Divergent and stabilizing selection shape the phenotypic space of Arabidopsis thaliana

Why do we observe some plant phenotypes but not others? The multivariate phenotypic space occupied by individuals or species often reveals both limits and phenotypes strikingly deviating from main syndromes. These observations are usually thought to indicate, respectively, inviable trait combinations and unique phenotypes adapted to specific environments. However, the evolutionary drivers underlying trait covariations often remain unclear. Here, we characterized the phenotypic space of Arabidopsis thaliana by comparing 713 wild accessions collected across the globe with 2,544 artificially-created recombinant individuals. This, combined with the detection of adaptive processes operating within species, allowed us to elucidate the roles of natural selection as a driver of phenotypic (co)variations within A. thaliana. We found that the phenotypic space of this species is constrained and driven by varying levels of divergent and stabilizing selection across different traits. Moreover, at the margins of the European geographic range, strong directional selection favored outlier phenotypes characterized by very late flowering and variation in a WRKY transcription factor gene. Genome analyses revealed that these extreme phenotypes may be explained by hybridization between ancestral and modern lineages of A. thaliana. Our findings demonstrate how interplays between population history and natural selection shape phenotypic diversity in a plant species.

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Journal
PLoS Biology
Published
2025-12-01
DOI
https://doi.org/10.1371/journal.pbio.3003536
Primary Topic
Genetic Mapping and Diversity in Plants and Animals
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article
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article

Divergent and stabilizing selection shape the phenotypic space of Arabidopsis thaliana

Aurélien Estarague, Denis Vile, Lucie Mahaut, J. F. Scheepens et al.
PLoS Biology
Genetic Mapping and Diversity in Plants and Animals
article

Divergent and stabilizing selection shape the phenotypic space of Arabidopsis thaliana

Aurélien Estarague, Denis Vile, Lucie Mahaut, J. F. Scheepens, François Vasseur, Moisés Expósito‐Alonso, Denis Cornet, Oliver Bossdorf, Lauriane Rouan, Elena Kazakou, Cyrille Violle, Maria Stefania Przybylska, Grégory Beurier, Luis‐Miguel Chevin, Detlef Weigel, François Munoz
article en

Abstract

Why do we observe some plant phenotypes but not others? The multivariate phenotypic space occupied by individuals or species often reveals both limits and phenotypes strikingly deviating from main syndromes. These observations are usually thought to indicate, respectively, inviable trait combinations and unique phenotypes adapted to specific environments. However, the evolutionary drivers underlying trait covariations often remain unclear. Here, we characterized the phenotypic space of Arabidopsis thaliana by comparing 713 wild accessions collected across the globe with 2,544 artificially-created recombinant individuals. This, combined with the detection of adaptive processes operating within species, allowed us to elucidate the roles of natural selection as a driver of phenotypic (co)variations within A. thaliana. We found that the phenotypic space of this species is constrained and driven by varying levels of divergent and stabilizing selection across different traits. Moreover, at the margins of the European geographic range, strong directional selection favored outlier phenotypes characterized by very late flowering and variation in a WRKY transcription factor gene. Genome analyses revealed that these extreme phenotypes may be explained by hybridization between ancestral and modern lineages of A. thaliana. Our findings demonstrate how interplays between population history and natural selection shape phenotypic diversity in a plant species.

PLoS BiologyVol. 23(12)
Université Claude Bernard Lyon 1 (FR), Goethe University Frankfurt (DE), Centre National de la Recherche Scientifique (FR), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (FR), Howard Hughes Medical Institute (US), École Pratique des Hautes Études (FR), Université de Montpellier (FR), Institut Agro Montpellier (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Centre d'Écologie Fonctionnelle et Évolutive (FR), Université Paul-Valéry Montpellier (FR), Amélioration Génétique et Adaptation des Plantes méditerranéennes et tropicales (FR), Laboratoire d'Ecophysiologie des Plantes sous Stress environnementaux (FR), Laboratoire de Biométrie et Biologie Evolutive (FR), Institut Agro Montpelier (FR), Max Planck Institute for Biology (DE), Institut de Recherche pour le Développement (FR), University of Tübingen (DE), University of California, Berkeley (US)
Openalex Percentile: Top 60%
Genetic Mapping and Diversity in Plants and Animals
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