Skip to main content

Advertisement

SpringerLink
Log in

Conservation genetics of a wide-ranged temperate snake: same species, different locations, and different behaviour

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Even though reptiles are threatened worldwide, few studies address their conservation, especially snakes. The goal of our study was to measure the genetic structure of a widely distributed temperate reptile, the smooth snake Coronella austriaca using microsatellite markers in two different areas at the core (Alsace, north-eastern France) and at the edge (Wallonia, southern Belgium) of its range. We sampled 506 individuals in 38 localities (respectively 10 and 28). Analysis of genetic structure conducted with a clustering method detected three clusters in Alsace, one group gathering all populations but two. In Wallonia, differentiation was observed on both sides of the Meuse River and in the Southern Ardenne region (southernmost sampling sites). Spatial autocorrelation analysis showed that statisticaly more related individuals occur together up to a distance of 2.8 km in Alsace and up to 10 km in Wallonia. Isolation by distance was detected in Wallonia but the distance explained a very limited part of the differentiation (r = 0.033), whereas no isolation-by-distance pattern was detected in Alsace. Even though genetic differentiation between populations separated by large rivers, highways, or crop fields was detected, dispersal between populations seem currently sufficient to avoid any kind of genetic drift in both regions. These results are similar to a previous study conducted in Poland, but strongly contrast with another analysis held in England which detected a sharp genetic structuring among populations that are geographically close. We consequently suggest that discrepancies could be related to the ecology of island populations and smaller densities.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

All DNA samples are deposited in the Natural History Museum Bern, Switzerland.

References

  • Andrews KM, Gibbons JW (2005) How do highways influence snake movement? Behavioral responses to roads and vehicles. Copeia 2005:772–782. https://doi.org/10.1643/0045-8511(2005)005[0772:HDHISM]2.0.CO;2

    Article  Google Scholar 

  • Böhme M, SchneeweiĂź N, Fritz U et al (2007) Small edge populations at risk: genetic diversity of the green lizard (Lacerta viridis viridis) in Germany and implications for conservation management. Conserv Genet 8:555–563

    Article  Google Scholar 

  • Bond JM, Porteous R, Hugues S et al (2005) Polymorphic microsatellite markers, isolated using a simple enrichment procedure, in the threatened smooth snake (Coronella austriaca). Mol Ecol Notes 5:42–44

    Article  CAS  Google Scholar 

  • Bonnet X, Naulleau G, Shine R (1999) The dangers of leaving home: dispersal and mortality in snakes. Biol Conserv 89:39–50. https://doi.org/10.1016/S0006-3207(98)00140-2

    Article  Google Scholar 

  • Carrier JA, Beebee TJC (2003) Recent, substantial, and unexplained declines of the common toad Bufo bufo in lowland England. Biol Conserv 111:395–399. https://doi.org/10.1016/S0006-3207(02)00308-7

    Article  Google Scholar 

  • Ceballos G, Ehrlich PR, Barnosky AD, et al (2015) Accelerated modern human–induced species losses: Entering the sixth mass extinction. Sci Adv 1:

  • Clobert J, Baguette M, Benton TG, Bullock JM (2012) Dispersal ecology and evolution. Oxford University Press, Oxford

    Book  Google Scholar 

  • Collins JP, Crump ML (2009) Extinction in our times: global amphibian decline. Oxford University Press, Oxford

  • Corbett K (1989) Conservation of European amphibians and reptiles. Christopher Helm, London

    Google Scholar 

  • Cox NA, Temple HJ (2009) European red list of reptiles

  • Desvars-Larrive A, Pascal M, Gasqui P et al (2017) Population genetics, community of parasites, and resistance to rodenticides in an urban brown rat (Rattus norvegicus) population. PLoS ONE 12:e0184015. https://doi.org/10.1371/journal.pone.0184015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dick DCD, Mebert K (2017) Between housing and deep forest: long-term population biology and dispersal of suburban Smooth snakes (Coronella austriaca). Zool Anz 270:98–106. https://doi.org/10.1016/j.jcz.2017.09.007

