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.
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
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
Bonnet X, Naulleau G (1996) Catchability in snakes: consequences for estimates of breeding frequency. Can J Zool 74:233–239
Brassel KE, Reif D (1979) A procedure to generate Thiessen polygons. Geogr Anal 325:31–36
Castanet J, Guyetant R (1989) Atlas de répartition des Amphibiens et Reptiles de France. Société Herpétologique de France, Paris
Caughley G (1994) Directions in conservation biology. J Anim Ecol 63:215–244
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
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660
Corbett K (1989) Conservation of European reptiles and amphibians. SEH, IUCN, London
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
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
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
Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, UK
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
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
Gibbs HL, Prior KA, Weatherhead PJ (1994) Genetic analysis of populations of threatened snake species using RAPD markers. Mol Ecol 3:329–337
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
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
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
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
Hartl D, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, Sunderland
Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112
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
Kaufmann M (1893) Les Vipères de France: morsures—traitement. Asselin et Houzeau, Paris
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
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
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
Luiselli L (1993) High philopatry can produce strong sexual competition in male adders, Vipera berus. Amphib Reptil 14:310–311
Madsen T, Shine R (1992) Sexual competition among brothers may influence offspring sex ratio in snake. Evolution 46:1549–1552
Madsen T, Stille B, Shine R (1996) Inbreeding depression in an isolated population of adders Vipera berus. Biol Conserv 75:113–118
Madsen T, Shine R, Olsson M et al (1999) Conservation biology—restoration of an inbred adder population. Nature 402:34–35
Madsen T, Ujvari B, Olsson M (2004) Novel genes continue to enhance population growth in adders (Vipera berus). Biol Conserv 120:145–147
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
Mantel N (1967) Detection of disease clustering and a generalized regression approach. Cancer Res 27:209
Marshall TC, Slate J, Kruuk LEB et al (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
Monmonier MS (1973) Maximum-difference barriers—alternative numerical regionalization method. Geogr Anal 5:245–261
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
Neumeyer R (1987) Density and seasonal movements of the adder (Vipera berus L.) on a subalpine environment. Amphib Reptil 2:63–82
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
Otis DL, Burnham KP, White GC et al (1978) Statistical inference from capture data on closed animal population. Wildl Monogr 62:7–135
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
Prestt I (1971) An ecological study of the viper Vipera berus in southern Britain. J Zool 164:373–418
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
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Saint Girons H (1980) Biogéographie et évolution des vipères européennes. C R Soc Biogéogr 496:146–172
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
Sokal RR, Wartenberg DE (1983) A test of spatial autocorrelation analysis using an isolation-by-distance model. Genetics 105:219–237
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
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
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
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
Viitanen P (1967) Hibernation and seasonal movements of the viper, Vipera berus berus (L.), in southern Finland. Ann Zool Fenn 4:472–546
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
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
Vitalis R, Couvet D (2001b) Two-locus identity probabilities and identity disequilibrium in a partially selfing subdivided population. Genet Res 77:67–81
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
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
Corresponding author
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-008-9580-7