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

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posted on 2023-01-19, 08:40 authored by Christophe Dufresnes, Patricia Sourrouille, Anthony Olivier, Jean-Marie Ballouard, Marie-France Leccia, Rémi Tiné, Marc Cheylan, Maxime Le Henanff, Jean Nicolas, Sébastien Caron, Grégoire Massez, Alexandre Cluchier, Romain Levasseur, Fabien Pille, Olivier Peyre, Marc Thibault, Angelica Crottini, Nicolas Fuento, Pierre-André Crochet

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 low 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.