    Article  Google Scholar 

  • Dixo M, Metzger JP, Morgante JS, Zamudio KR (2009) Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian Atlantic Coastal Forest. Biol Conserv 142:1560–1569

    Article  Google Scholar 

  • Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20. https://doi.org/10.18637/jss.v022.i04

  • Driscoll DA (2004) Extinction and outbreaks accompany fragmentation of a reptile community. Ecol Appl 14:220–240

    Article  Google Scholar 

  • Dubey S, Sumner J, Pike DA et al (2011) Genetic connectivity among populations of an endangered snake species from southeastern Australia (Hoplocephalus bungaroides, Elapidae). Ecol Evol 1:218–227. https://doi.org/10.1002/ece3.25

    Article  PubMed  PubMed Central  Google Scholar 

  • Dudaniec RY, Spear SF, Richardson JS, Storfer A (2012) Current and historical drivers of landscape genetic structure differ in core and peripheral salamander populations. PLoS ONE 7:e36769

  • Ferchaud AL, Lyet A, Cheylan M et al (2011) High genetic differentiation among french populations of the orsini’s viper (Vipera ursinii ursinii) based on mitochondrial and microsatellite data: Implications for conservation management. J Hered 102:67–78. https://doi.org/10.1093/jhered/esq098

    Article  CAS  PubMed  Google Scholar 

  • Foden WB, Butchart SHM, Stuart SN, et al (2013) Identifying the world’s most climate change vulnerable species: a systematic trait-based assessment of all birds, amphibians and corals. PLoS ONE 8:e65427

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Gibbons JW, Scott DE, Ryan TJ et al (2000) The global decline of reptiles, dĂ©jĂ  vu amphibians. Bioscience 50:653–666

    Article  Google Scholar 

  • Gibbs HL, Prior KA, Weatherhead PJ, Johnson G (1997) Genetic structure of populations of the threatened eastern massasauga rattlesnake, Sistrurus c. catenatus: evidence from microsatellite DNA markers. Mol Ecol 6:1123–1132

    Article  CAS  Google Scholar 

  • Gill J, Langston R, Alves JA et al (2007) Contrasting trends in two Black-tailed Godwit populations: a review of causes and recommendations. Wader Study Gr Bull 114:43–50

    Google Scholar 

  • Goudet J (1995) Fstat version 1.2: a computer program to calculate Fstatistics. J Hered 86:485–486

    Article  Google Scholar 

  • Graitson E, Hussin J, Vacher J-P (2012) Synthèse de 24 annĂ©es de suivi d’une communautĂ© de reptiles typiques du nord de l’Europe. Bull La SociĂ©tĂ© HerpĂ©tologique Fr 141:63–81

    Google Scholar 

  • Guicking D, Herzberg A, Wink M (2004) Population genetics of the Dice Snake (Natrix tessellata) in Germany: implications for conservation. Salamandra 40:217–234

    Google Scholar 

  • Guiller G (2009) DĂ©clin et biologie d’une population de Zamenis longissimus (Laurenti, 1768) (Serpentes, Colubridae) en Loire-Atlantique. Bull La SociĂ©tĂ© HerpĂ©tologique Fr 132:85–114

    Google Scholar 

  • Guiller G, Legentilhomme J (2006) Impact des pratiques agricoles sur une population de Vipera berus (Linnaeus, 1758) (Ophidia, Viperidae) en Loire-Atlantique. Bull La SociĂ©tĂ© Sci Nat L’ouest La Fr Nouv SĂ©rie 28:73–81

    Google Scholar 

  • Guillot G, Mortier F, Estoup A (2005) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715. https://doi.org/10.1111/j.1471-8286.2005.01031.x

    Article  CAS  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDI: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Howard C, Flather CH, Stephens PA (2020) A global assessment of the drivers of threatened terrestrial species richness. Nat Commun 11:1–10. https://doi.org/10.1038/s41467-020-14771-6

