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Multi-environment fitness landscapes of a tRNA gene

Abstract

A fitness landscape (FL) describes the genotype–fitness relationship in a given environment. To explain and predict evolution, it is imperative to measure the FL in multiple environments because the natural environment changes frequently. Using a high-throughput method that combines precise gene replacement with next-generation sequencing, we determine the in vivo FL of a yeast tRNA gene comprising over 23,000 genotypes in four environments. Although genotype-by-environment interaction is abundantly detected, its pattern is so simple that we can transform an existing FL to that in a new environment with fitness measures of only a few genotypes in the new environment. Under each environment, we observe prevalent, negatively biased epistasis between mutations. Epistasis-by-environment interaction is also prevalent, but trends in epistasis difference between environments are predictable. Our study thus reveals simple rules underlying seemingly complex FLs, opening the door to understanding and predicting FLs in general.

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Fig. 1: Determining the FL of the yeast \({{{\mathbf{tRNA}}}_{{{\mathbf{CCU}}}}^{{{\mathbf{Arg}}}}}\) gene in multiple environments.
Fig. 2: Yeast \({{{\mathbf{tRNA}}}_{{{\mathbf{CCU}}}}^{{{\mathbf{Arg}}}}}\) gene FL in each of the four environments examined.
Fig. 3: A piecewise linear model predicts the FL in one environment based on that in another.
Fig. 4: G × G × E interaction is prevalent.

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Acknowledgements

We thank W.-C. Ho, W. Qian, X. Wei and J.-R. Yang for valuable comments. This work was supported by an NSF DDIG (DEB-1501788) to J.Z. and C.L., and an NIH grant (R01GM103232) to J.Z.

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J.Z. conceived the project. C.L. and J.Z. designed the experiment. C.L. performed the experiment and analysed the data. C.L. and J.Z. wrote the paper.

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Correspondence to Jianzhi Zhang.

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Li, C., Zhang, J. Multi-environment fitness landscapes of a tRNA gene. Nat Ecol Evol 2, 1025–1032 (2018). https://doi.org/10.1038/s41559-018-0549-8

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