Due to the accelerating climate change, it is crucial to understand how plants adapt to rapid environmental changes. Such adaptation may be mediated by epigenetic mechanisms like DNA methylation, which could heritably alter phenotypes without changing the DNA sequence, especially across clonal generations. However, we are still missing robust evidence of the adaptive potential of DNA methylation in wild clonal populations. Here, we studied genetic, epigenetic and transcriptomic variation of Fragaria vesca, a predominantly clonally reproducing herb. We examined samples from 21 natural populations across three climatically distinct geographic regions, as well as clones of the same individuals grown in a common garden. We found that epigenetic variation was partly associated with climate of origin, particularly in non-CG contexts. Importantly, a large proportion of this variation was heritable across clonal generations. Additionally, a subset of these epigenetic changes affected the expression of genes mainly involved in plant growth and responses to pathogen and abiotic stress. These findings highlight the potential influence of epigenetic changes on phenotypic traits. Our findings indicate that variation in DNA methylation, which can be environmentally inducible and heritable, may enable clonal plant populations to adjust to their environmental conditions even in the absence of genetic adaptation.

Department of Biology Philipps University Marburg Karl von Frisch Strasse 8 D 35043 Marburg Germany

Department of Botany Faculty of Science Charles University Benátská 2 128 01 Prague Czechia

Department of Computer Science University of Leipzig Härtelstraße 16 18 Leipzig 04107 Germany

Department of Forest Genetics Albert Ludwigs Universität Freiburg Bertoldstraße 17 79098 Freiburg i Br Germany

ecSeq Bioinformatics GmbH Sternwartenstraße 29 04103 Saxony Germany

Gregor Mendel Institute of Molecular Plant Biology Austrian Academy of Sciences Vienna BioCenter Dr Bohr Gasse 3 1030 Vienna Austria

Institute of Botany Czech Academy of Sciences Zámek 1 252 43 Průhonice Czechia

LMU Biocenter Faculty of Biology Ludwig Maximilians University Munich Grosshaderner Str 2 4 82152 Martinsried Germany

Natural Resources and Climate Area CARTIF Technology Centre Parque Tecnológico de Boecillo parc 205 47151 Boecillo Valladolid Spain

Plant Evolutionary Ecology Institute of Evolution and Ecology University of Tübingen Auf der Morgenstelle 5 72076 Tübingen Germany

Royal Botanic Gardens Kew Richmond UK

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The evolutionary consequences of interactions between the epigenome, the genome and the environment