Polyploidy can drive rapid adaptation in yeast

• Published in: Nature (London) 2015-03, Vol.519 (7543), p.349-352
• Main Authors: Selmecki, Anna M., Maruvka, Yosef E., Richmond, Phillip A., Guillet, Marie, Shoresh, Noam, Sorenson, Amber L., De, Subhajyoti, Kishony, Roy, Michor, Franziska, Dowell, Robin, Pellman, David
• Format: Article
• Language: English
• Subjects: 45; 45/23; 45/61; 45/77; 631/181/2475; 631/208/182; Adaptation (Biology); Adaptation, Physiological - genetics; Aneuploidy; Biological Evolution; Biological research; Biology, Experimental; Chromosomes; Chromosomes, Fungal - genetics; Clone Cells - cytology; Clone Cells - metabolism; Cloning; Diploidy; Ecological adaptation; Genetic diversity; Genetic Fitness - genetics; Genomes; Haploidy; Humanities and Social Sciences; letter; Mathematical models; multidisciplinary; Mutation; Mutation Rate; Point Mutation - genetics; Polyploidy; Saccharomyces cerevisiae - cytology; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae - metabolism; Saccharomyces cerevisiae - physiology; Science; Time Factors; Yeast; Yeast fungi; Yeasts
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature14187

In vitro evolution experiments on haploid, diploid, and tetraploid yeast strains show that adaptation is faster in tetraploids, providing direct quantitative evidence that in some environments polyploidy can accelerate evolutionary adaptation. Evolution accelerated by polyploidy Polyploidization — where the chromosome number is more than double the normal or haploid number — is common in fungi, plants and animals, but its influence on evolution is unclear. This study describes bench-top evolution experiments on haploid, diploid and tetraploid asexual yeast strains showing that polyploidy can accelerate adaptation to growth on a poor carbon source, with tetraploids adapting the fastest. This go-faster evolution is driven by the acquisition of more and more beneficial mutations. Polyploidy can be unstable however, but aneuploidy, concerted chromosome loss and point mutations all provide substantial gains in fitness in this context. Polyploidy is observed across the tree of life, yet its influence on evolution remains incompletely understood 1 , 2 , 3 , 4 . 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 2 , 5 , 6 , 7 . For example, in diverse cell types and organisms, immediately after a whole-genome duplication, newly formed polyploids missegregate chromosomes and undergo genetic instability 8 , 9 , 10 , 11 , 12 , 13 . The instability following whole-genome duplications is thought to provide adaptive mutations in microorganisms 13 , 14 and can promote tumorigenesis in mammalian cells 11 , 15 . Polyploidy may also affect adaptation independently of beneficial mutations through ploidy-specific changes in cell physiology 16 . 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