    Article  CAS  Google Scholar 

  • IUCN (2020) The IUCN Red List of Threatened Species. Version 2020–2. https://www.iucnredlist.org. Accessed 1 Oct 2020

  • Jablonski D, Nagy ZT, Avcı A et al (2019) Cryptic diversity in the smooth snake (Coronella austriaca). Amphibia-Reptilia 40:179–192. https://doi.org/10.1163/15685381-20181025

    Article  Google Scholar 

  • Keogh JS, Webb JK, Shine R (2007) Spatial genetic analysis and long-term mark-recapture data demonstrate male-biased dispersal in a snake. Biol Lett 3:33–35

    Article  Google Scholar 

  • Kyek M, Kaufmann PH, Lindner R (2017) Differing long term trends for two common amphibian species (Bufo bufo and Rana temporaria) in alpine landscapes of Salzburg, Austria. PLoS ONE 12:e0187148–e0187148. https://doi.org/10.1371/journal.pone.0187148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lane A, Shine R (2011) Intraspecific variation in the direction and degree of sex-biased dispersal among sea-snake populations. Mol Ecol 20:1870–1876. https://doi.org/10.1111/j.1365-294X.2011.05059.x

    Article  PubMed  Google Scholar 

  • Loiseau N, Mouquet N, Casajus N et al (2020) Global distribution and conservation status of ecologically rare mammal and bird species. Nat Commun 11:5071. https://doi.org/10.1038/s41467-020-18779-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madsen T, Stille B, Shine R (1996) Inbreeding depression in an isolated population of adders Vipera berus. Biol Conserv 75:113–118. https://doi.org/10.1016/0006-3207(95)00067-4

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Meeus S, Honnay O, Jacquemyn H (2012) Strong differences in genetic structure across disjunct, edge, and core populations of the distylous forest herb Pulmonaria officinalis (Boraginaceae). Am J Bot 99:1809–1818

    Article  Google Scholar 

  • Moran PAP (1950) Notes on the continuous stochastic phenomena. Biometrika 37:17–23

    Article  CAS  Google Scholar 

  • Mullin SJ, Seigel RA (2009) Snakes. Ecology and Conservation. Cornell University Press, Ithaca

    Google Scholar 

  • Munwes I, Geffe E, Roll U et al (2010) The change in genetic diversity down the core-edge gradient in the eastern spadefoot toad (Pelobates syriacus). Mol Ecol 19:2675–2689

    Article  CAS  Google Scholar 

  • Orme CDL, Mayor S, dos Anjos L et al (2019) Distance to range edge determines sensitivity to deforestation. Nat Ecol Evol 3:886–891. https://doi.org/10.1038/s41559-019-0889-z

    Article  PubMed  Google Scholar 

  • Pattishall A, Cundall D (2008) Spatial biology of northern watersnakes (Nerodia sipedon) living along an urban stream. Copeia 2008:752–762

    Article  Google Scholar 

  • Pauls SU, Nowak C, Bálint M, Pfenninger M (2013) The impact of global climate change on genetic diversity within populations and species. Mol Ecol 22:925–946. https://doi.org/10.1111/mec.12152

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  • Pernetta AP, Allen JA, Beebee TJC, Reading CJ (2011) Fine-scale population genetic structure and sex-biased dispersal in the smooth snake (Coronella austriaca) in southern England. Heredity (edinb) 107:231–238

    Article  CAS  Google Scholar 

  • Peterman WE, Feist SM, Semlitsch RD, Eggert LS (2013) Conservation and management of peripheral populations: spatial and temporal influences on the genetic structure of wood frogs (Rana sylvatica) populations. Biol Conserv 158:351–358

    Article  Google Scholar 

  • Pimm SL, Jenkins CN, Abell R, et al (2014) The biodiversity of species and their rates of extinction, distribution, and protection. Science (80- ) 344:1246752

  • Pounds JA, Crump ML (1994) Amphibian declines and climate disturbance: the case of the golden toad and the harlequin frog. Conserv Biol 8:72–85

    Article  Google Scholar 

  • R Development Core Team (2016) R: a language and environment for statistical computing. R Found. Stat. Comput. Vienna Austria

  • Reading C, JofrĂ© G (2020) Smooth snake population decline and its link with prey availability. Amphibia-Reptilia 41:43–48

    Article  Google Scholar 

  • Reading CJ, Luiselli LM, Akani GC et al (2010) Are snake populations in widespread decline? Biol Lett 6:777–780

    Article  CAS  Google Scholar 

  • Rosenberg K V., Dokter AM, Blancher PJ, et al (2019) Decline of the North American avifauna. Science (80- ) 366:120–124

  • Rousset F (1997) Genetic differentiation and estimation of gene flow F-statistics under isolation by distance. Genetics 145:1219–1228

    Article  CAS  Google Scholar 

  • Sánchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: a review of its drivers. Biol Conserv 232:8–27. https://doi.org/10.1016/J.BIOCON.2019.01.020

    Article  Google Scholar 

  • Sauer A (1994) Methode zur Identifizierung der Schlingnatter (Coronella austriaca). Salamandra 30:43–47

    Google Scholar 

  • Sauer A (1997) Fotografische Individualidentifikation und erste Ergebnisse zur Langzeitbeobachtung einer Schlingnatterpopulation (Coronella austriaca). Mertensiella 7:103–110

    Google Scholar 

  • Sillero N, Campos J, Bonardi A et al (2014) Updated distribution and biogeography of amphibians and reptiles of Europe. Amphibia-Reptilia 35:1–31. https://doi.org/10.1163/15685381-00002935

    Article  Google Scholar 

  • Sokal RR, Wartemberg DE (1983) A test of spatial autocorrelation analysis using an isolation-by-distance model. Genetics 105:219–237

    Article  CAS  Google Scholar 

  • Stuart S, Hoffmann M, Chanson J, et al (2008) Threatened amphibians of the world. Lynx Edicions; IUCN; Conservation International. 758 pp., Barcelona, Spain, Gland, Switzerland, Arlington, Virginia, USA

  • Studds CE, Kendall BE, Murray NJ et al (2017) Rapid population decline in migratory shorebirds relying on Yellow Sea tidal mudflats as stopover sites. Nat Commun 8:1–7. https://doi.org/10.1038/ncomms14895

    Article  CAS  Google Scholar 

  • Sztencel-Jablonka A, Mazgajski TD, Bury S et al (2015) Phylogeography of the smooth snake Coronella austriaca (Serpentes: Colubridae): evidence for a reduced gene pool and a genetic discontinuity in Central Europe. Biol J Linn Soc 115:195–210. https://doi.org/10.1111/bij.12496

    Article  Google Scholar 

  • Taubmann J, Theissinger K, Feldheim KA et al (2011) Modelling range shifts and assessing genetic diversity distribution of the montane aquatic mayfly Ameletus inopinatus in Europe under climate change scenarios. Conserv Genet 12:503–515. https://doi.org/10.1007/s10592-010-0157-x

    Article  Google Scholar 

  • Ursenbacher S, Monney J-C, Fumagalli L (2009) Limited genetic diversity and high differentiation among the remnant adder (Vipera berus) populations in the Swiss and French Jura Mountains. Conserv Genet 10:303–315

    Article  Google Scholar 

  • Ursenbacher S, Guillon M, Cubizolle H et al (2015) Postglacial recolonization in a cold climate specialist in western Europe: patterns of genetic diversity in the adder (Vipera berus) support the central–marginal hypothesis. Mol Ecol 24:3639–3651. https://doi.org/10.1111/mec.13259

    Article  PubMed  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Völkl W, Käsewieter D (2003) Die Schlingnatter. Laurenti Verlag, Bielefeld

