Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation

Abstract
Data availability
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Abstract

Building a genotype-phenotype-fitness map of adaptation is a central goal in evolutionary biology. It is difficult even when adaptive mutations are known because it is hard to enumerate which phenotypes make these mutations adaptive. We address this problem by first quantifying how the fitness of hundreds of adaptive yeast mutants responds to subtle environmental shifts. We then model the number of phenotypes these mutations collectively influence by decomposing these patterns of fitness variation. We find that a small number of inferred phenotypes can predict fitness of the adaptive mutations near their original glucose-limited evolution condition. Importantly, inferred phenotypes that matter little to fitness at or near the evolution condition can matter strongly in distant environments. This suggests that adaptive mutations are locally modular—affecting a small number of phenotypes that matter to fitness in the environment where they evolved—yet globally pleiotropic—affecting additional phenotypes that may reduce or improve fitness in new environments.

Data availability

All sequencing data has been deposited to SRA under NIH BioProject number PRJNA641718.

The following data sets were generated

(2020) A genotype-phenotype-fitness map reveals local modularity and global pleiotropy of adaptation
NCBI Bioproject, PRJNA641718.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA641718/

The following previously published data sets were used

(2016) A comprehensive genotype-fitness map of adaptation-driving mutations in yeast
NCBI BioProject, PRJNA310010.

https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA310010
(2018) Understanding S. Cerevisiae adaptation and trade-offs under batch culture condition
NCBI BioProject, PRJNA388215.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA388215/

Article and author information

Author details

Grant Kinsler

Department of Biology, Stanford University, Stanford, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8308-4665
Kerry Geiler-Samerotte

Biodesign Institute, Arizona State University, Tempe, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4666-2192
Dmitri A Petrov

Department of Biology, Stanford University, Stanford, United States

For correspondence
dpetrov@stanford.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3664-9130

Funding

National Institutes of Health (R35GM118165)

Dmitri A Petrov

National Institutes of Health (R35GM133674)

Kerry Geiler-Samerotte

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.