Integrative taxonomy provides evidence for the species status of the Ibero-Maghrebian grass snakeNatrix astreptophora

Abstract

The grass snake (Natrix natrix) is Europe's most widely distributed and, in many regions, most common snake species, with many morphologically defined subspecies. Yet, the taxonomy of grass snakes is relatively little studied and recent work has shown major conflicts between morphologically defined subspecies and phylogeographical differentiation. Using external morphology, osteological characters, and information from 13 microsatellite loci and two mitochondrial markers, we examine differentiation of the subspecies N. n. astreptophora from the North African Maghreb region, the Iberian Peninsula and neighbouring France. According to previous studies, N. n. astreptophora corresponds to a deeply divergent mitochondrial clade and constitutes the sister taxon of all remaining grass snakes. In the French Pyrenees region, there is a contact zone of N. n. astreptophora with another subspecies, N. n. helvetica. Our analyses of microsatellites and mitochondrial DNA reveal that the distribution ranges of the two taxa abut there, but both hybridize only exceptionally. Even though many morphological characters are highly variable and homoplastic in grass snakes, N. n. astreptophora differs consistently from all other grass snakes by its reddish iris coloration and in having significantly fewer ventral scales and another skull morphology. Considering further the virtual absence of gene flow between N. n. astreptophora and N. n. helvetica, and acknowledging the morphological distinctiveness of N. n. astreptophora and its sister group relationship to all remaining subspecies of grass snakes, we conclude that Natrix astreptophora (Seoane, 1884) should be recognized as a distinct species. Further research is needed to explore whether N. astreptophora is polytypic because a single sample of N. astreptophora from Tunisia turned out to be genetically highly distinct from its European conspecifics.

Distribution and hybridisation of barred and common grass snakes (Natrix helvetica, N. natrix) in Baden-Württemberg, South-western Germany

“…As nuclear genomic markers, 13 informative polymorphic microsatellite loci were used to genotype the same samples. Laboratory approaches were described in detail in Kindler et al (2013) and Pokrant et al (2016). For embedding the genetic variation within Baden-Württemberg into a broader framework, data for additional 421 grass snakes from adjacent regions in the Czech Republic, France, Germany, and Switzerland were included in all calculations (Suppl.…”

“…Grass snakes were, until recently, thought to represent a widespread species distributed from North-western Africa and the Iberian Peninsula across much of Western, Central, Northern and Eastern Europe into Central Asia (Kabisch 1999). Genetic investigations revealed three deeply divergent genealogical lineages without or with very restricted, unidirectional gene flow and prompted the recognition of three distinct species (Kindler et al 2013(Kindler et al , 2014(Kindler et al , 2017(Kindler et al , 2018aPokrant et al 2016). According to these investigations, the red-eyed grass snake, Natrix astreptophora (Seoane, 1884), occurs in North-western Africa, the Iberian Peninsula and South-western France.…”

“…Its range abuts in the French pre-Pyrenean region that of the barred grass snake Natrix helvetica (Lacepède, 1789). Hybridisation is very rare, and the distribution of the two species seems to be mutually exclusive (Pokrant et al 2016). Natrix helvetica is a polytypic species (Kindler and Fritz 2018) distributed over France, the Benelux countries, Great Britain, Switzerland, Western Germany, and Italy.…”

Phylogeny of the Eurasian Wren Nannus troglodytes (Aves: Passeriformes: Troglodytidae) reveals deep and complex diversification patterns of Ibero-Maghrebian and Cyrenaican populations

“…The latter stretches from the northernmost part of the Western Sahara Territory over Morocco and northern Algeria to Tunisia [14,15]. The IMR has previously been described in different scientific contexts, such as seismotectonics [16][17][18] and biogeography [19][20][21][22][23]. It furthermore includes the three Biodiversity sub-Hotspots of the High and Middle Atlas, the Baetic-Rifan mountain complex, and Kabylia-Numidia-Kroumire and is neighboured by the Mediterranean Cyrenaica of northeast Libya [9,12].…”

Patterns of gene flow across multiple anthropogenic infrastructures: Insights from a multi-species approach

“…Care was taken to minimise animal handling and stress and all individuals were rapidly released at the place of capture after manipulation. We amplified 13 (Pokrant et al, 2016), 14 (Tobler et al, 2013; Maia-Carvalho et al, 2014), 15 (Richard et al, 2015) and 14 (Marcus et al, 2013) polymorphic microsatellite loci in N. helvetica , A. obstetricans , M. jurtina and A. parallelepipedus , respectively. For a detailed procedure of DNA extraction, amplification and genotyping, see Appendix 1.…”