Mammalian Biology

, Volume 77, Issue 1, pp 13–21 | Cite as

Dwindling genetic diversity in European ground squirrels?

  • Hichem Ben Slimen
  • Csongor I. Gedeon
  • Ilse E. Hoffmann
  • Franz SuchentrunkEmail author
Original Investigation


The European ground squirrel (Spermophilus citellus) is endangered and in decline. Populations are increasingly fragmented, and only a coordinated conservation effort at the European level may guarantee its long-term survival. To obtain a general population genetic picture on a larger geographic scale, we screened 117 individuals from seven local populations in Hungary, Romania, and Austria for allelic variation at eleven microsatellite loci. We found a high (23.4%) proportion of private alleles, and a moderate to some what elevated level (15.27%)of partitioning of genetic diversity among populations, compared to that found in many other terrestrial mammals. Genetic variability was significantly higher than in earlier studied Czech populations that are considered genetically depleted, but significantly lower than in undisturbed populations of S. suslicus and S. brunneus, that are similar to the European ground squirrel in their ecological requirements, reproductive biology, and social organization. Genetic diversity was also lower than in most presumably “undisturbed” populations of other Sciurid species. This, together with the observed level and pattern of genetic differentiation among populations, such as no significant increase of genetic differentiation with geographic distance and similar variance of genetic differentiation between populations independent of geographic distance, indicated the prevalence of relatively strong drift effects for all populations. A Bayesian STRUCTURE analysis and a factorial correspondence analysis concordantly revealed a fairly complex genetic composition of local populations, but no major geographic trend in the pattern of the genetic composition. Overall, the results suggest disintegration of local colonies that might earlier have been more connected genetically. The STRUCTURE analysis also suggested anthropogenic translocations among single Hungarian populations. Our data on genetic diversity and its distribution do not object to such conservation measures. Translocation of individuals particularly from nearby populations may increase the chances of survival of small and isolated populations and counteract inbreeding at low densities.


