Antagonistic pleiotropy conceals molecular adaptations in changing environments

Abstract

The importance of positive selection in molecular evolution is debated. Evolution experiments under invariant laboratory conditions typically show a higher rate of nonsynonymous nucleotide changes than the rate of synonymous changes, demonstrating prevalent molecular adaptations. Natural evolution inferred from genomic comparisons, however, almost always exhibits the opposite pattern even among closely related conspecifics, which is indicative of a paucity of positive selection. Here we hypothesize that this apparent contradiction is at least in part attributable to ubiquitous and frequent environmental changes in nature, causing nonsynonymous mutations that are beneficial at one time to become deleterious soon after because of antagonistic pleiotropy and hindering their fixations relative to synonymous mutations despite continued population adaptations. To test this hypothesis, we performed yeast evolution experiments in changing and corresponding constant environments, followed by genome sequencing of the evolving populations. We observed a lower nonsynonymous to synonymous rate ratio in antagonistic changing environments than in the corresponding constant environments, and the population dynamics of mutations supports our hypothesis. These findings and the accompanying population genetic simulations suggest that molecular adaptation is consistently underestimated in nature due to the antagonistic fitness effects of mutations in changing environments.

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Fig. 1: Experimental evolution of yeast in constant and changing environments.
Fig. 2: The rate of molecular evolution in constant and changing environments.
Fig. 3: Population dynamics of individual nonsynonymous mutant alleles in the antagonistic changing or constant environments.
Fig. 4: Computer simulations explain the observations of the experimental evolutions in the antagonistic changing or constant environments.

Data availability

The raw sequencing data are available from NCBI BioProject (PRJNA597653).

Code availability

The computer code can be downloaded from https://github.com/PiaopiaoChen/simulation.git.

Change history

  • 19 February 2020

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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Acknowledgements

We thank W.-C. Ho, X. Wei and members of the Zhang laboratory for comments. This work was supported by a research grant (2R01GM103232) from the US National Institutes of Health to J.Z.

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J.Z. conceived the project, secured funding and supervised the study; P.C. performed the research and analysed the data; P.C. and J.Z. designed the study and wrote the manuscript.

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Correspondence to Jianzhi Zhang.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–10 and Supplementary Table 1.

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Supplementary Data 1

SNVs in the end populations.

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Chen, P., Zhang, J. Antagonistic pleiotropy conceals molecular adaptations in changing environments. Nat Ecol Evol 4, 461–469 (2020). https://doi.org/10.1038/s41559-020-1107-8

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