Polyploidy can drive rapid adaptation in yeast

Anna M. Selmecki, Yosef E. Maruvka, Phillip A. Richmond, Marie Guillet, Noam Shoresh, Amber L. Sorenson, Subhajyoti De, Roy Kishony, Franziska Michor, Robin Dowell, David Pellman

Research output: Contribution to journalArticlepeer-review

198 Scopus citations

Abstract

Polyploidy is observed across the tree of life, yet its influence on evolution remains incompletely understood. Polyploidy, usually whole-genome duplication, is proposed to alter the rate of evolutionary adaptation. This could occur through complex effects on the frequency or fitness of beneficial mutations. For example, in diverse cell types and organisms, immediately after a whole-genome duplication, newly formed polyploids missegregate chromosomes and undergo genetic instability. The instability following whole-genome duplications is thought to provide adaptive mutations in microorganisms and can promote tumorigenesis in mammalian cells. Polyploidy may also affect adaptation independently of beneficial mutations through ploidy-specific changes in cell physiology. Here we perform in vitro evolution experiments to test directly whether polyploidy can accelerate evolutionary adaptation. Compared with haploids and diploids, tetraploids undergo significantly faster adaptation. Mathematical modelling suggests that rapid adaptation of tetraploids is driven by higher rates of beneficial mutations with stronger fitness effects, which is supported by whole-genome sequencing and phenotypic analyses of evolved clones. Chromosome aneuploidy, concerted chromosome loss, and point mutations all provide large fitness gains. We identify several mutations whose beneficial effects are manifest specifically in the tetraploid strains. Together, these results provide direct quantitative evidence that in some environments polyploidy can accelerate evolutionary adaptation.

Original languageEnglish (US)
Pages (from-to)349-351
Number of pages3
JournalNature
Volume519
Issue number7543
DOIs
StatePublished - Mar 19 2015
Externally publishedYes

Bibliographical note

Funding Information:
AcknowledgementsThisworkwas supported bythe Howard HughesMedicalInstitute, the National Institutes of Health (R37 GM61345), the G. Harold & Leila Y. Mathers Charitable Foundation, the Dana-Farber Cancer Institute Physical Sciences-Oncology Center (U54CA143798), the Boettcher Foundation’s Webb-Waring Biomedical Research Program, the National Science Foundation (NSF 1350915), the National Institutes of Health (R01 GM081617), and an American Cancer Society Postdoctoral Fellowship.

Publisher Copyright:
© 2015 Macmillan Publishers Limited.

Copyright:
Copyright 2016 Elsevier B.V., All rights reserved.

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