Genetic differentiation Genetic diversity Sciurids Population genetics Spermophilus citellus 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Beerli, P., Felsenstein, J., 2001a. Maximum likelihood estimation of a migration matrix and effective population sizes in n populations by using a coalescent approach. Proc. Natl. Acad. Sci. U.S.A. 98, 4563–4568.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Beerli, P., Felsenstein, J., 2001. Migrate 1.1. Scholar
  3. Belkhir, K., 2004. GENETIX V. 4.0, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions CNRS UMR 5000, Université de Montpellier II, Montpellier.Google Scholar
  4. Biedrzycka, A., Konopin´ ski, M.K., 2008. Genetic variability and the effect of habitat fragmentation in spotted suslik Spermophilus suslicus populations from two different regions. Conserv. Genet. 9, 1211–1221.CrossRefGoogle Scholar
  5. Biedrzycka, A., Kloch, A., Buczek, M., Radwan, J., 2011. Majorhistocompatibility complex DRB genes and blood parasite loads in fragmented populations of the spotted suslik Spermophilus suslicus. Mamm. Biol. 76, 672–677.CrossRefGoogle Scholar
  6. Bridgland, D.R., Schreve, D.C., Keen, D.H., Meyrick, R., Westaway, R., 2004. Biostrati-graphical correlation late Quaternary sequence of the Thames and key fluvial localities in central Germany. Proc. Geol. Assoc. 115, 125–140.CrossRefGoogle Scholar
  7. Cohas, A., Bonenfant, C., Kempenaers, B., Allainé, D., 2009. Age-specific effect of heterozygosity on survival in alpine marmots, Marmota marmota. Mol. Ecol. 18, 1491–1503.PubMedCrossRefGoogle Scholar
  8. Cohas, A., Yoccoz, N.G., Allainé, D., 2007. Extra-pair paternity in alpine marmots, Marmota marmota: genetic quality and genetic diversity effects. Behav. Ecol. Sociobiol. 61, 1081–1092.CrossRefGoogle Scholar
  9. Cornuet, J.M., Luikart, G., 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.PubMedPubMedCentralGoogle Scholar
  10. Cornuet, J.M., Piry, S., Luikart, G., Estoup, A., Solignac, M., 1999. New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153, 1989–2000.PubMedPubMedCentralGoogle Scholar
  11. Coroiu, C., Kryštufek, B., Vohralík, V., Zagorodnyuk, I., 2008. Spermophilus citellus. In: IUCN 2008. IUCN Red List of Threatened Species. Scholar
  12. Da Silva, A., Luikart, G., Yoccoz, N.G., Cohas, A., Allainé, D., 2006. Genetic diversity – fitness correlation revealed by microsatellite analyses in European alpine marmots (Marmota marmota). Conserv. Genet. 7, 371–382.CrossRefGoogle Scholar
  13. Di Rienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M., Freimer, N.B., 1994. Mutational processes of simple-sequence repeat loci in human populations. Proc. Natl. Acad. Sci. U.S.A. 91, 3166–3170.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Dieringer, D., Schlötterer, C., 2002. Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol. Notes 3, 167–169.CrossRefGoogle Scholar
  15. Evanno, G., Regnaut, S., Goudet, J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620.PubMedCrossRefGoogle Scholar
  16. Falush, D., Stephens, M., Pritchard, J.K., 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.PubMedPubMedCentralGoogle Scholar
  17. Fike, J.A., Rhodes Jr., O.E., 2009. Characterization of twenty-six polymorphic microsatellite markers for the fox squirrel (Sciurus niger) and their utility in gray squirrels (Sciurus carolinensis) and red squirrels (Tamiasciurus hudsonicus).CrossRefGoogle Scholar
  18. Garner, A., Rachlow, J.L., Hicks, J.F., 2005a. Patterns of genetic diversity and its loss in mammalian populations. Conserv. Biol. 19, 1215–1221.CrossRefGoogle Scholar
  19. Garner, G., Rachlow, J.L., Waits, L.P., 2005b. Genetic diversity and population divergence in fragmented habitats: conservation of Idaho ground squirrels. Conserv. Gen. 6, 759–774.CrossRefGoogle Scholar
  20. Garza, J.C., Williamson, E.G., 2001. Detection of reduction in population size using data from microsatellite loci. Mol. Ecol. 10, 305–318.PubMedCrossRefGoogle Scholar
  21. Gondek, A., Verduijn, M., Wolff, K., 2006. Polymorphic microsatellite markers for endangered spotted suslik, Spermophilus suslicus. Mol. Ecol. Notes 6, 359–361. Goudet, J., 1995. Fstat Version 1.2. A computer program to calculate F-statistics. J. Hered. 86, 485–486.Google Scholar
  22. Goudet, J., 2001. Fstat, A Program to Estimate and Test Gene Diversities and Fixation Indices (Version 2.9.3)., Scholar
  23. Gündüz, I., Jaarola, M., Tez, C., Yeniyurt, C., Polly, P.D., Searle, J.B., 2007. Multigenic and morphometric differentiation of ground squirrels (Spermophilus, Sciuridae, Rodentia) in Turkey, with description of a new species. Mol. Phylogenet. Evol. 43, 916–935.PubMedCrossRefGoogle Scholar
  24. Hale, M.L., Bevan, R., Wolff, K., 2001. New polymorphic microsatellite markers for the red squirrel (Sciurus vulgaris) and their applicability to the grey squirrel (S. carolinensis). Mol. Ecol. Notes 1, 47–49.CrossRefGoogle Scholar
  25. Halliburton, R., 2004. Introduction to Population Genetics. Benjamin Cummings Publ., San Francisco.Google Scholar
  26. Hanslik, S., Kruckenhauser, L., 2000. Microsatellite loci for two European sciurid species (Marmota marmota, Spermophilus citellus). Mol. Ecol. 9, 2163–2165.PubMedCrossRefGoogle Scholar
  27. Hedirck, P.W., 1999. Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53, 313–318.CrossRefGoogle Scholar
  28. Helgen, K.M., Cole, F.R., Helgen, L.E., Wilson, D.E., 2009. Generic revision in the holarctic ground squirrel genus Spermophilus. J. Mammal. 90, 270–305.CrossRefGoogle Scholar
  29. Hoffmann, I.E., Muck, E., Millesi, E., 2004. Why males incur a greater predation risk than females in juvenile European sousliks (Spermophilus citellus). Lutra 47, 85–94.Google Scholar
