Sex alters molecular evolution in diploid experimental populations of S. cerevisiae

Abstract

Sex is common among eukaryotes, but entails considerable costs. The selective conditions that drive the evolutionary maintenance of sexual reproduction remain an open question. One long-standing explanation is that sex and recombination facilitate adaptation to fluctuating environmental conditions, although the genetic mechanisms that underlie such a benefit have not been empirically observed. In this study, we compare the dynamics and fitness effects of mutations in sexual and asexual diploid populations of the yeast Saccharomyces cerevisiae during adaptation to a fluctuating environment. While we find no detectable difference in the rate of adaptation between sexual and asexual populations, only the former evolve high fitness mutations in parallel, a genetic signature of adaptation. Using genetic reconstructions and fitness assays, we demonstrate that evolved, overdominant mutations can be beneficial in asexual populations, but maintained at lower frequencies in sexual populations due to segregation load. Overall these data show that sex alters the molecular basis of adaptation in diploids, and confers both costs and benefits.

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Fig. 1: Experimental populations of diploids were propagated in a fluctuating environment.
Fig. 2: Total fitness difference (selection coefficient per cycle) for evolved asexual and sexual populations compared to reference.
Fig. 3: The dynamics of mutations in asexual and sexual populations over ~1,440 generations of evolution.
Fig. 4: The fitness effects of individual mutations from sexual and asexual populations.

Data availability

Raw sequencing reads used to generate the data in Figs. 2–4 have been deposited in GenBank under the Bioproject ID: PRJNA530331. Custom scripts used for the parallel evolution analysis are available at GitHub (https://github.com/woodlaur189/Parall-expect).

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Acknowledgements

J.-Y.L. was supported by Academia Sinica of Taiwan (grant nos. AS-IA-105-L01 and AS-TP-107-ML06) and the Taiwan Ministry of Science and Technology (grant no. MOST107-2321-B-001-010). M.J.M. was supported by ARC Discovery (grant no. DP180102161) and an ARC Future Fellowship (no. FT170100441).

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J.-Y.L., S.-L.C. and M.J.M. conceived and designed the study. S.-L.C., J.-C.C. and M.J.M. carried out experiments. J.-Y.L., S.-L.C., L.C.W. and M.J.M. analysed the data.

Corresponding author

Correspondence to Michael J. McDonald.

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The authors declare no competing interests.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–6, rationalization of invasion assays used to compare heterozygotes and homozygotes and Tables 1–3.

Reporting Summary

Supplementary Data 1

DNA sequence data for all genetic variants called in this project.

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Leu, J., Chang, S., Chao, J. et al. Sex alters molecular evolution in diploid experimental populations of S. cerevisiae. Nat Ecol Evol 4, 453–460 (2020). https://doi.org/10.1038/s41559-020-1101-1

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