Aneuploidy Can Be an Evolutionary Diversion on the Path to Adaptation

Ilia Kohanovski, Martin Pontz, Pétra Vande Zande, Anna Selmecki, Orna Dahan, Yitzhak Pilpel, Avihu H. Yona, Yoav Ram*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Aneuploidy is common in eukaryotes, often leading to decreased fitness. However, evidence from fungi and human tumur cells suggests that specific aneuploidies can be beneficial under stressful conditions and facilitate adaptation. In a previous evolutionary experiment with yeast, populations evolving under heat stress became aneuploid, only to later revert to euploidy after beneficial mutations accumulated. It was therefore suggested that aneuploidy is a “stepping stone” on the path to adaptation. Here, we test this hypothesis. We use Bayesian inference to fit an evolutionary model with both aneuploidy and mutation to the experimental results. We then predict the genotype frequency dynamics during the experiment, demonstrating that most of the evolved euploid population likely did not descend from aneuploid cells, but rather from the euploid wild-type population. Our model shows how the beneficial mutation supply—the product of population size and beneficial mutation rate–determines the evolutionary dynamics: with low supply, much of the evolved population descends from aneuploid cells; but with high supply, beneficial mutations are generated fast enough to outcompete aneuploidy due to its inherent fitness cost. Our results suggest that despite its potential fitness benefits under stress, aneuploidy can be an evolutionary “diversion” rather than a “stepping stone”: it can delay, rather than facilitate, the adaptation of the population, and cells that become aneuploid may leave less descendants compared to cells that remain diploid.

Original languageEnglish
Article numbermsae052
JournalMolecular Biology and Evolution
Volume41
Issue number3
DOIs
StatePublished - 1 Mar 2024

Funding

FundersFunder number
Lilach Hadany
Jane Coffin Childs Memorial Fund for Medical Research
Investigators in the Pathogenesis of Infectious Diseases
Minerva Foundation
Israel Science FoundationY.R. 552/19
Israel Science Foundation
United States-Israel Binational Science Foundation2021276
United States-Israel Binational Science Foundation
National Institutes of HealthAI143689
National Institutes of Health
Burroughs Wellcome Fund1020388
Burroughs Wellcome Fund

    Keywords

    • adaptive evolution
    • evolutionary model
    • whole-chromosome duplication

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