  30. Hoffmann, I.E., Millesi, E., Huber, S., Everts, L.G., Dittami, J.P., 2003a. Population dynamics of European ground squirrels (Spermophilus citellus) in a suburban area. J. Mammal. 84, 615–626.CrossRefGoogle Scholar
  31. Hoffmann, I.E., Millesi, E., Pieta, K., Dittami, J.P., 2003b. Anthropogenic effects on the population ecology of European ground squirrels (Spermophilus citellus) at the periphery of their geographic range. Mamm. Biol. 68, 205–213.CrossRefGoogle Scholar
  32. Hulová, Š., Sedláček, F., 2008. Population genetic structure of the European ground squirrel in the Czech Republic. Conserv. Genet. 9, 615–625.CrossRefGoogle Scholar
  33. The IUCN Red List of Threatened Species. Spermophilus citellus. Scholar
  34. Jones, R.T., Martin, A.P., Mitchell, A.J., Collinge, S.K., Ray, C., 2005. Characterization of 14polymorphic microsatellite markers for the black-tailed prairiedog (Cynomys ludovicianus). Mol. Ecol. Notes 5, 71–73.CrossRefGoogle Scholar
  35. Kruckenhauser, L., Bryant, A.E., Griffin, S.C., Amish, S.J., Pinsker, W., 2009. Patterns of within and between-colony microsatellite variation in the endangered Vancouver Island marmot (Marmota vancouverensis): implications for conservation. Conserv. Genet. 10, 1759–1772.CrossRefGoogle Scholar
  36. Kryštufek, B., 1999. Spermophilus citellus (Linnaeus, 1766). In: Mitchell-Jones, A.J. (Ed.), The Atlas of European Mammals. Academic Press, London.Google Scholar
  37. Kryštufek, B., Bryja, J., Bužan, E.V., 2009. Mitochondrial phylogeography of the European ground squirrel, Spermophilus citellus, yields evidence on refugia for steppic taxa in the southern Balkans. Heredity 103, 129–135.PubMedCrossRefPubMedCentralGoogle Scholar
  38. Lance, S.L., Maldonado, J.E., Bocetti, C.I., Pattee, O.H., Ballou, J.D., Fleischer, R.C., 2003. Genetic variation in natural and translocated populations of the endangered Delmarva fox squirrel (Sciurus niger cinereus). Conserv. Genet. 4, 707–718.CrossRefGoogle Scholar
  39. Lane, J.E., Boutin, S., Gunn, M.R., Slate, J., Coltman, D.W., 2007. Genetic relatedness of mates does not predict patterns of parentage in North American red squirrels. Anim. Behav. 74, 611–619.CrossRefGoogle Scholar
  40. Leberg, P.L., 1992. Effects of population bottlenecks on genetic diversity asmeasured by allozyme electrophoresis. Evolution 46, 477–494.PubMedCrossRefGoogle Scholar
  41. Mantel, N., 1967. The detection of disease clustering and generalized regression approach. Cancer Res. 27, 209–220.PubMedGoogle Scholar
  42. May, B., Gavin, T.A., Sherman, P.W., Korves, T.M., 1997. Characterization of microsatellite loci in the northern Idaho ground squirrel Spermophilus brunneus brunneus. Mol. Ecol. 6, 399–400.PubMedCrossRefGoogle Scholar
  43. Millesi, E., Huber, S., Dittami, J.P., Hoffmann, I., Daan, S., 1998. Parameters of mating effort and success in male European ground squirrels, Spermophilus citellus. Ethology 104, 298–313.CrossRefGoogle Scholar
  44. Narum, S.R., 2006. Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv. Genet. 7, 783–787.CrossRefGoogle Scholar
  45. Nei, M., 1978. Estimation of average heterozygosity and genetic distances from a small number of individuals. Genetics 89, 583–590.PubMedPubMedCentralGoogle Scholar
  46. Ogden, R., Shuttleworth, C., McEwing, R., Cesarini, S., 2005. Genetic management of the red squirrel, Sciurus vulgaris: a practical approach to regional conservation. Conserv. Genet. 6, 511–525.CrossRefGoogle Scholar
  47. Paetkau, D., Slade, R., Burden, M., Estoup, A., 2004. Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol. Ecol. 13, 55–65.PubMedCrossRefPubMedCentralGoogle Scholar
  48. Piry, S., Alapetite, A., Cornuet, J.-M., Paetkau, D., Baudouin, L., Estoup, A., 2004. GeneClass2: a software for genetic assignment and first-generation migrant detection. J. Hered. 95, 536–539.PubMedCrossRefGoogle Scholar
  49. Pritchard, J.K., Stephens, P., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.PubMedPubMedCentralGoogle Scholar
  50. Pritchard, J.K., Wen, W., 2004. Documentation for the STRUCTURE Software Version 2. Chicago. Scholar
  51. Rannala, B., Mountain, J.L., 1997. Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. U.S.A. 94, 9197–9201.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Raymond,M., Rousset, F., 1995. Genepop(version1.2):population genetics software for exact tests and ecumenism. J. Hered. 86, 248–249.CrossRefGoogle Scholar
  53. Reed, D.H., Frankham, R., 2003. Correlation between fitness and genetic diversity. Conserv. Biol. 17, 230–237.CrossRefGoogle Scholar
  54. Říčanová, Š., Bryja, J., Cosson, J.-F., Gedeon, C., Choleva, L., Ambros, M., Sedláček, F., 2011. Depleted genetic variation of the European ground squirrel in Central Europe in both microsatellites and the major histocompatibility complex gene: implications for conservation. Conserv. Genet. 12, 1115–1129.CrossRefGoogle Scholar
  55. Roach, J.L., Stapp, P., Van Horne, B., Antolin, M.F., 2001. Genetic structure of a metapopulation of black-tailed prairie dogs. J. Mammal. 82, 946–959.CrossRefGoogle Scholar
  56. Rousset, F., 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228.PubMedPubMedCentralGoogle Scholar
  57. Ružić, A., 1978. Citellus citellus (Linnaeus, 1766) – Der oder das Europäische Ziesel. In: Niethammer, J., Krapp, F. (Eds.), Handbuch der Säugetiere Europas. Bd.1, Nagetiere, vol. I. Akademische Verlagsgesellschaft, Wiesbaden, pp. 123–144.Google Scholar
  58. Schneider, S., Roessli, D., Excoffier, L., 2000. Arlequin: A Software for Population Genetics Data Analysis Ver 2.000. Genetics and Biometry Lab, Department of Anthropology, University of Geneva, Geneva.Google Scholar
  59. Schulte-Hoestedde, A.I., Gibbsm, H.L., Millarm, J.S., 2001. Microgeographic genetic structure in the yellow-pine chipmunk (Tamias amoenus). Mol. Ecol. 10, 1625–1631.CrossRefGoogle Scholar
  60. