Genome‐wide evolutionary response of European oaks during the Anthropocene

Abstract The pace of tree microevolution during Anthropocene warming is largely unknown. We used a retrospective approach to monitor genomic changes in oak trees since the Little Ice Age (LIA). Allelic frequency changes were assessed from whole‐genome pooled sequences for four age‐structured cohorts...

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Main Authors: Dounia Saleh, Jun Chen, Jean‐Charles Leplé, Thibault Leroy, Laura Truffaut, Benjamin Dencausse, Céline Lalanne, Karine Labadie, Isabelle Lesur, Didier Bert, Frédéric Lagane, François Morneau, Jean‐Marc Aury, Christophe Plomion, Martin Lascoux, Antoine Kremer
Format: Article
Language:English
Published: Oxford University Press 2022-02-01
Series:Evolution Letters
Subjects:
Online Access:https://doi.org/10.1002/evl3.269
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author Dounia Saleh
Jun Chen
Jean‐Charles Leplé
Thibault Leroy
Laura Truffaut
Benjamin Dencausse
Céline Lalanne
Karine Labadie
Isabelle Lesur
Didier Bert
Frédéric Lagane
François Morneau
Jean‐Marc Aury
Christophe Plomion
Martin Lascoux
Antoine Kremer
author_facet Dounia Saleh
Jun Chen
Jean‐Charles Leplé
Thibault Leroy
Laura Truffaut
Benjamin Dencausse
Céline Lalanne
Karine Labadie
Isabelle Lesur
Didier Bert
Frédéric Lagane
François Morneau
Jean‐Marc Aury
Christophe Plomion
Martin Lascoux
Antoine Kremer
author_sort Dounia Saleh
collection DOAJ
description Abstract The pace of tree microevolution during Anthropocene warming is largely unknown. We used a retrospective approach to monitor genomic changes in oak trees since the Little Ice Age (LIA). Allelic frequency changes were assessed from whole‐genome pooled sequences for four age‐structured cohorts of sessile oak (Quercus petraea) dating back to 1680, in each of three different oak forests in France. The genetic covariances of allelic frequency changes increased between successive time periods, highlighting genome‐wide effects of linked selection. We found imprints of parallel linked selection in the three forests during the late LIA, and a shift of selection during more recent time periods of the Anthropocene. The changes in allelic covariances within and between forests mirrored the documented changes in the occurrence of extreme events (droughts and frosts) over the last 300 years. The genomic regions with the highest covariances were enriched in genes involved in plant responses to pathogens and abiotic stresses (temperature and drought). These responses are consistent with the reported sequence of frost (or drought) and disease damage ultimately leading to the oak dieback after extreme events. They provide support for adaptive evolution of long‐lived species during recent climatic changes. Although we acknowledge that other sources (e.g., gene flow, generation overlap) may have contributed to temporal covariances of allelic frequency changes, the consistent and correlated response across the three forests lends support to the existence of a systematic driving force such as natural selection.
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spelling doaj.art-7c97443498b14197be9c8b45156d38e42023-08-02T02:44:04ZengOxford University PressEvolution Letters2056-37442022-02-016142010.1002/evl3.269Genome‐wide evolutionary response of European oaks during the AnthropoceneDounia Saleh0Jun Chen1Jean‐Charles Leplé2Thibault Leroy3Laura Truffaut4Benjamin Dencausse5Céline Lalanne6Karine Labadie7Isabelle Lesur8Didier Bert9Frédéric Lagane10François Morneau11Jean‐Marc Aury12Christophe Plomion13Martin Lascoux14Antoine Kremer15UMR BIOGECO, INRAE Université de Bordeaux Cestas 33612 FranceCollege of Life Sciences Zhejiang University Hangzhou 310058 ChinaUMR BIOGECO, INRAE Université de Bordeaux Cestas 33612 FranceDepartment of Botany and Biodiversity Research University of Vienna Vienna 1010 AustriaUMR BIOGECO, INRAE Université de Bordeaux Cestas 33612 FranceUMR BIOGECO, INRAE Université de Bordeaux Cestas 33612 FranceUMR BIOGECO, INRAE Université de Bordeaux Cestas 33612 FranceGenoscope, Institut de Biologie François Jacob, Commissariat à l’énergie atomique (CEA) Université de Paris‐Saclay Evry 91057 FranceHelix Venture Merignac 33700 FranceUMR BIOGECO, INRAE Université de Bordeaux Cestas 33612 FranceUMR BIOGECO, INRAE Université de Bordeaux Cestas 33612 FranceDépartement Recherche Développement Innovation Office National des Forêts Boigny‐Sur‐Bionne 45760 FranceGénomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS Univ Evry, Université Paris‐Saclay Evry 91057 FranceUMR BIOGECO, INRAE Université de Bordeaux Cestas 33612 FranceDepartment of Ecology and Genetics, Evolutionary Biology Centre Uppsala University Uppsala SE‐75236 SwedenUMR BIOGECO, INRAE Université de Bordeaux Cestas 33612 FranceAbstract The pace of tree microevolution during Anthropocene warming is largely unknown. We used a retrospective approach to monitor genomic changes in oak trees since the Little Ice Age (LIA). Allelic frequency changes were assessed from whole‐genome pooled sequences for four age‐structured cohorts of sessile oak (Quercus petraea) dating back to 1680, in each of three different oak forests in France. The genetic covariances of allelic frequency changes increased between successive time periods, highlighting genome‐wide effects of linked selection. We found imprints of parallel linked selection in the three forests during the late LIA, and a shift of selection during more recent time periods of the Anthropocene. The changes in allelic covariances within and between forests mirrored the documented changes in the occurrence of extreme events (droughts and frosts) over the last 300 years. The genomic regions with the highest covariances were enriched in genes involved in plant responses to pathogens and abiotic stresses (temperature and drought). These responses are consistent with the reported sequence of frost (or drought) and disease damage ultimately leading to the oak dieback after extreme events. They provide support for adaptive evolution of long‐lived species during recent climatic changes. Although we acknowledge that other sources (e.g., gene flow, generation overlap) may have contributed to temporal covariances of allelic frequency changes, the consistent and correlated response across the three forests lends support to the existence of a systematic driving force such as natural selection.https://doi.org/10.1002/evl3.269Anthropoceneevolutionlinked selectionLittle Ice AgeQuercus petraea
spellingShingle Dounia Saleh
Jun Chen
Jean‐Charles Leplé
Thibault Leroy
Laura Truffaut
Benjamin Dencausse
Céline Lalanne
Karine Labadie
Isabelle Lesur
Didier Bert
Frédéric Lagane
François Morneau
Jean‐Marc Aury
Christophe Plomion
Martin Lascoux
Antoine Kremer
Genome‐wide evolutionary response of European oaks during the Anthropocene
Evolution Letters
Anthropocene
evolution
linked selection
Little Ice Age
Quercus petraea
title Genome‐wide evolutionary response of European oaks during the Anthropocene
title_full Genome‐wide evolutionary response of European oaks during the Anthropocene
title_fullStr Genome‐wide evolutionary response of European oaks during the Anthropocene
title_full_unstemmed Genome‐wide evolutionary response of European oaks during the Anthropocene
title_short Genome‐wide evolutionary response of European oaks during the Anthropocene
title_sort genome wide evolutionary response of european oaks during the anthropocene
topic Anthropocene
evolution
linked selection
Little Ice Age
Quercus petraea
url https://doi.org/10.1002/evl3.269
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