Estimating the proportion of beneficial mutations that are not adaptive in mammals.

Mutations can be beneficial by bringing innovation to their bearer, allowing them to adapt to environmental change. These mutations are typically unpredictable since they respond to an unforeseen change in the environment. However, mutations can also be beneficial because they are simply restoring a...

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Main Authors: Thibault Latrille, Julien Joseph, Diego A Hartasánchez, Nicolas Salamin
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-12-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1011536
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author Thibault Latrille
Julien Joseph
Diego A Hartasánchez
Nicolas Salamin
author_facet Thibault Latrille
Julien Joseph
Diego A Hartasánchez
Nicolas Salamin
author_sort Thibault Latrille
collection DOAJ
description Mutations can be beneficial by bringing innovation to their bearer, allowing them to adapt to environmental change. These mutations are typically unpredictable since they respond to an unforeseen change in the environment. However, mutations can also be beneficial because they are simply restoring a state of higher fitness that was lost due to genetic drift in a stable environment. In contrast to adaptive mutations, these beneficial non-adaptive mutations can be predicted if the underlying fitness landscape is stable and known. The contribution of such non-adaptive mutations to molecular evolution has been widely neglected mainly because their detection is very challenging. We have here reconstructed protein-coding gene fitness landscapes shared between mammals, using mutation-selection models and a multi-species alignments across 87 mammals. These fitness landscapes have allowed us to predict the fitness effect of polymorphisms found in 28 mammalian populations. Using methods that quantify selection at the population level, we have confirmed that beneficial non-adaptive mutations are indeed positively selected in extant populations. Our work confirms that deleterious substitutions are accumulating in mammals and are being reverted, generating a balance in which genomes are damaged and restored simultaneously at different loci. We observe that beneficial non-adaptive mutations represent between 15% and 45% of all beneficial mutations in 24 of 28 populations analyzed, suggesting that a substantial part of ongoing positive selection is not driven solely by adaptation to environmental change in mammals.
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spelling doaj-art-66d1443f0f9f4c61a0546e89225f61272025-01-17T05:31:12ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042024-12-012012e101153610.1371/journal.pgen.1011536Estimating the proportion of beneficial mutations that are not adaptive in mammals.Thibault LatrilleJulien JosephDiego A HartasánchezNicolas SalaminMutations can be beneficial by bringing innovation to their bearer, allowing them to adapt to environmental change. These mutations are typically unpredictable since they respond to an unforeseen change in the environment. However, mutations can also be beneficial because they are simply restoring a state of higher fitness that was lost due to genetic drift in a stable environment. In contrast to adaptive mutations, these beneficial non-adaptive mutations can be predicted if the underlying fitness landscape is stable and known. The contribution of such non-adaptive mutations to molecular evolution has been widely neglected mainly because their detection is very challenging. We have here reconstructed protein-coding gene fitness landscapes shared between mammals, using mutation-selection models and a multi-species alignments across 87 mammals. These fitness landscapes have allowed us to predict the fitness effect of polymorphisms found in 28 mammalian populations. Using methods that quantify selection at the population level, we have confirmed that beneficial non-adaptive mutations are indeed positively selected in extant populations. Our work confirms that deleterious substitutions are accumulating in mammals and are being reverted, generating a balance in which genomes are damaged and restored simultaneously at different loci. We observe that beneficial non-adaptive mutations represent between 15% and 45% of all beneficial mutations in 24 of 28 populations analyzed, suggesting that a substantial part of ongoing positive selection is not driven solely by adaptation to environmental change in mammals.https://doi.org/10.1371/journal.pgen.1011536
spellingShingle Thibault Latrille
Julien Joseph
Diego A Hartasánchez
Nicolas Salamin
Estimating the proportion of beneficial mutations that are not adaptive in mammals.
PLoS Genetics
title Estimating the proportion of beneficial mutations that are not adaptive in mammals.
title_full Estimating the proportion of beneficial mutations that are not adaptive in mammals.
title_fullStr Estimating the proportion of beneficial mutations that are not adaptive in mammals.
title_full_unstemmed Estimating the proportion of beneficial mutations that are not adaptive in mammals.
title_short Estimating the proportion of beneficial mutations that are not adaptive in mammals.
title_sort estimating the proportion of beneficial mutations that are not adaptive in mammals
url https://doi.org/10.1371/journal.pgen.1011536
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