Cited by 376Evolution and Genetic DynamicsChromosomal and Genetic VariationsFungal and yeast genetics research

Chromosomal duplication is a transient evolutionary solution to stress

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Yona, Avihu H., Manor, Yair S., Herbst, Rebecca H., Romano, Gal H., Mitchell, Amir, Kupiec, Martin, Pilpel, Yitzhak, Dahan, Orna·2012·Proceedings of the National Academy of Sciences

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 genome-scale 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. Here we show that 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 chromosomal duplication is a first 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.

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Crossref · 10.1073/pnas.1211150109

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  • Aneuploidies, while largely transient, may be an important intermediate giving rise to more stable adaptive genotypes in some cases.

    “In this context, it appears that aneuploidies (Figure 7A, green), while largely transient, may be an important intermediate giving rise to more stable adaptive genotypes in some cases”

    From The evolution of drug resistance in clinical isolates of Candida albicans. (2015) · cites this paper as Yona et al., 2012

  • C. albicans, like S. cerevisiae, generates large scale genetic variation as a means of adaptation.

    “Thus, C. albicans like S. cerevisiae (Gresham et al., 2008; Pavelka et al., 2010; Yona et al., 2012; Chang et al., 2013) generates large scale genetic variation as a means of adaptation.”

    From The evolution of drug resistance in clinical isolates of Candida albicans. (2015) · cites this paper as Yona et al., 2012

  • A transient role for aneuploidy is consistent with recent findings from in vitro evolution studies in S. cerevisiae in which a transient aneuploidy was responsible for fitness at elevated temperature, but was eventually replaced by a more stable mutation.

    “A transient role for aneuploidy is consistent with recent findings from in vitro evolution studies in S. cerevisiae (Yona et al., 2012) in which a transient aneuploidy was responsible for fitness at elevated temperature, but was eventually replaced by a more stable mutation.”

    From The evolution of drug resistance in clinical isolates of Candida albicans. (2015) · cites this paper as Yona et al., 2012

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Authors
Yona, A. H., Manor, Y. S., Herbst, R. H., Romano, G. H., Mitchell, A., Kupiec, M., Pilpel, Y., & Dahan, O.
Affiliations
  • Weizmann Institute of Science (IL)
  • Tel Aviv University (IL)
Venue
Proceedings of the National Academy of Sciences
Published
2012-11-29
Volume
109
Issue
51
Pages
21010-21015
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W1994213227
Cited by
376
References
31
Citations by year
2026: 10 · 2025: 32 · 2024: 32 · 2023: 25 · 2022: 27 · 2021: 32 · 2020: 29 · 2019: 34 · 2018: 32 · 2017: 32 · 2016: 17 · 2015: 32 · 2014: 22 · 2013: 18
FWCI
13.88
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Keywords
chromosomal duplication, aneuploidy, stress adaptation, experimental evolution, Saccharomyces cerevisiae, genome evolution, evolutionary intermediates
MeSH terms
Aneuploidy, Chromosome Mapping, Chromosomes, Environment, Biological Evolution, Fungal Proteins, Genes, Fungal, Haploidy, Hot Temperature, Heat-Shock Proteins, Hydrogen-Ion Concentration, Models, Genetic, Neoplasms, Phenotype, Saccharomyces cerevisiae, Temperature, Evolution, Molecular, Oligonucleotide Array Sequence Analysis, Chromosome Duplication

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