Chance and necessity in the pleiotropic consequences of adaptation for budding yeast

Abstract

Mutations that a population accumulates during evolution in one ‘home’ environment may cause fitness gains or losses in other environments. Such pleiotropic fitness effects determine the evolutionary fate of the population in variable environments and can lead to ecological specialization. It is unclear how the pleiotropic outcomes of evolution are shaped by the intrinsic randomness of the evolutionary process and by the deterministic variation in selection pressures across environments. Here, to address this question, we evolved 20 replicate populations of the yeast Saccharomyces cerevisiae in 11 laboratory environments and measured their fitness across multiple conditions. We found that evolution led to diverse pleiotropic fitness gains and losses, driven by multiple types of mutations. Approximately 60% of this variation is explained by the home environment of a clone and the most common parallel genetic changes, whereas about 40% is attributed to the stochastic accumulation of mutations whose pleiotropic effects are unpredictable. Although populations are typically specialized to their home environment, generalists also evolved in almost all of the conditions. Our results suggest that the mutations that accumulate during evolution incur a variety of pleiotropic costs and benefits with different probabilities. Thus, whether a population evolves towards a specialist or a generalist phenotype is heavily influenced by chance.

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Fig. 1: Fitness gains and losses in diagnostic conditions after evolution in each condition.
Fig. 2: Environmental and stochastic determinants of pleiotropic profiles.
Fig. 3: The V phenotype is caused by the loss of yeast killer virus.
Fig. 4: Mutations across evolution conditions and genetic determinants of pleiotropy.
Fig. 5: Specialization across salt, pH and temperature panels of environments.

Data availability

The data used in Figs. 1, 2 and 5 are provided in Supplementary Table 1. The data used in Fig. 3 are provided in Supplementary Table 2. The data used in Fig. 4 are provided in Supplementary Tables 1 and 3. The sequences reported in this paper have been deposited in the BioProject database (accession number, PRJNA554163). All of the strains are available from the corresponding authors on request.

Code availability

The code used for analysis and figure generation is available at https://github.com/erjerison/pleiotropy.

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Acknowledgements

We thank members of the Desai and Kryazhimskiy laboratories for experimental assistance and comments on the manuscript. M.M.D. acknowledges support from the Simons Foundation (grant no. 376196), NSF (grant no. DEB-1655960) and NIH (grant no. GM104239). S.K. acknowledges support from the BWF Career Award at Scientific Interface (grant no. 1010719.01), the Alfred P. Sloan Foundation (grant no. FG-2017-9227) and the Hellman Foundation.

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E.R.J., M.M.D. and S.K. designed the research. E.R.J., S.K. and A.N.N.B. performed experiments and analysis. E.R.J., M.M.D. and S.K. wrote the paper.

Corresponding authors

Correspondence to Michael M. Desai or Sergey Kryazhimskiy.

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Extended data

Extended Data Fig. 1 Median fitness gains and losses, restricted to V+ clones.

Median fitness gains and losses among groups of clones from the same home environment, excluding V clones. Notations as in Fig. 1.

Extended Data Fig. 2 Frequency-dependence of competition between V+ and V.

Fitness of a V clone relative to the ancestor at Low Temp, initiated at different initial frequencies. The frequency dependence of the relative fitness suggests that the fitness defect might be caused by a direct interaction between the competitors. Error bars show ± 1 s.e.m.

Extended Data Fig. 3 Variance in fitness across environmental panels.

As in Fig. 5a–c, but variance in fitness across groups of clones rather than means. Error bars represent ± 1 standard error of the variance.

Extended Data Fig. 4 Correlations between clone fitness in different salt conditions.

Each panel below the diagonal shows clone fitness in a particular pair of environments. (Error bars: ± 1 s.e.m. on clone fitness.) The diagonal shows the correlation between technical replicates in the fitness assay in each condition. Panels above the diagonal are colored by and display the Pearson correlation coefficient between clone fitness in the corresponding pair of environments.

Extended Data Fig. 5 Correlations between clone fitness in different pH conditions.

Each panel below the diagonal shows clone fitness in a particular pair of environments. (Error bars: ± 1 s.e.m. on clone fitness.) The diagonal shows the correlation between technical replicates in the fitness assay in each condition. Panels above the diagonal are colored by and display the Pearson correlation coefficient between clone fitness in the corresponding pair of environments.

Extended Data Fig. 6 Correlations between clone fitness in different temperature conditions.

Each panel below the diagonal shows clone fitness in a particular pair of environments. (Error bars: ± 1 s.e.m. on clone fitness.) The diagonal shows the correlation between technical replicates in the fitness assay in each condition. Panels above the diagonal are colored by and display the Pearson correlation coefficient between clone fitness in the corresponding pair of environments.

Supplementary information

Supplementary Information

Supplementary Figs. 1–5.

Reporting Summary

Supplementary Table 1

Fitness measurement data.

Supplementary Table 2

Fitness measurement data in low temperature with respect to the cured reference.

Supplementary Table 3

Identified mutations.

Supplementary Table 4

Primers used in this study.

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Jerison, E.R., Nguyen Ba, A.N., Desai, M.M. et al. Chance and necessity in the pleiotropic consequences of adaptation for budding yeast. Nat Ecol Evol 4, 601–611 (2020). https://doi.org/10.1038/s41559-020-1128-3

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