Prevalence and polymorphism of a mussel transmissible cancer in Europe

Type Article
Date 2022-02
Language English
Author(s) Hammel Maurine1, 2, Simon Alexis1, Arbiol Christine1, Villalba Antonio3, 4, 5, Burioli Erika Av2, 6, Pépin Jean-Francois7, Lamy Jean-BaptisteORCID8, Benabdelmouna AbdellahORCID8, Bernard Ismael9, Houssin Maryline6, Charrière Guillaume2, Destoumieux Garzon Delphine2, Welch John J.10, Metzger Michael J11, Bierne Nicolas1
Affiliation(s) 1 : ISEM, Univ Montpellier, CNRS, EPHE, IRD Montpellier,France
2 : IHPE, Univ Montpellier, CNRS, Ifremer, Univ Perpignan Via Domitia, France
3 : Centro de Investigacións Mariñas Consellería do Mar, Xunta de Galicia Vilanova de Arousa ,Spain
4 : Departamento de Ciencias de la Vida Universidad de Alcalá Alcalá de Henares, Spain
5 : Research Centre for Experimental Marine Biology and Biotechnology (PIE) University of the Basque Country (UPV/EHU) Plentzia, Basque Country, Spain
6 : LABÉO, Caen, France
7 : Laboratoire Environnement ressources des Pertuis Charentais IFREMER La Tremblade ,France
8 : Santé, Génétique, Microbiologie des Mollusques, IFREMER La Tremblade, France
9 : Eurêka Mer, Lézardrieux, France
10 : Department of Genetics,University of Cambridge Downing Street, Cambridge, UK
11 : Pacific Northwest Research Institute, Seattle, USA
Source Molecular Ecology (0962-1083) (Wiley), 2022-02 , Vol. 31 , N. 3 , P. 736-751
DOI 10.1111/mec.16052
WOS© Times Cited 9
Keyword(s) disseminated neoplasia, genetic chimerism, genetic polymorphism, Mytilus sp, mussels, transmissible cancer
Abstract

Transmissible cancers are parasitic malignant cell lineages that acquired the ability to infect new hosts from the same species, or sometimes related species. First described in dogs and Tasmanian devils, transmissible cancers were later discovered in some marine bivalves affected by a leukemia-like disease. In Mytilus mussels, two lineages of Bivalve Transmissible Neoplasia (BTN) have been described to date (MtrBTN1 and MtrBTN2), both emerged in a M. trossulus founder individual. Here, we performed an extensive screening of genetic chimerism, a hallmark of transmissible cancer, by genotyping 106 SNPs of 5907 European Mytilus mussels. The genetic analysis allowed us to simultaneously obtain the genotype of hosts - M. edulis, M. galloprovincialis or hybrids - and the genotype of tumors of heavily infected individuals. In addition, a subset of 222 individuals were systematically genotyped and analysed by histology in order to screen for possible non-transmissible cancers. We detected MtrBTN2 at low prevalence in M.edulis, and also in M. galloprovincialis and hybrids although at a much lower prevalence. No MtrBTN1 or new BTN were found, but 8 individuals with non-transmissible neoplasia were observed at a single polluted site on the same sampling date. We observed a diversity of MtrBTN2 genotypes that appeared more introgressed or more ancestral than MtrBTN1 and reference healthy M. trossulus individuals. The observed polymorphism is most likely due to somatic null alleles caused by structural variations or point mutations in primer-binding sites leading to enhanced detection of the host alleles. Despite low prevalence, two sublineages divergent by 10% fixed somatic null alleles and one non-synonymous mtCOI substitution, are co-spreading in the same geographic area, suggesting a complex diversification of MtrBTN2 since its emergence and host species shift.

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Hammel Maurine, Simon Alexis, Arbiol Christine, Villalba Antonio, Burioli Erika Av, Pépin Jean-Francois, Lamy Jean-Baptiste, Benabdelmouna Abdellah, Bernard Ismael, Houssin Maryline, Charrière Guillaume, Destoumieux Garzon Delphine, Welch John J., Metzger Michael J, Bierne Nicolas (2022). Prevalence and polymorphism of a mussel transmissible cancer in Europe. Molecular Ecology, 31(3), 736-751. Publisher's official version : https://doi.org/10.1111/mec.16052 , Open Access version : https://archimer.ifremer.fr/doc/00703/81540/