Skip to main content

Advertisement

Log in

Limited genetic diversity and high differentiation among the remnant adder (Vipera berus) populations in the Swiss and French Jura Mountains

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

Abstract

Although the adder (Vipera berus) has a large distribution area, this species is particularly threatened in Western Europe due to high habitat fragmentation and human persecution. We developed 13 new microsatellite markers in order to evaluate population structure and genetic diversity in the Swiss and French Jura Mountains, where the species is limited to only a few scattered populations. We found that V. berus exhibits a considerable genetic differentiation among populations (global FST = 0.269), even if these are not geographically isolated. Moreover, the genetic diversity within populations in the Jura Mountains and in the less perturbed Swiss Alps is significantly lower than in other French populations, possibly due to post-glacial recolonisation processes. Finally, in order to minimize losses of genetic diversities within isolated populations, suggestions for the conservation of this species in fragmented habitats are proposed.

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

Access this article

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

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations, 1st edn. Blackwell Publishing Ltd, Malden, MA, USA

    Google Scholar 

  • Bartley D, Bagley M, Gall G et al (1992) Use of linkage disequilibrium data to estimate effective size of hatchery and natural fish populations. Conserv Biol 6:365–375

    Article  Google Scholar 

  • Bonnet X, Naulleau G (1996) Catchability in snakes: consequences for estimates of breeding frequency. Can J Zool 74:233–239

    Google Scholar 

  • Brassel KE, Reif D (1979) A procedure to generate Thiessen polygons. Geogr Anal 325:31–36

    Google Scholar 

  • Castanet J, Guyetant R (1989) Atlas de répartition des Amphibiens et Reptiles de France. Société Herpétologique de France, Paris

    Google Scholar 

  • Caughley G (1994) Directions in conservation biology. J Anim Ecol 63:215–244

    Article  Google Scholar 

  • Clark RW, Brown WS, Stechert R et al (2008) Integrating individual behaviour and landscape genetics: the population structure of timber rattlesnake hibernacula. Mol Ecol 17:719–730

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  PubMed  CAS  Google Scholar 

  • Corbett K (1989) Conservation of European reptiles and amphibians. SEH, IUCN, London

    Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • di Rienzo A, Peterson AC, Garza JC et al (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci U S A 91:3166–3170

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

  • Frankham R (1995) Effective population-size adult population size ratios in wildlife—a review. Genet Res 66:95–107

    Article  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Article  Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

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

    Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Gautschi B, Widmer A, Joshi J et al (2002) Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of the dice snake, Natrix tessellata. Conserv Genet 3:235–245

    Article  CAS  Google Scholar 

  • Gibbs HL, Prior KA, Weatherhead PJ (1994) Genetic analysis of populations of threatened snake species using RAPD markers. Mol Ecol 3:329–337

    Article  CAS  Google Scholar 

  • Gibbs HL, Prior KA, Weatherhead PJ et al (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  PubMed  CAS  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Hardy OJ, Vekemans X (1999) Isolation by distance in a continuous population: reconciliation between spatial autocorrelation analysis and population genetics models. Heredity 83:145–154

    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

    Google Scholar 

  • Hartl D, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

  • Hofer U, Monney J-C, Dusej G (2001) Les reptiles de Suisse. Répartition, habitats, protection. Birkhäuser Verlag AG

  • Ischer A (1930) La Vipère péliade des Ponts de Martel. Le Rameau de Sapin du club jurassien 1:2–5

  • Jäggi C, Wirth T, Baur B (2000) Genetic variability in subpopulations of the asp viper (Vipera aspis) in the Swiss Jura mountains: implications for a conservation strategy. Biol Conserv 94:69–77

    Article  Google Scholar 

  • Kaufmann M (1893) Les Vipères de France: morsures—traitement. Asselin et Houzeau, Paris

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Google Scholar 

  • Leimu R, Mutikainen P, Koricheva J et al (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952

    Article  Google Scholar 

  • Lougheed SC, Gibbs HL, Prior KA et al (1999) Hierarchical patterns of genetic population structure in black rat snakes (Elaphe obsoleta obsoleta) as revealed by microsatellite DNA analysis. Evolution 53:1995–2001

    Article  CAS  Google Scholar 

  • Luiselli L (1993) High philopatry can produce strong sexual competition in male adders, Vipera berus. Amphib Reptil 14:310–311

    Article  Google Scholar 

  • Madsen T, Shine R (1992) Sexual competition among brothers may influence offspring sex ratio in snake. Evolution 46:1549–1552

    Article  Google Scholar 

  • Madsen T, Stille B, Shine R (1996) Inbreeding depression in an isolated population of adders Vipera berus. Biol Conserv 75:113–118

    Article  Google Scholar 

  • Madsen T, Shine R, Olsson M et al (1999) Conservation biology—restoration of an inbred adder population. Nature 402:34–35

    Article  CAS  Google Scholar 

  • Madsen T, Ujvari B, Olsson M (2004) Novel genes continue to enhance population growth in adders (Vipera berus). Biol Conserv 120:145–147

