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Influence of Recombination and GC-biased Gene Conversion on the Adaptive and Nonadaptive Substitution Rate in Mammals versus Birds

Recombination is expected to affect functional sequence evolution in several ways. On the one hand, recombination is thought to improve the efficiency of multilocus selection by dissipating linkage disequilibrium. On the other hand, natural selection can be counteracted by recombination-associated t...

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Autores principales: Rousselle, Marjolaine, Laverré, Alexandre, Figuet, Emeric, Nabholz, Benoit, Galtier, Nicolas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6389324/
https://www.ncbi.nlm.nih.gov/pubmed/30590692
http://dx.doi.org/10.1093/molbev/msy243
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author Rousselle, Marjolaine
Laverré, Alexandre
Figuet, Emeric
Nabholz, Benoit
Galtier, Nicolas
author_facet Rousselle, Marjolaine
Laverré, Alexandre
Figuet, Emeric
Nabholz, Benoit
Galtier, Nicolas
author_sort Rousselle, Marjolaine
collection PubMed
description Recombination is expected to affect functional sequence evolution in several ways. On the one hand, recombination is thought to improve the efficiency of multilocus selection by dissipating linkage disequilibrium. On the other hand, natural selection can be counteracted by recombination-associated transmission distorters such as GC-biased gene conversion (gBGC), which tends to promote G and C alleles irrespective of their fitness effect in high-recombining regions. It has been suggested that gBGC might impact coding sequence evolution in vertebrates, and particularly the ratio of nonsynonymous to synonymous substitution rates (dN/dS). However, distinctive gBGC patterns have been reported in mammals and birds, maybe reflecting the documented contrasts in evolutionary dynamics of recombination rate between these two taxa. Here, we explore how recombination and gBGC affect coding sequence evolution in mammals and birds by analyzing proteome-wide data in six species of Galloanserae (fowls) and six species of catarrhine primates. We estimated the dN/dS ratio and rates of adaptive and nonadaptive evolution in bins of genes of increasing recombination rate, separately analyzing AT → GC, GC → AT, and G ↔ C/A ↔ T mutations. We show that in both taxa, recombination and gBGC entail a decrease in dN/dS. Our analysis indicates that recombination enhances the efficiency of purifying selection by lowering Hill–Robertson effects, whereas gBGC leads to an overestimation of the adaptive rate of AT → GC mutations. Finally, we report a mutagenic effect of recombination, which is independent of gBGC.
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spelling pubmed-63893242019-03-05 Influence of Recombination and GC-biased Gene Conversion on the Adaptive and Nonadaptive Substitution Rate in Mammals versus Birds Rousselle, Marjolaine Laverré, Alexandre Figuet, Emeric Nabholz, Benoit Galtier, Nicolas Mol Biol Evol Discoveries Recombination is expected to affect functional sequence evolution in several ways. On the one hand, recombination is thought to improve the efficiency of multilocus selection by dissipating linkage disequilibrium. On the other hand, natural selection can be counteracted by recombination-associated transmission distorters such as GC-biased gene conversion (gBGC), which tends to promote G and C alleles irrespective of their fitness effect in high-recombining regions. It has been suggested that gBGC might impact coding sequence evolution in vertebrates, and particularly the ratio of nonsynonymous to synonymous substitution rates (dN/dS). However, distinctive gBGC patterns have been reported in mammals and birds, maybe reflecting the documented contrasts in evolutionary dynamics of recombination rate between these two taxa. Here, we explore how recombination and gBGC affect coding sequence evolution in mammals and birds by analyzing proteome-wide data in six species of Galloanserae (fowls) and six species of catarrhine primates. We estimated the dN/dS ratio and rates of adaptive and nonadaptive evolution in bins of genes of increasing recombination rate, separately analyzing AT → GC, GC → AT, and G ↔ C/A ↔ T mutations. We show that in both taxa, recombination and gBGC entail a decrease in dN/dS. Our analysis indicates that recombination enhances the efficiency of purifying selection by lowering Hill–Robertson effects, whereas gBGC leads to an overestimation of the adaptive rate of AT → GC mutations. Finally, we report a mutagenic effect of recombination, which is independent of gBGC. Oxford University Press 2019-03 2018-12-27 /pmc/articles/PMC6389324/ /pubmed/30590692 http://dx.doi.org/10.1093/molbev/msy243 Text en © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
Rousselle, Marjolaine
Laverré, Alexandre
Figuet, Emeric
Nabholz, Benoit
Galtier, Nicolas
Influence of Recombination and GC-biased Gene Conversion on the Adaptive and Nonadaptive Substitution Rate in Mammals versus Birds
title Influence of Recombination and GC-biased Gene Conversion on the Adaptive and Nonadaptive Substitution Rate in Mammals versus Birds
title_full Influence of Recombination and GC-biased Gene Conversion on the Adaptive and Nonadaptive Substitution Rate in Mammals versus Birds
title_fullStr Influence of Recombination and GC-biased Gene Conversion on the Adaptive and Nonadaptive Substitution Rate in Mammals versus Birds
title_full_unstemmed Influence of Recombination and GC-biased Gene Conversion on the Adaptive and Nonadaptive Substitution Rate in Mammals versus Birds
title_short Influence of Recombination and GC-biased Gene Conversion on the Adaptive and Nonadaptive Substitution Rate in Mammals versus Birds
title_sort influence of recombination and gc-biased gene conversion on the adaptive and nonadaptive substitution rate in mammals versus birds
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6389324/
https://www.ncbi.nlm.nih.gov/pubmed/30590692
http://dx.doi.org/10.1093/molbev/msy243
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