The Environment Affects Epistatic Interactions to Alter the Topology of an Empirical Fitness Landscape

The fitness effect of mutations can be influenced by their interactions with the environment, other mutations, or both. Previously, we constructed 32 ( = 25) genotypes that comprise all possible combinations of the first five beneficial mutations to fix in a laboratory-evolved population of Escheric...

Full description

Bibliographic Details
Main Authors: Flynn, Kenneth M., Cooper, Tim F., Moore, Francisco B-G., Cooper, Vaughn S.
Format: Online
Language:English
Published: Public Library of Science 2013
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3616912/
id pubmed-3616912
recordtype oai_dc
spelling pubmed-36169122013-04-16 The Environment Affects Epistatic Interactions to Alter the Topology of an Empirical Fitness Landscape Flynn, Kenneth M. Cooper, Tim F. Moore, Francisco B-G. Cooper, Vaughn S. Research Article The fitness effect of mutations can be influenced by their interactions with the environment, other mutations, or both. Previously, we constructed 32 ( = 25) genotypes that comprise all possible combinations of the first five beneficial mutations to fix in a laboratory-evolved population of Escherichia coli. We found that (i) all five mutations were beneficial for the background on which they occurred; (ii) interactions between mutations drove a diminishing returns type epistasis, whereby epistasis became increasingly antagonistic as the expected fitness of a genotype increased; and (iii) the adaptive landscape revealed by the mutation combinations was smooth, having a single global fitness peak. Here we examine how the environment influences epistasis by determining the interactions between the same mutations in two alternative environments, selected from among 1,920 screened environments, that produced the largest increase or decrease in fitness of the most derived genotype. Some general features of the interactions were consistent: mutations tended to remain beneficial and the overall pattern of epistasis was of diminishing returns. Other features depended on the environment; in particular, several mutations were deleterious when added to specific genotypes, indicating the presence of antagonistic interactions that were absent in the original selection environment. Antagonism was not caused by consistent pleiotropic effects of individual mutations but rather by changing interactions between mutations. Our results demonstrate that understanding adaptation in changing environments will require consideration of the combined effect of epistasis and pleiotropy across environments. Public Library of Science 2013-04-04 /pmc/articles/PMC3616912/ /pubmed/23593024 http://dx.doi.org/10.1371/journal.pgen.1003426 Text en © 2013 Flynn et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Flynn, Kenneth M.
Cooper, Tim F.
Moore, Francisco B-G.
Cooper, Vaughn S.
spellingShingle Flynn, Kenneth M.
Cooper, Tim F.
Moore, Francisco B-G.
Cooper, Vaughn S.
The Environment Affects Epistatic Interactions to Alter the Topology of an Empirical Fitness Landscape
author_facet Flynn, Kenneth M.
Cooper, Tim F.
Moore, Francisco B-G.
Cooper, Vaughn S.
author_sort Flynn, Kenneth M.
title The Environment Affects Epistatic Interactions to Alter the Topology of an Empirical Fitness Landscape
title_short The Environment Affects Epistatic Interactions to Alter the Topology of an Empirical Fitness Landscape
title_full The Environment Affects Epistatic Interactions to Alter the Topology of an Empirical Fitness Landscape
title_fullStr The Environment Affects Epistatic Interactions to Alter the Topology of an Empirical Fitness Landscape
title_full_unstemmed The Environment Affects Epistatic Interactions to Alter the Topology of an Empirical Fitness Landscape
title_sort environment affects epistatic interactions to alter the topology of an empirical fitness landscape
description The fitness effect of mutations can be influenced by their interactions with the environment, other mutations, or both. Previously, we constructed 32 ( = 25) genotypes that comprise all possible combinations of the first five beneficial mutations to fix in a laboratory-evolved population of Escherichia coli. We found that (i) all five mutations were beneficial for the background on which they occurred; (ii) interactions between mutations drove a diminishing returns type epistasis, whereby epistasis became increasingly antagonistic as the expected fitness of a genotype increased; and (iii) the adaptive landscape revealed by the mutation combinations was smooth, having a single global fitness peak. Here we examine how the environment influences epistasis by determining the interactions between the same mutations in two alternative environments, selected from among 1,920 screened environments, that produced the largest increase or decrease in fitness of the most derived genotype. Some general features of the interactions were consistent: mutations tended to remain beneficial and the overall pattern of epistasis was of diminishing returns. Other features depended on the environment; in particular, several mutations were deleterious when added to specific genotypes, indicating the presence of antagonistic interactions that were absent in the original selection environment. Antagonism was not caused by consistent pleiotropic effects of individual mutations but rather by changing interactions between mutations. Our results demonstrate that understanding adaptation in changing environments will require consideration of the combined effect of epistasis and pleiotropy across environments.
publisher Public Library of Science
publishDate 2013
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3616912/
_version_ 1611967690333749248