The hidden side of a major marine biogeographic boundary: a wide mosaic hybrid zone at the Atlantic–Mediterranean divide reveals the complex interaction between natural and genetic barriers in mussels

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The Almeria–Oran Front (AOF) is a recognised hotspot of genetic differentiation in the sea, with genetic discontinuities reported in more than 50 species. The AOF is a barrier to dispersal and an ecological boundary; both can determine the position of these genetic breaks. However, the maintenance of genetic differentiation is likely reinforced by genetic barriers. A general drawback of previous studies is an insufficient density of sampling sites at the transition zone, with a conspicuous lack of samples from the southern coastline. We analysed the fine-scale genetic structure in the mussel Mytilus galloprovincialis using a few ancestry-informative loci previously identified from genome scans. We discovered a 600-km-wide mosaic hybrid zone eastward of the AOF along the Algerian coasts. This mosaic zone provides a new twist to our understanding of the Atlantic–Mediterranean transition because it demonstrates that the two lineages can live in sympatry with ample opportunities to interbreed in a large area, but they hardly do so. This implies that some form of reproductive isolation must exist to maintain the two genetic backgrounds locally cohesive. The mosaic zone ends with an abrupt genetic shift at a barrier to dispersal in the Gulf of Bejaia, Eastern Algeria. Simulations of endogenous or exogenous selection in models that account for the geography and hydrodynamic features of the region support the hypothesis that sister hybrid zones could have been differentially trapped at two alternative barriers to dispersal and/or environmental boundaries, at Almeria in the north and Bejaia in the south. A preponderantly unidirectional north–south gene flow next to the AOF can also maintain a patch of intrinsically maintained genetic background in the south and the mosaic structure, even in the absence of local adaptation. Our results concur with the coupling hypothesis that suggests that natural barriers can explain the position of genetic breaks, while their maintenance depends on genetic barriers.

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It is a pleasure to thank Marie-Thérèse Augé and Cathy Haag-Liautard for their technical help in the lab, and Marina Albentosa as well as Carlos Saavedra for Spanish samples. We also thank Pierre-Alexandre Gagnaire, Christelle Fraïsse, François Bonhomme, Nathalie Charbonnel, Sophie Arnaud-Haond and Lilia Bahri-Sfar for discussion, as well as Cynthia Riginos, Heiko Stuckas and six anonymous referees for their insightful comments on earlier drafts. Molecular data were produced through the ISEM platform Génomique des Populations Marines (PGPM7) at the Station Marine de Sète (OSU OREME, Observatoire de Recherche Méditerranéen de l’Environnement) and the platform Génomique Environnementale of the LabEx CeMEB (Laboratoire d’Excellence Centre Méditerranéen de l’Environnement et de la Biodiversité). This work was funded by a Languedoc-Roussillon “Chercheur(se)s d’Avenir” grant (Connect7 project). This is article 2018-286 of Institut des Sciences de l’Evolution de Montpellier.

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Sequence data have been deposited in GenBank: accession numbers MK259098–MK259664. Genotype data have been deposited in Dryad:

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