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On the incongruence of genotype-phenotype and fitness landscapes

The mapping from genotype to phenotype to fitness typically involves multiple nonlinearities that can transform the effects of mutations. For example, mutations may contribute additively to a phenotype, but their effects on fitness may combine non-additively because selection favors a low or interme...

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Autores principales: Srivastava, Malvika, Payne, Joshua L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9521842/
https://www.ncbi.nlm.nih.gov/pubmed/36121840
http://dx.doi.org/10.1371/journal.pcbi.1010524
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author Srivastava, Malvika
Payne, Joshua L.
author_facet Srivastava, Malvika
Payne, Joshua L.
author_sort Srivastava, Malvika
collection PubMed
description The mapping from genotype to phenotype to fitness typically involves multiple nonlinearities that can transform the effects of mutations. For example, mutations may contribute additively to a phenotype, but their effects on fitness may combine non-additively because selection favors a low or intermediate value of that phenotype. This can cause incongruence between the topographical properties of a fitness landscape and its underlying genotype-phenotype landscape. Yet, genotype-phenotype landscapes are often used as a proxy for fitness landscapes to study the dynamics and predictability of evolution. Here, we use theoretical models and empirical data on transcription factor-DNA interactions to systematically study the incongruence of genotype-phenotype and fitness landscapes when selection favors a low or intermediate phenotypic value. Using the theoretical models, we prove a number of fundamental results. For example, selection for low or intermediate phenotypic values does not change simple sign epistasis into reciprocal sign epistasis, implying that genotype-phenotype landscapes with only simple sign epistasis motifs will always give rise to single-peaked fitness landscapes under such selection. More broadly, we show that such selection tends to create fitness landscapes that are more rugged than the underlying genotype-phenotype landscape, but this increased ruggedness typically does not frustrate adaptive evolution because the local adaptive peaks in the fitness landscape tend to be nearly as tall as the global peak. Many of these results carry forward to the empirical genotype-phenotype landscapes, which may help to explain why low- and intermediate-affinity transcription factor-DNA interactions are so prevalent in eukaryotic gene regulation.
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spelling pubmed-95218422022-09-30 On the incongruence of genotype-phenotype and fitness landscapes Srivastava, Malvika Payne, Joshua L. PLoS Comput Biol Research Article The mapping from genotype to phenotype to fitness typically involves multiple nonlinearities that can transform the effects of mutations. For example, mutations may contribute additively to a phenotype, but their effects on fitness may combine non-additively because selection favors a low or intermediate value of that phenotype. This can cause incongruence between the topographical properties of a fitness landscape and its underlying genotype-phenotype landscape. Yet, genotype-phenotype landscapes are often used as a proxy for fitness landscapes to study the dynamics and predictability of evolution. Here, we use theoretical models and empirical data on transcription factor-DNA interactions to systematically study the incongruence of genotype-phenotype and fitness landscapes when selection favors a low or intermediate phenotypic value. Using the theoretical models, we prove a number of fundamental results. For example, selection for low or intermediate phenotypic values does not change simple sign epistasis into reciprocal sign epistasis, implying that genotype-phenotype landscapes with only simple sign epistasis motifs will always give rise to single-peaked fitness landscapes under such selection. More broadly, we show that such selection tends to create fitness landscapes that are more rugged than the underlying genotype-phenotype landscape, but this increased ruggedness typically does not frustrate adaptive evolution because the local adaptive peaks in the fitness landscape tend to be nearly as tall as the global peak. Many of these results carry forward to the empirical genotype-phenotype landscapes, which may help to explain why low- and intermediate-affinity transcription factor-DNA interactions are so prevalent in eukaryotic gene regulation. Public Library of Science 2022-09-19 /pmc/articles/PMC9521842/ /pubmed/36121840 http://dx.doi.org/10.1371/journal.pcbi.1010524 Text en © 2022 Srivastava, Payne https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Srivastava, Malvika
Payne, Joshua L.
On the incongruence of genotype-phenotype and fitness landscapes
title On the incongruence of genotype-phenotype and fitness landscapes
title_full On the incongruence of genotype-phenotype and fitness landscapes
title_fullStr On the incongruence of genotype-phenotype and fitness landscapes
title_full_unstemmed On the incongruence of genotype-phenotype and fitness landscapes
title_short On the incongruence of genotype-phenotype and fitness landscapes
title_sort on the incongruence of genotype-phenotype and fitness landscapes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9521842/
https://www.ncbi.nlm.nih.gov/pubmed/36121840
http://dx.doi.org/10.1371/journal.pcbi.1010524
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