    Google Scholar 

  • Wagner N, Rödder D, BrĂĽhl CA, et al (2014) Evaluating the risk of pesticide exposure for amphibian species listed in Annex II of the European Union Habitats Directive. Biol Conserv 176:64–70. https://doi.org/10.1016/j.biocon.2014.05.014

  • Weihmann F, Weihmann S, Weihmann T (2019) Conservation genetic analysis of a Central-European range-margin population of the yellow-bellied toad (Bombina v. variegata). Conserv Genet 20:557–569. https://doi.org/10.1007/s10592-019-01156-6

    Article  Google Scholar 

  • Zipkin EF, DiRenzo G V., Ray JM, et al (2020) Tropical snake diversity collapses after widespread amphibian loss. Science (80- ) 367:814–816. https://doi.org/10.1126/science.aay5733

Download references

Acknowledgements

We are grateful to the following people for providing help on the field and in the lab: Nicolas Boileau, Gaël Fellet, Charles Huyttenhoven, Charlotte Mathelart, Barbara Meister, Victoria Michel, Daniel Muller, Eric Pellerin†, Matthieu Raemy, Laurent Schwebel†, Jacques Thiriet. We also thank three anonymous referees for their useful comments that helped improve the quality of this article. We would like to dedicate this article to the memory of Laurent Schwebel, a dear friend and fellow naturalist who passed away in 2012 and whose help on the field was invaluable, and to the memory of Eric Pellerin who helped us collect data in Belgium.

Funding

This study benefited of the support of the “Département de l'Etude du Milieu Naturel et Agricole du Service Public de Wallonie”.

Author information

Authors and Affiliations

  1. Association BUFO, Musée d’Histoire naturelle et d’Ethnographie, 11 rue de Turenne, 68000, Colmar, France

    Jean-Pierre Vacher

  2. Section of Conservation Biology, Department of Environmental Sciences, University of Basel, St. Johanns-Vorstadt 10, 4056, Basel, Switzerland

    Jean-Pierre Vacher, Julie Cauwenbergh & Sylvain Ursenbacher

  3. DĂ©partement Etudes, Association Natagora, Traverses des Muses, 1, 5000, Namur, Belgium

    Eric Graitson

  4. Section of Conservation Biology, University of Liège, Sart Tilman B22, 4000, Liège, Belgium

    Eric Graitson

  5. Info Fauna - Karch, University of Neuchâtel, Avenue de Bellevaux 51, 2000, Neuchâtel, Switzerland

    Sylvain Ursenbacher

  6. Balaton Limnological Research Institute, Klebelsberg K. 3, Tihany, 8237, Hungary

    Sylvain Ursenbacher

Authors
  1. Jean-Pierre Vacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eric Graitson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julie Cauwenbergh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sylvain Ursenbacher
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JPV, EG, JC, and SU designed the study and wrote the manuscript. JPV did the field work in Alsace and the subsequent lab work. EG and JC did the field work in Wallonia. JPV, JC, and SU analysed the data.

Corresponding author

Correspondence to Jean-Pierre Vacher.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest in the scope of this study.

Consent to participate

All authors approved to participate to this study.

Consent to publish

All authors approved to the publication of this study.

Research involving in animal rights

Permits (no reference number provided) were delivered by the Prefect of Alsace to J.-P. Vacher, and by the department of Nature and Forest from Wallonia Public Service to E. Graitson for capture and handling of Coronella austriaca. Snakes were captured and released on spot right after sampling, no other tissue/blood collection has been performed other than buccal swabbing. A permit to drive on forest tracks in the Haut-Rhin department was issued to J.-P. Vacher by the National Forest Department (Mr. Pierrat, Mulhouse, France).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vacher, JP., Graitson, E., Cauwenbergh, J. et al. Conservation genetics of a wide-ranged temperate snake: same species, different locations, and different behaviour. Conserv Genet 23, 167–177 (2022). https://doi.org/10.1007/s10592-021-01416-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-021-01416-4

Keywords

Search

Navigation