Chromosomal duplication is a transient evolutionary solution to stress

Avihu H. Yona, Yair S. Manor, Rebecca H. Herbst, Gal H. Romano, Amir Mitchell, Martin Kupiec, Yitzhak Pilpel*, Orna Dahan

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

247 Scopus citations

Abstract

Aneuploidy, an abnormal number of chromosomes, is a widespread phenomenon found in unicellulars such as yeast, as well as in plants and in mammalians, especially in cancer. Aneuploidy is a genomescale aberration that imposes a severe burden on the cell, yet under stressful conditions specific aneuploidies confer a selective advantage. This dual nature of aneuploidy raises the question of whether it can serve as a stable and sustainable evolutionary adaptation. To clarify this, we conducted a set of laboratory evolution experiments in yeast and followed the long-term dynamics of aneuploidy under diverse conditions. Herewe showthat chromosomal duplications are first acquired as a crude solution to stress, yet only as transient solutions that are eliminated and replaced by more efficient solutions obtained at the individual gene level. These transient dynamics of aneuploidy were repeatedly observed in our laboratory evolution experiments; chromosomal duplications gained under stress were eliminated not only when the stress was relieved, but even if it persisted. Furthermore, when stress was applied gradually rather than abruptly, alternative solutions appear to have emerged, but not aneuploidy. Our findings indicate that chromosomalduplicationis afirst evolutionary line of defense, that retains survivability under strong and abrupt selective pressures, yet it merely serves as a "quick fix," whereas more refined and sustainable solutions take over. Thus, in the perspective of genome evolution trajectory, aneuploidy is a useful yet short-lived intermediate that facilitates further adaptation.

Original languageAmerican English
Pages (from-to)21010-21015
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number51
DOIs
StatePublished - 18 Dec 2012
Externally publishedYes

Keywords

  • Environmental stress
  • Evolutionary dynamics
  • Heat tolerance
  • pH tolerance

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