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Altered access to beneficial mutations slows adaptation and biases fixed mutations in diploids

Abstract

Ploidy varies considerably in nature. However, our understanding of the impact of ploidy on adaptation is incomplete. Many microbial evolution experiments characterize adaptation in haploid organisms, but few focus on diploid organisms. Here, we perform a 4,000-generation evolution experiment using diploid strains of the yeast Saccharomyces cerevisiae. We show that the rate of adaptation and spectrum of beneficial mutations are influenced by ploidy. Haldane’s sieve effectively alters access to recessive beneficial mutations in diploid populations, leading to a slower rate of adaptation and a spectrum of beneficial mutations that is shifted towards dominant mutations. Genomic position also has an important role, as the prevalence of homozygous mutations is largely dependent on their proximity to a recombination hotspot. Our results demonstrate key aspects of diploid adaptation that have previously been understudied and provide support for several proposed theories.

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Fig. 1: Beneficial mutations in evolved haploids are recessive.
Fig. 2: The rate of adaptation of haploid and diploid populations.
Fig. 3: Genome-wide distribution of mutations in diploids evolved for 2,000 generations.
Fig. 4: Evolved alleles show varying degrees of dominance and ploidy dependence.
Fig. 5: Dynamics of adaptation and LOH.

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Acknowledgements

We thank M. Remillard (Princeton University) for providing strains; A. Nguyen and M. Desai (Harvard University) for providing the plasmid with mating-type-specific selectable markers; A. Selmecki, K. Fisher and R. Vignogna for their comments on the manuscript. This work was supported by the Charles E. Kaufman Foundation of The Pittsburgh Foundation.

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G.I.L. designed the project. D.A.M. performed the experiments. S.W.B. and D.A.M. performed the sequencing analysis pipeline. D.A.M. and G.I.L. analysed the data and wrote the manuscript.

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Correspondence to Gregory I. Lang.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–8, Supplementary Table 1

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Supplementary Table 2

Mutations detected in two clones each from 24 diploid populations

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Marad, D.A., Buskirk, S.W. & Lang, G.I. Altered access to beneficial mutations slows adaptation and biases fixed mutations in diploids. Nat Ecol Evol 2, 882–889 (2018). https://doi.org/10.1038/s41559-018-0503-9

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