% and 51.5% in hydroxyurea and rapamycin, respectively. The causative pre-existing and de novo variants were selected on shared targets: RNR4 in hydroxyurea and TOR1, TOR2 in rapamycin. Interestingly, the pre-existing and de novo TOR variants map to different functional domains and act via distinct mechanisms. The pre-existing TOR variants from two domesticated strains exhibited opposite rapamycin resistance effects, reflecting lineage-specific functional divergence. This study provides a dynamic view on how pre-existing and de novo variants interactively drive adaptation and deepens our understanding of clonally evolving populations.

Keywords: adaptation; budding yeast; de novo mutation; drug resistance; pre-existing genetic variation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biological Evolution*
  • Cell Cycle Proteins / genetics
  • Drug Resistance, Fungal / genetics*
  • Hydroxyurea
  • Mutation
  • Phosphatidylinositol 3-Kinases / genetics
  • Quantitative Trait Loci
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae Proteins / genetics
  • Selection, Genetic
  • Sirolimus

Substances

  • Cell Cycle Proteins
  • Saccharomyces cerevisiae Proteins
  • TOR1 protein, S cerevisiae
  • TOR2 protein, S cerevisiae
  • Sirolimus
  • Hydroxyurea