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Exploring the speciation continuum of slow worms: location and extent of the Anguis fragilis/veronensis hybrid zone in southeastern France

In: Amphibia-Reptilia
Authors:
Christophe Dufresnes Laboratory for Amphibian Systematic & Evolutionary Research, College of Biology & the Environment, Nanjing Forestry University, Nanjing, 210037, People’s Republic of China

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https://orcid.org/0000-0002-8497-8908
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Patricia Sourrouille CEFE, CNRS, Univ. Montpellier, EPHE, IRD, 34293 Montpellier, France

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Anthony Olivier Tour du Valat, Research Institute for the Conservation of Mediterranean Wetlands, 13200 Arles, France

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Jean-Marie Ballouard CRCC – Centre for Research and Conservation of Chelonians, SOPTOM, Var, 1065 routes du Luc, 83660 Carnoules, France

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Marie-France Leccia Parc National du Mercantour, 06000 Nice, France

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Rémi Tiné Syndicat Mixte Camargue Gardoise, Centre du Scamandre, Route des Iscles, Gallician, 30600 Vauvert, France

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Marc Cheylan Biogéographie et Ecologie des Vertébrés, CEFE, EPHE-PSL University, Univ. Montpellier, CNRS, IRD, 34293 Montpellier, France

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Maxime Le Henanff ECO-MED – Ecologie & Médiation, Résidence Atrium, 113 rue Raymond Recouly, 34070 Montpellier, France

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Jean Nicolas , 7, rue du Labro, 34260 Camplong, France

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Sébastien Caron CRCC – Centre for Research and Conservation of Chelonians, SOPTOM, Var, 1065 routes du Luc, 83660 Carnoules, France

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Grégoire Massez Les Amis des Marais du Vigueirat, Les Marais du Vigueirat, Chemin de l’Etourneau, 13104 Mas Thibert, France

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Alexandre Cluchier ECO-MED – Ecologie & Médiation, Résidence Atrium, 113 rue Raymond Recouly, 34070 Montpellier, France

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Romain Levasseur CRCC – Centre for Research and Conservation of Chelonians, SOPTOM, Var, 1065 routes du Luc, 83660 Carnoules, France
, 474 rue des Comtes de Provence, 83143 Le Val, France

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Fabien Pille CRCC – Centre for Research and Conservation of Chelonians, SOPTOM, Var, 1065 routes du Luc, 83660 Carnoules, France
Laboratory of Ecology and Conservation of Amphibians (LECA), Freshwater and Oceanic Science Unit of Research (FOCUS), University of Liège, 4020 Liege, Belgium

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Olivier Peyre PANDORA, 20 rue Durrell, BP61261, 84922 Avignon cédex 9, France

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Marc Thibault Tour du Valat, Research Institute for the Conservation of Mediterranean Wetlands, 13200 Arles, France

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Angelica Crottini CIBIO/InBio, Centro de Investigação em Biodiversidade e Recursos Genéticos Campus Agrário de Vairão, Rua Padre Armando Quintas, 4485-661 Vairão, Portugal
Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, 4099-002 Porto, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Campus de Vairão, 4485-661 Vairão, Portugal

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Nicolas Fuento LPO PACA, 6 Av. Jean Jaurès, 83400 Hyères, France

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Pierre-André Crochet CEFE, CNRS, Univ. Montpellier, EPHE, IRD, 34293 Montpellier, France

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Abstract

With five currently recognized species that form several secondary contact zones, slow worms (Anguidae: Anguis) offer a valuable model to study the fate of evolutionary lineages in the face of hybridization and genetic introgression. The relationships between the Western Slow Worm Anguis fragilis and the Italian Slow Worm Anguis veronensis are particularly puzzling. Their respective distributions remain poorly known on the edges of their parapatric ranges, as both species lack external differentiation. Contra earlier mitochondrial phylogenies, new phylogenomic inferences have shown that A. fragilis and A. veronensis are sister taxa, thus casting doubts on their specific status. In this study, we analyze the A. fragilis/veronensis transition in southeastern France, based on one mitochondrial (ND2) and two nuclear (PRLR and HA1) genetic markers in 81 specimens from 61 localities. The ranges of A. fragilis and A. veronensis roughly extends northwest and southeast of the Rhône-Durance valleys, respectively, with clear signs of introgressive hybridization in the areas of contact (notably the eastern parts of the lower Rhône valley). Based on the three molecular markers analyzed, gene flow does not seem to reach outside the narrow hybrid zone, which likely indicates (incomplete) intrinsic reproductive isolation. Hence, we provisionally suggest maintaining A. veronensis as a separate species from A. fragilis. More generally, patterns of genetic divergence, external differentiation, and hybridization (both historical and contemporary) in Anguis ssp. supports a speciation continuum spanning from cryptic, genetically compatible alloparapatric lineages to phenotypically distinct, deeply diverged and fully reproductively isolated taxa able to coexist in sympatry.

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