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Genes and sites under adaptation at the phylogenetic scale also exhibit adaptation at the population-genetic scale

Adaptation in protein-coding sequences can be detected from multiple sequence alignments across species or alternatively by leveraging polymorphism data within a population. Across species, quantification of the adaptive rate relies on phylogenetic codon models, classically formulated in terms of th...

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Autores principales: Latrille, Thibault, Rodrigue, Nicolas, Lartillot, Nicolas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10089192/
https://www.ncbi.nlm.nih.gov/pubmed/36897968
http://dx.doi.org/10.1073/pnas.2214977120
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author Latrille, Thibault
Rodrigue, Nicolas
Lartillot, Nicolas
author_facet Latrille, Thibault
Rodrigue, Nicolas
Lartillot, Nicolas
author_sort Latrille, Thibault
collection PubMed
description Adaptation in protein-coding sequences can be detected from multiple sequence alignments across species or alternatively by leveraging polymorphism data within a population. Across species, quantification of the adaptive rate relies on phylogenetic codon models, classically formulated in terms of the ratio of nonsynonymous over synonymous substitution rates. Evidence of an accelerated nonsynonymous substitution rate is considered a signature of pervasive adaptation. However, because of the background of purifying selection, these models are potentially limited in their sensitivity. Recent developments have led to more sophisticated mutation–selection codon models aimed at making a more detailed quantitative assessment of the interplay between mutation, purifying, and positive selection. In this study, we conducted a large-scale exome-wide analysis of placental mammals with mutation–selection models, assessing their performance at detecting proteins and sites under adaptation. Importantly, mutation–selection codon models are based on a population-genetic formalism and thus are directly comparable to the McDonald and Kreitman test at the population level to quantify adaptation. Taking advantage of this relationship between phylogenetic and population genetics analyses, we integrated divergence and polymorphism data across the entire exome for 29 populations across 7 genera and showed that proteins and sites detected to be under adaptation at the phylogenetic scale are also under adaptation at the population-genetic scale. Altogether, our exome-wide analysis shows that phylogenetic mutation–selection codon models and the population-genetic test of adaptation can be reconciled and are congruent, paving the way for integrative models and analyses across individuals and populations.
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spelling pubmed-100891922023-09-10 Genes and sites under adaptation at the phylogenetic scale also exhibit adaptation at the population-genetic scale Latrille, Thibault Rodrigue, Nicolas Lartillot, Nicolas Proc Natl Acad Sci U S A Biological Sciences Adaptation in protein-coding sequences can be detected from multiple sequence alignments across species or alternatively by leveraging polymorphism data within a population. Across species, quantification of the adaptive rate relies on phylogenetic codon models, classically formulated in terms of the ratio of nonsynonymous over synonymous substitution rates. Evidence of an accelerated nonsynonymous substitution rate is considered a signature of pervasive adaptation. However, because of the background of purifying selection, these models are potentially limited in their sensitivity. Recent developments have led to more sophisticated mutation–selection codon models aimed at making a more detailed quantitative assessment of the interplay between mutation, purifying, and positive selection. In this study, we conducted a large-scale exome-wide analysis of placental mammals with mutation–selection models, assessing their performance at detecting proteins and sites under adaptation. Importantly, mutation–selection codon models are based on a population-genetic formalism and thus are directly comparable to the McDonald and Kreitman test at the population level to quantify adaptation. Taking advantage of this relationship between phylogenetic and population genetics analyses, we integrated divergence and polymorphism data across the entire exome for 29 populations across 7 genera and showed that proteins and sites detected to be under adaptation at the phylogenetic scale are also under adaptation at the population-genetic scale. Altogether, our exome-wide analysis shows that phylogenetic mutation–selection codon models and the population-genetic test of adaptation can be reconciled and are congruent, paving the way for integrative models and analyses across individuals and populations. National Academy of Sciences 2023-03-10 2023-03-14 /pmc/articles/PMC10089192/ /pubmed/36897968 http://dx.doi.org/10.1073/pnas.2214977120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Latrille, Thibault
Rodrigue, Nicolas
Lartillot, Nicolas
Genes and sites under adaptation at the phylogenetic scale also exhibit adaptation at the population-genetic scale
title Genes and sites under adaptation at the phylogenetic scale also exhibit adaptation at the population-genetic scale
title_full Genes and sites under adaptation at the phylogenetic scale also exhibit adaptation at the population-genetic scale
title_fullStr Genes and sites under adaptation at the phylogenetic scale also exhibit adaptation at the population-genetic scale
title_full_unstemmed Genes and sites under adaptation at the phylogenetic scale also exhibit adaptation at the population-genetic scale
title_short Genes and sites under adaptation at the phylogenetic scale also exhibit adaptation at the population-genetic scale
title_sort genes and sites under adaptation at the phylogenetic scale also exhibit adaptation at the population-genetic scale
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10089192/
https://www.ncbi.nlm.nih.gov/pubmed/36897968
http://dx.doi.org/10.1073/pnas.2214977120
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