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

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 hu...

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Main Authors: Grant Kinsler, Kerry Geiler-Samerotte, Dmitri A Petrov
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/61271
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spelling doaj-14e9f3caaa7e4aa3a620e28a7076eb2f2021-05-05T21:47:05ZengeLife Sciences Publications LtdeLife2050-084X2020-12-01910.7554/eLife.61271Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptationGrant Kinsler0https://orcid.org/0000-0001-8308-4665Kerry Geiler-Samerotte1https://orcid.org/0000-0003-4666-2192Dmitri A Petrov2https://orcid.org/0000-0002-3664-9130Department of Biology, Stanford University, Stanford, United StatesDepartment of Biology, Stanford University, Stanford, United States; Center for Mechanisms of Evolution, School of Life Sciences, Arizona State University, Tempe, United StatesDepartment of Biology, Stanford University, Stanford, United StatesBuilding 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.https://elifesciences.org/articles/61271adaptationpleiotropymodularity
collection DOAJ
language English
format Article
sources DOAJ
author Grant Kinsler
Kerry Geiler-Samerotte
Dmitri A Petrov
spellingShingle Grant Kinsler
Kerry Geiler-Samerotte
Dmitri A Petrov
Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation
eLife
adaptation
pleiotropy
modularity
author_facet Grant Kinsler
Kerry Geiler-Samerotte
Dmitri A Petrov
author_sort Grant Kinsler
title Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation
title_short Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation
title_full Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation
title_fullStr Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation
title_full_unstemmed Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation
title_sort fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-12-01
description 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.
topic adaptation
pleiotropy
modularity
url https://elifesciences.org/articles/61271
work_keys_str_mv AT grantkinsler fitnessvariationacrosssubtleenvironmentalperturbationsrevealslocalmodularityandglobalpleiotropyofadaptation
AT kerrygeilersamerotte fitnessvariationacrosssubtleenvironmentalperturbationsrevealslocalmodularityandglobalpleiotropyofadaptation
AT dmitriapetrov fitnessvariationacrosssubtleenvironmentalperturbationsrevealslocalmodularityandglobalpleiotropyofadaptation
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