Polyploidy can drive rapid adaptation in yeast.
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.
1] Department of Pediatric Oncology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, Massachusetts 02215, USA [2] Department of Cell Biology, Harvard Medical School, 25 Shattuck Street, Boston, Massachusetts 02215, USA [3] Howard Hughes Medical Institute, 4000 Jones Bridge Road, Chevy Chase, Maryland 20815, USA.
Anna M
AM
Selmecki
1] Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue Boston, Massachusetts 02215, USA [2] Department of Biostatistics, Harvard School of Public Health, 158 Longwood Avenue, Boston, Massachusetts 02215, USA.
Yosef E
YE
Maruvka
1] BioFrontiers Institute, University of Colorado at Boulder, 3415 Colorado Avenue, Boulder, Colorado 80303, USA [2] Department of Molecular, Cellular and Developmental Biology, University of Colorado at Boulder, 347 UCB, Boulder, Colorado 80309, USA.
Phillip A
PA
Richmond
1] Department of Pediatric Oncology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, Massachusetts 02215, USA [2] Department of Cell Biology, Harvard Medical School, 25 Shattuck Street, Boston, Massachusetts 02215, USA [3] Howard Hughes Medical Institute, 4000 Jones Bridge Road, Chevy Chase, Maryland 20815, USA.
Marie
M
Guillet
Broad Institute, 415 Main Street, Cambridge, Massachusetts 02142, USA.
Noam
N
Shoresh
1] BioFrontiers Institute, University of Colorado at Boulder, 3415 Colorado Avenue, Boulder, Colorado 80303, USA [2] Department of Molecular, Cellular and Developmental Biology, University of Colorado at Boulder, 347 UCB, Boulder, Colorado 80309, USA.
Amber L
AL
Sorenson
1] Department of Medicine, University of Colorado School of Medicine, 13001 East 17th Place, Aurora, Colorado 80045, USA [2] Department of Biostatistics and Informatics, Colorado School of Public Health, 13001 East 17th Place, Aurora, Colorado 80045, USA [3] Molecular Oncology Program, University of Colorado Cancer Center, 13001 East 17th Place, Aurora, Colorado 80045, USA.
Subhajyoti
S
De
1] Department of Systems Biology, Harvard Medical School, 200 Longwood Ave, Boston, Massachusetts 02115, USA [2] Department of Biology, Technion - Israel Institute of Technology, Haifa, 32000, Israel.
Roy
R
Kishony
1] Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue Boston, Massachusetts 02215, USA [2] Department of Biostatistics, Harvard School of Public Health, 158 Longwood Avenue, Boston, Massachusetts 02215, USA.
Franziska
F
Michor
1] BioFrontiers Institute, University of Colorado at Boulder, 3415 Colorado Avenue, Boulder, Colorado 80303, USA [2] Department of Molecular, Cellular and Developmental Biology, University of Colorado at Boulder, 347 UCB, Boulder, Colorado 80309, USA.
Robin
R
Dowell
1] Department of Pediatric Oncology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, Massachusetts 02215, USA [2] Department of Cell Biology, Harvard Medical School, 25 Shattuck Street, Boston, Massachusetts 02215, USA [3] Howard Hughes Medical Institute, 4000 Jones Bridge Road, Chevy Chase, Maryland 20815, USA [4] Department of Pediatric Hematology/Oncology, Children's Hospital, 300 Longwood Avenue, Boston, Massachusetts 02115, USA.
David
D
Pellman
D000222:Adaptation, Physiological / Q000235:genetics*; D000782:Aneuploidy; D005075:Biological Evolution; D015825:Chromosomes, Fungal / Q000235:genetics; D002999:Clone Cells / Q000166:cytology / Q000378:metabolism; D004171:Diploidy; D056084:Genetic Fitness / Q000235:genetics; D006238:Haploidy; D059645:Mutation Rate; D017354:Point Mutation / Q000235:genetics; D011123:Polyploidy; D012441:Saccharomyces cerevisiae / Q000166:cytology / Q000235:genetics* / Q000378:metabolism / Q000502:physiology*; D013997:Time Factors