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Epigenetic variation causes heritable variation in complex traits in the mollusk Biomphalaria glabrata, vector of the human parasite Schistosoma mansoni

Nelia Luviano, Marie Lopez, Fleur Gawehns, Bart Haegeman, Pierick Mouginot, Cristian Chaparro, Paola B. Arimondo, Benoit Pujol, Damien Pouzol, Céline Cosseau, View ORCID ProfileChristoph Grunau
doi: https://doi.org/10.1101/2023.07.08.548202
Nelia Luviano
1Interactions Hôtes Pathogènes Environnements (IHPE), Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan France
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Marie Lopez
2Institut des Biomolécules Max Mousseron (IBMM), CNRS, Univ Montpellier, ENSCM UMR 5247, 240 avenue du Prof. E. Jeanbrau, 34296 Montpellier cedex 5, France
3Epigenetic Targeting of Cancer (ETaC), CNRS FRE3600, Centre de Recherche et Développement Pierre Fabre, Toulouse, France
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Fleur Gawehns
4Bioinformatics Unit, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
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Bart Haegeman
5CNRS/Sorbonne Université, UMR7621 Laboratoire d’Océanographie Microbienne, Banyuls-sur-Mer, France
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Pierick Mouginot
1Interactions Hôtes Pathogènes Environnements (IHPE), Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan France
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Cristian Chaparro
1Interactions Hôtes Pathogènes Environnements (IHPE), Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan France
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Paola B. Arimondo
3Epigenetic Targeting of Cancer (ETaC), CNRS FRE3600, Centre de Recherche et Développement Pierre Fabre, Toulouse, France
6Epigenetic Chemical Biology (EpiChBio), Department Structural Biology and Chemistry, UMR 3523 CNRS, Institute Pasteur, 75015 Paris, France
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Benoit Pujol
7PSL Université Paris : EPHE-UPVD-CNRS, USR 3278 CRIOBE, Université de Perpignan, Perpignan, France
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Damien Pouzol
1Interactions Hôtes Pathogènes Environnements (IHPE), Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan France
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Céline Cosseau
1Interactions Hôtes Pathogènes Environnements (IHPE), Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan France
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Christoph Grunau
1Interactions Hôtes Pathogènes Environnements (IHPE), Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan France
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  • ORCID record for Christoph Grunau
  • For correspondence: christoph.grunau@univ-perp.fr
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Abstract

DNA methylation variation may play a role in phenotypic variation as it can be directly affected by the environment and be inherited. DNA methylation variations were introduced into the parasite vector snail Biomphalaria glabrata with low genetic diversity by chemical treatment in F0 and followed over 3 generations using epigenetic recombinant inbred lines (epiRILs). We observed phenotypic variation in complex traits such as fecundity and susceptibility to infestation by Schistosoma mansoni and DNA methylation differences in F3. Both, increase and decrease of infestation success (up to 100% and down to 20% prevalence in epiRILs and from 86% to 94% in control RILs) indicated variation in complex resistance/compatibility trait. Average prevalence in control RILs was 84±5% but only 68±21 % in epiRILs. Fecundity also changed and was in average 47±7% in control RILs and 59±18% in epiRILs, being 12% higher in epiRILs. We found that the heritability h2 of the fecundity in the epiRILs was between 0.5 and 0.6 depending on the method used to estimate it. We developed a model for introducing epimutant offspring snails into resident susceptible populations. If genetic assimilation of the resistant phenotype occured in a small fraction of the introduced epimutant snails, we predict that the susceptible phenotype is replaced by the resistant phenotype after 50-70 generations.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Add auteur who was accidentally missing from the author list in the web interface but who was already on the manuscript.

  • https://www.ncbi.nlm.nih.gov/bioproject/PRJNA973008

  • https://doi.org/10.5281/zenodo.8114403

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted July 11, 2023.
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Epigenetic variation causes heritable variation in complex traits in the mollusk Biomphalaria glabrata, vector of the human parasite Schistosoma mansoni
Nelia Luviano, Marie Lopez, Fleur Gawehns, Bart Haegeman, Pierick Mouginot, Cristian Chaparro, Paola B. Arimondo, Benoit Pujol, Damien Pouzol, Céline Cosseau, Christoph Grunau
bioRxiv 2023.07.08.548202; doi: https://doi.org/10.1101/2023.07.08.548202
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Epigenetic variation causes heritable variation in complex traits in the mollusk Biomphalaria glabrata, vector of the human parasite Schistosoma mansoni
Nelia Luviano, Marie Lopez, Fleur Gawehns, Bart Haegeman, Pierick Mouginot, Cristian Chaparro, Paola B. Arimondo, Benoit Pujol, Damien Pouzol, Céline Cosseau, Christoph Grunau
bioRxiv 2023.07.08.548202; doi: https://doi.org/10.1101/2023.07.08.548202

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