Skip to main content

Advertisement

Log in

Phylogeography of the Ibero-Maghrebian red-eyed grass snake (Natrix astreptophora)

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

We examined phylogeographic differentiation of the red-eyed grass snake (Natrix astreptophora) using 1984 bp of mtDNA and 13 microsatellite loci from specimens collected across its distribution range in southwestern Europe and northwestern Africa. Based on phylogenetic analyses of mtDNA, European N. astreptophora constituted the sister clade to a weakly supported North African clade comprised of two deeply divergent and well-supported clades, one corresponding to Moroccan snakes and the other to snakes from Algeria and Tunisia. This tripartite differentiation was confirmed by analyses of microsatellite loci. According to a fossil-calibrated molecular clock, European and North African N. astreptophora diverged 5.44 million years ago (mya), and the two Maghrebian clades split 4.64 mya. These dates suggest that the radiation of the three clades was initiated by the environmental changes related to the Messinian Salinity Crisis and the reflooding of the Mediterranean Basin. The differentiation of N. astreptophora, with distinct clades in the Iberian Peninsula and in the western and eastern Maghreb, corresponds to a general phylogeographic paradigm and resembles the differentiation found in another co-distributed Natrix species, the viperine snake (N. maura). Despite both species being good swimmers, the Strait of Gibraltar constitutes a significant biogeographic barrier for them. The discovery that North Africa harbours two endemic lineages of N. astreptophora necessitates more conservation efforts for these imperilled snakes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Barata, M., Harris, D. J., & Castilho, R. (2008). Comparative phylogeography of northwest African Natrix maura (Serpentes: Colubridae) inferred from mtDNA sequences. African Zoology, 43, 1–7.

    Article  Google Scholar 

  • Blouin-Demers, G., & Gibbs, H. L. (2003). Isolation and characterization of microsatellite loci in the black rat snake (Elaphe obsoleta). Molecular Ecology Notes, 3, 98–99.

    Article  CAS  Google Scholar 

  • Bons, J., & Geniez, P. (1996). Amphibiens et reptiles du Maroc (Sahara Occidental compris). Atlas biogéographique. Barcelona: AHE.

    Google Scholar 

  • Burns, E. L., & Houlden, B. A. (1999). Isolation and characterization of microsatellite markers in the broad-headed snake Hoplocephalus bungaroides. Molecular Ecology, 8, 520–521.

    CAS  Google Scholar 

  • Carranza, S., Arnold, E. N., Wade, E., & Fahd, S. (2004). Phylogeography of the false smooth snakes, Macroprotodon (Serpentes, Colubridae): mitochondrial DNA sequences show European populations arrived recently from Northwest Africa. Molecular Phylogenetics and Evolution, 33, 523–532.

    Article  CAS  PubMed  Google Scholar 

  • Carranza, S., Arnold, E. N., & Pleguezuelos, J. M. (2006). Phylogeny, biogeography, and evolution of two Mediterranean snakes, Malpolon monspessulanus and Hemorrhois hippocrepis (Squamata, Colubridae), using mtDNA sequences. Molecular Phylogenetics and Evolution, 40, 532–546.

    Article  CAS  PubMed  Google Scholar 

  • Clement, M., Posada, D., & Crandall, K. A. (2000). tcs: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1660.

    Article  CAS  PubMed  Google Scholar 

  • Delfino, M., Bailon, S., & Pitruzella, G. (2011). The Late Pliocene amphibians and reptiles from “Capo Mannu D1 Local Fauna” (Mandriola, Sardinia, Italy). Geodiversitas, 33, 357–382.

    Article  Google Scholar 

  • Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with beauti and the beast 1.7. Molecular Biology and Evolution, 29, 1969–1973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier, L., & Lischer, H. E. L. (2010). arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.

    Article  PubMed  Google Scholar 

  • Fritz, U., Barata, M., Busack, S. D., Fritzsch, G., & Castilho, R. (2006). Impact of mountain chains, sea straits and peripheral populations on genetic and taxonomic structure of a freshwater turtle, Mauremys leprosa. Zoologica Scripta, 35, 97–108.

    Article  Google Scholar 

  • Fritz, U., Corti, C., & Päckert, M. (2012). Mitochondrial DNA sequences suggest unexpected phylogenetic position of Corso-Sardinian grass snakes (Natrix cetti) and do not support their species status, with notes on phylogeography and subspecies delineation of grass snakes. Organisms, Diversity & Evolution, 12, 71–80.

    Article  Google Scholar 

  • Garner, T. W. J., Gregory, P. T., McCracken, G. F., Burghardt, G. M., Koop, B. F., McLain, S. E., & Nelson, R. J. (2002). Geographic variation of multiple paternity in the common garter snake (Thamnophis sirtalis). Copeia, 2002, 15–23.

    Article  Google Scholar 

  • Gautschi, B., Widmer, A., & Koella, J. (2000). Isolation and characterization of microsatellite loci in the dice snake (Natrix tessellata). Molecular Ecology, 9, 2192–2193.

