Transalpine dispersal: Italian barred grass snakes in southernmost Bavaria—This far but no further!

Abstract

Based on 1031 samples of grass snakes from Central Europe, we examine the recently reported occurrence of the southern subspecies of the barred grass snake (Natrix helvetica sicula) in southern Bavaria, Germany. Using 13 microsatellite loci and mtDNA coding for the cytb gene and the partial ND4 gene plus adjacent tRNAs, we show that N. h. sicula is restricted to a few river valleys (Inn, Isar, Loisach) in southernmost Bavaria and adjacent Tyrol, Austria. At the widening of the river valleys into the pre‐Alpine plains, N. h. sicula hybridizes locally with the common grass snake (Natrix natrix) in a bimodal hybrid zone. Our study provides evidence that Central Europe was colonized by Natrix helvetica over two distinct immigration routes. In addition to the previously known western route of the nominotypical subspecies, leading to the colonization of the Rhine region, N. h. sicula crossed the Alps, most likely using the Brenner Pass and/or the Reschen Pass. Our study underlines that the Alps are not an impermeable biogeographic barrier, as often assumed. North of the Alps, the combination of geographic setting (occurrence of N. h. sicula in sheltered Alpine valleys) and population‐density‐dependent blocking of immigrants by the resident species (N. natrix), acting in concert with intrinsic genetic factors, prevented the formation of a geographically more extended hybrid zone. Unlike N. helvetica, the two subspecies of N. natrix hybridize north of the Alps broadly, in accordance with their better genetic compatibility. Many populations of the resident Central European subspecies (Natrix natrix natrix) have been “genetically swamped” by Natrix natrix vulgaris immigrating from the Balkans. This led to the complete replacement of N. n. natrix by N. n. vulgaris in some regions, where today only the mtDNA of the nominotypical subspecies persists.

It takes two to tango – Phylogeography, taxonomy and hybridization in grass snakes and dice snakes (Serpentes: Natricidae: Natrix natrix, N. tessellata)

“…A total of 181 tissue samples (115 N. natrix, 66 N. tessellata) were newly processed and microsatellite data were generated for 15 additional samples of N. natrix with previously published mtDNA sequences (Kindler et al 2013(Kindler et al , 2017. The remaining data originate from earlier studies (Guicking et al 2006(Guicking et al , 2009Kindler et al 2013Kindler et al , 2017Kyriazi et al 2013;Asztalos et al 2021a). Among our material were five samples of big-headed grass snakes from the putative distribution range of N. megaloce phala that were, according to their morphology, tentatively identified with this nominal species (Table S1).…”

“…Until a few years ago, the three grass snake species were lumped together in one polytypic species, N. natrix sensu lato (Mertens and Wermuth 1960;Kabisch 1999;Kreiner 2007). However, recent studies using mtDNA sequences and microsatellite loci revealed only limited gene flow across narrow geographic contact zones and led to their recognition as three distinct species (Pokrant et al 2016;Kindler et al 2017;Schultze et al 2019Schultze et al , 2020Asztalos et al 2020Asztalos et al , 2021aSpeybroeck et al 2020). Natrix astreptophora occurs in the northern Maghreb region, the Iberian Peninsula and southwestern France (Mertens and Wermuth 1960;Kabisch 1999).…”

“…This contact zone is a bimodal hybrid zone (see Jiggins and Mallet 2000), with pure parental genotypes and hybrid genotypes occurring together or in close proximity. Natrix helvetica is distributed in France, Great Britain, the Benelux countries, western Germany, Switzerland, Italy and across the Alps to southern Bavaria and Tyrol (Geniez 2015;Schultze et al 2020;Asztalos et al 2021a). The third grass snake species is Natrix natrix sensu stricto, which occurs from the Rhine region in the west to Lake Baikal in the east.…”

“…In the two other hybrid zones another subspecies of the barred grass snake is involved, N. h. sicula (Cuvier, 1829). It hybridizes with N. natrix in northeastern Italy (Schultze et al 2020) and, beyond the Alps, in southern Bavaria and Tyrol (Asztalos et al 2021a).…”

“…In addition, we scrutinize whether the phylogeographic and taxonomic differentiation of the dice snake (N. tessellata) parallels that of N. natrix in our study region, and we examine, for the first time, whether and, if so, to which extent, natural hybridization occurs between these two sympatric species. For doing so, we apply an established toolbox consisting of combined evidence from mitochondrial DNA (mtDNA) sequences and 13 nuclear genomic microsatellite loci (Kindler et al 2013(Kindler et al , 2017(Kindler et al , 2018aKindler and Fritz 2018;Pokrant et al 2016;Asztalos et al 2020Asztalos et al , 2021aSchultze et al 2019Schultze et al , 2020 to examine 683 grass snakes and 332 dice snakes from our immediate study region and beyond. We also reassess the status of N. megalocephala Orlov and Tuniyev, 1987 based on nuclear genomic microsatellite loci.…”