Epigenetic then genetic variations underpin rapid adaptation of oyster populations (Crassostrea gigas) to Pacific Oyster Mortality Syndrome (POMS)

Type Article
Acceptance Date 2023-03-12 IN PRESS
Language English
Author(s) Gawra Janan1, Valdivieso Alejandro2, Roux FabriceORCID3, Laporte Martin4, de Lorgeril JulienORCID2, 5, Gueguen YannickORCID2, 6, Saccas Mathilde2, Escoubas Jean-Michel2, Montagnani CarolineORCID2, Destoumieux-Garzón Delphine2, Lagarde FranckORCID6, Leroy Marc A.2, Haffner Philippe2, Petton BrunoORCID7, Cosseau Céline1, Morga BenjaminORCID8, Dégremont LionelORCID8, Mitta GuillaumeORCID1, 9, Grunau ChristophORCID1, Vidal-Dupiol JeremieORCID2
Affiliation(s) 1 : IHPE, Univ Perpignan Via Domitia, CNRS, Ifremer, Univ Montpellier, Perpignan, France
2 : IHPE, Univ Montpellier, CNRS, Ifremer, Univ Perpignan Via Domitia, Montpellier, France
3 : Division de l'expertise sur la faune Aquatique, Ministère des Forêts, de la Faune et des Parcs (MFFP), 880 chemin Sainte-Foy, G1S 4X4, Québec, Québec, Canada
4 : LIPME, INRAE, CNRS, Université de Toulouse, Castanet-Tolosan, France
5 : Ifremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, ENTROPIE, Nouméa, Nouvelle- Calédonie, France
6 : MARBEC, Univ Montpellier, CNRS, Ifremer, IRD, Sète, France
7 : LEMAR UMR 6539, UBO/CNRS/IRD/Ifremer, 11 presqu’île du vivier, 29840 Argenton-en-Landunvez, France
8 : Ifremer, ASIM, Adaptation Santé des Invertébrés Marins, La Tremblade, France
9 : Univ Polynesie Francaise, ILM, IRD, Ifremer, F-98719 Tahiti, French Polynesia, France
Source BioRxiv (Cold Spring Harbor Laboratory) In Press
DOI 10.1101/2023.03.09.531494
Keyword(s) rapid adaptation, genetic, epigenetic, POMS, oyster, exome capture

Disease emergence is accelerating in response to human activity-induced global changes. Understanding the mechanisms by which host populations can rapidly adapt to this threat will be crucial for developing future management practices. Pacific Oyster Mortality Syndrome (POMS) imposes a substantial and recurrent selective pressure on oyster populations (Crassostrea gigas). Rapid adaptation to this disease may arise through both genetic and epigenetic mechanisms. In this study, we used a combination of whole exome capture of bisulfite-converted DNA, next-generation sequencing, and (epi)genome-wide association mapping, to show that natural oyster populations differentially exposed to POMS displayed signatures of selection both in their genome (single nucleotide polymorphisms) and epigenome (CG-context DNA methylation). Consistent with higher resistance to POMS, the genes targeted by genetic and epigenetic variations were mainly related to host immunity. By combining correlation analyses, DNA methylation quantitative trait loci, and variance partitioning, we revealed that a third of the observed phenotypic variation was explained by interactions between the genetic sequence and epigenetic information, ∼14% by the genetic sequence, and up to 25% by the epigenome alone. Thus, as well as genetic adaptation, epigenetic mechanisms governing immune responses contribute significantly to the rapid adaptation of hosts to emerging infectious diseases.

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Gawra Janan, Valdivieso Alejandro, Roux Fabrice, Laporte Martin, de Lorgeril Julien, Gueguen Yannick, Saccas Mathilde, Escoubas Jean-Michel, Montagnani Caroline, Destoumieux-Garzón Delphine, Lagarde Franck, Leroy Marc A., Haffner Philippe, Petton Bruno, Cosseau Céline, Morga Benjamin, Dégremont Lionel, Mitta Guillaume, Grunau Christoph, Vidal-Dupiol Jeremie Epigenetic then genetic variations underpin rapid adaptation of oyster populations (Crassostrea gigas) to Pacific Oyster Mortality Syndrome (POMS). BioRxiv IN PRESS. Publisher's official version : https://doi.org/10.1101/2023.03.09.531494 , Open Access version : https://archimer.ifremer.fr/doc/00827/93938/