    Article  Google Scholar 

  • Guicking, D., Lawson, R., Joger, U., & Wink, M. (2006). Evolution and phylogeny of the genus Natrix (Serpentes: Colubridae). Biological Journal of the Linnean Society, 87, 127–143.

    Article  Google Scholar 

  • Guicking, D., Joger, U., & Wink, M. (2008). Molecular phylogeography of the viperine snake Natrix maura (Serpentes: Colubridae): evidence for strong intraspecific differentiation. Organisms, Diversity & Evolution, 8, 130–145.

    Article  Google Scholar 

  • Hecht, G. (1930). Systematik, Ausbreitungsgeschichte und Ökologie der europäischen Arten der Gattung Tropidonotus (Kuhl) H. Boie. Mitteilungen aus dem Zoologischen Museum Berlin, 16, 244–393.

    Google Scholar 

  • Husemann, M., Schmitt, T., Zachos, F. E., Ulrich, W., & Habel, J. C. (2014). Palaearctic biogeography revisited: evidence for the existence of a north African refugium for Western Palaearctic biota. Journal of Biogeography, 41, 81–94.

    Article  Google Scholar 

  • Jombart, T. (2008). adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403–1405.

    Article  CAS  PubMed  Google Scholar 

  • Kabisch, K. (1999). Natrix natrix (Linnaeus, 1758) – Ringelnatter. In W. Böhme (Ed.), Handbuch der Reptilien und Amphibien Europas. Band 3/IIA: Schlangen II (pp. 513–580). Aula: Wiebelsheim.

    Google Scholar 

  • Kindler, C., Böhme, W., Corti, C., Gvoždík, V., Jablonski, D., Jandzik, D., Metallinou, M., Široký, P., & Fritz, U. (2013). Mitochondrial phylogeography, contact zones and taxonomy of grass snakes (Natrix natrix, N. megalocephala). Zoologica Scripta, 42, 458–472.

    Article  Google Scholar 

  • Kindler, C., Chèvre, M., Ursenbacher, S., Böhme, W., Hille, A., Jablonski, D., Vamberger, M., & Fritz, U. (2017). Hybridization patterns in two contact zones of grass snakes reveal a new Central European snake species. Scientific Reports, 7, 7378.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar, S., Stecher, G., & Tamura, K. (2016). mega7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.

    Article  CAS  PubMed  Google Scholar 

  • Lacepède, B.-G.-É. (1789). Histoire naturelle des quadrupèdes ovipares et des serpens, vol. 2 (Histoire naturelle des serpens). Paris: Hôtel de Thou.

  • Lanfear, R., Calcott, B., Ho, S. Y. W., & Guindon, S. (2012). partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.

    Article  CAS  PubMed  Google Scholar 

  • Linnaeus, C. (1758). Systema Naturae per regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis. Tomus I. Regnum Animale. Editio Decima. Stockholm: Laurentius Salvius.

  • Martínez-Freiría, F., Crochet, P.-A., Fahd, S., Geniez, P., Brito, J. C., & Velo-Antón, G. (2017). Integrative phylogeographic and ecological analyses reveal multiple Pleistocene refugia for Mediterranean Daboia vipers in north-west Africa. Biological Journal of the Linnean Society, 122, 366–384.

    Article  Google Scholar 

  • Meister, B., Armbruster, F. J., Frauenfelder, N., & Bauer, B. (2009). Novel microsatellite loci in the grass snake (Natrix natrix) and cross-amplification in the dice snake (Natrix tessellata). Molecular Ecology Resources, 9, 604–606.

    Article  CAS  PubMed  Google Scholar 

  • Nicolas, V., Mataame, A., Crochet, P.-A., Geniez, P., & Ohler, A. (2015). Phylogeographic patterns in North African water frog Pelophylax saharicus (Anura: Ranidae). Journal of Zoological Systematics and Evolutionary Research, 53, 239–248.

    Article  Google Scholar 

  • Pokrant, F., Kindler, C., Ivanov, M., Cheylan, M., Geniez, P., Böhme, W., & Fritz, U. (2016). Integrative taxonomy provides evidence for the species status of the Ibero-Maghrebian grass snake Natrix astreptophora. Biological Journal of the Linnean Society, 118, 873–888.

    Article  Google Scholar 

  • Prosser, M. R., Gibbs, H. L., & Weatherhead, P. J. (1999). Microgeographic population genetic structure in the northern water snake, Nerodia sipedon sipedon detected using microsatellite DNA loci. Molecular Ecology, 8, 329–333.

    Article  CAS  PubMed  Google Scholar 

  • Recuero, E., Iraola, A., Rubio, X., Machordom, A., & García-Paris, M. (2007). Mitochondrial differentiation and biogeography of Hyla meridionalis (Anura: Hylidae): an unusual phylogeographical pattern. Journal of Biogeography, 34, 1207–1219.