    Article  Google Scholar 

  • Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB et al (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  PubMed  CAS  Google Scholar 

  • Monmonier MS (1973) Maximum-difference barriers—alternative numerical regionalization method. Geogr Anal 5:245–261

    Google Scholar 

  • Monney J-C (1996) Biologie comparée de Vipera aspis L. et de Vipera berus L. (Reptilia, Ophidia, Viperidae) dans une station des Préalpes bernoises. Unpublished thesis, University of Neuchâtel, Switzerland, 179 pp

  • Moran PAP (1950) Notes on continuous stochastic phenomena. Biometrika 27:17–23

    Google Scholar 

  • Neumeyer R (1987) Density and seasonal movements of the adder (Vipera berus L.) on a subalpine environment. Amphib Reptil 2:63–82

    Google Scholar 

  • Ohta T, Kimura M (1973) Model of mutation appropriate to estimate number of electrophoretically detectable alleles in a finite population. Genet Res 22:201–204

    Google Scholar 

  • Otis DL, Burnham KP, White GC et al (1978) Statistical inference from capture data on closed animal population. Wildl Monogr 62:7–135

    Google Scholar 

  • Peel D, Ovenden JR, Peel SL (2004) NeEstimator: software for estimating effective population size. Queensland Government, Department of Primary Industries and Fisheries

  • Pinston H, Craney E, Pépin D et al (2000) Amphibiens et Reptiles de Franche-Comté. Atlas commenté de répartition. Groupe naturaliste de Franche-Comté, Besançon, France

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Prestt I (1971) An ecological study of the viper Vipera berus in southern Britain. J Zool 164:373–418

    Article  Google Scholar 

  • Prosser MR, Gibbs HL, Weatherhead PJ (1999) Microgeographic population genetic structure in the northern water snake, Nerodia sipedon sipedon detected using microsatellite DNA loci. Mol Ecol 8:329–333

    Article  PubMed  CAS  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Saint Girons H (1980) Biogéographie et évolution des vipères européennes. C R Soc Biogéogr 496:146–172

    Google Scholar 

  • Saint Girons H (1981) Quelques observations sur la dispersion des nouveau-nés chez Vipera berus et Vipera aspis dans le bocage atlantique (Reptilia: Viperidae). Amphib Reptil 2:269–272

    Article  Google Scholar 

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

    Google Scholar 

  • Soulé ME (1986) Conservation biology: the science of scarcity and diversity. Sinauer Associates

  • Ujvari B, Madsen T, Kotenko T et al (2002) Low genetic diversity threatens imminent extinction for the Hungarian meadow viper (Vipera ursinii rakosiensis). Biol Conserv 105:127–130

    Article  Google Scholar 

  • Ursenbacher S, Monney JC (2003) Résultats de 5 années de suivi d’une population de Vipère péliade (Vipera berus) dans le Jura Suisse: estimation des effectifs et discussion des méthodes d’estimation. Bull Soc Herp Fr 107:15–25

    Google Scholar 

  • Ursenbacher S, Carlsson M, Helfer V et al (2006) Phylogeography and Pleistocene refugia of the Adder (Vipera berus) as inferred from mitochondrial DNA sequence data. Mol Ecol 15:3425–3437

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Viitanen P (1967) Hibernation and seasonal movements of the viper, Vipera berus berus (L.), in southern Finland. Ann Zool Fenn 4:472–546

    Google Scholar 

  • Villarreal X, Bricker J, Reinert HK et al (1996) Isolation and characterization of microsatellite loci for use in population genetic analysis in the timber rattlesnake, Crotalus horridus. J Hered 87:152–155

    PubMed  CAS  Google Scholar 

  • Vitalis R, Couvet D (2001a) ESTIM 1.0: a computer program to infer population parameters from one- and two-locus gene identity probabilities. Mol Ecol Notes 1:354–356

    Article  Google Scholar 

  • Vitalis R, Couvet D (2001b) Two-locus identity probabilities and identity disequilibrium in a partially selfing subdivided population. Genet Res 77:67–81

    Article  PubMed  CAS  Google Scholar 

  • Völkl W, Thiesmeier B (2002) Die Kreuzotter—ein Leben in festen Bahnen? Laurenti Verlag

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

Download references

Acknowledgments

This work was funded by grants from the Swiss National Foundation (Grant Number 3100-059132.99/1 and Fellowship for prospective researchers) and the Société Académique Vaudoise. We acknowledge T. Durand, F. Paysant and G. Thiery for the sampling. Samples were taken with the permission of la Conservation de la Faune du Canton de Vaud (Switzerland), le Service de la Faune from Neuchâtel and Fribourg (Switzerland), the Préfecture du Département du Doubs (France) and the Préfecture du Département du Jura (France). Discussions with J. Goudet, J. Parker, C. E. Pook, P. Taberlet and J. Yearsley, and comments from two anonymous reviewers, greatly improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sylvain Ursenbacher.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ursenbacher, S., Monney, JC. & Fumagalli, L. 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 (2009). https://doi.org/10.1007/s10592-008-9580-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-008-9580-7

Keywords

Navigation