    Article  Google Scholar 

  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Roveri, M., Flecker, R., Krijgsman, W., Lofi, J., Lugli, S., Manzi, V., Sierro, F. J., Bertini, A., Camerlenghi, A., De Lange, G., & Govers, R. (2014). The Messinian Salinity Crisis: past and future of a great challenge for marine sciences. Marine Geology, 352, 25–58.

    Article  Google Scholar 

  • Santos, X., Rato, C., Carranza, S., Carretero, M. A., & Pleguezuelos, J. M. (2012). Complex phylogeography in the southern smooth snake (Coronella girondica) supported by mtDNA sequences. Journal of Zoological Systematics and Evolutionary Research, 50, 210–219.

    Article  Google Scholar 

  • Schleich, H. H., Kästle, W., & Kabisch, K. (1996). Amphibians and reptiles of North Africa. Königstein: Koeltz Scientific Publishers.

    Google Scholar 

  • Seoane, V. L. (1884). Identidad de Lacerta schreiberi (Bedriaga) y Lacerta viridis var. gadovi (Boulenger) e investigaciones herpetológicas de Galicia. A Coruña: Vicente Abad.

    Google Scholar 

  • Sindaco, R., Venchi, A., & Grieco, C. (2013). The reptiles of the Western Palearctic, volume 2: Annotated checklist and distributional atlas of the snakes of Europe, North Africa, Middle East and Central Asia, with an update to volume 1. Latina: Edizioni Belvedere.

    Google Scholar 

  • Sloss, B. L., Schuurman, G. W., Paloski, R. A., Boyle, O. D., & Kapfer, J. M. (2012). Novel microsatellite loci for studies of Thamnophis gartersnake genetic identity and hybridization. Conservation Genetics Resources, 4, 383–386.

    Article  Google Scholar 

  • Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stuckas, H., Velo-Antón, G., Fahd, S., Kalboussi, M., Rouag, R., Arculeo, M., Marrone, F., Sacco, F., Vamberger, M., & Fritz, U. (2014). Where are you from, stranger? The enigmatic biogeography of North African pond turtles (Emys orbicularis). Organisms, Diversity & Evolution, 14, 295–306.

    Article  Google Scholar 

  • Veith, M., Mayer, C., Samraoui, B., Donaire Barroso, D., & Bogaerts, S. (2004). From Europe to Africa and vice versa: evidence for multiple intercontinental dispersal in ribbed salamanders (genus Pleurodeles). Journal of Biogeography, 31, 159–171.

    Article  Google Scholar 

  • Velo-Antón, G., Godinho, R., Harris, D. J., Santos, F., Martínez-Freiría, F., Fahd, S., Larbes, S., Pleguezuelos, J. M., & Brito, J. C. (2012). Deep evolutionary lineages in a Western Mediterranean snake (Vipera latastei/monticola group) and high genetic structuring in Southern Iberian populations. Molecular Phylogenetics and Evolution, 65, 965–973.

    Article  PubMed  Google Scholar 

  • Velo-Antón, G., Pereira, P., Fahd, S., Teixeira, J., & Fritz, U. (2015). Out of Africa: did Emys orbicularis occidentalis cross the Strait of Gibraltar twice? Amphibia-Reptilia, 36, 133–140.

    Article  Google Scholar 

  • Veríssimo, J., Znari, M., Stuckas, H., Fritz, U., Pereira, P., Teixeira, J., Arculeo, M., Marrone, F., Sacco, F., Naimi, M., Kehlmaier, C., & Velo-Antón, G. (2016). Pleistocene diversification in Morocco and recent demographic expansion in the Mediterranean pond turtle Mauremys leprosa. Biological Journal of the Linnean Society, 119, 943–959.

    Article  Google Scholar 

  • Zazo, C. (1999). Interglacial sea levels. Quaternary International, 55, 101–113.

    Article  Google Scholar 

Download references

Acknowledgements

Markus Auer, José Carlos Brito, Pierre-André Crochet, Boualem Dellaoui, Marco Favelli, Daniel Jablonski, Jérôme Maran, Olivier Peyre, and Ulrich Scheidt donated samples. Philippe Evrard provided a photo of a red-eyed grass snake from Spain. Cäcilia Spitzweg helped with laboratory work.

Funding

This study was funded by the German Research Foundation (DFG; FR 1435/11-2). Menad Beddek’s PhD research was supported by a grant from ANRT/Naturalia Environnement CIFRE (no. 2013/0145); field work in Algeria was funded by Naturalia Environnement. Salvador Carranza’s work was funded by CGL2015-70390-P from the Ministerio de Economía y Competitividad, Spain (cofunded by FEDER).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Uwe Fritz.

Electronic supplementary material

ESM 1

(PDF 1.24 mb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kindler, C., de Pous, P., Carranza, S. et al. Phylogeography of the Ibero-Maghrebian red-eyed grass snake (Natrix astreptophora). Org Divers Evol 18, 143–150 (2018). https://doi.org/10.1007/s13127-017-0354-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-017-0354-2

Keywords

Navigation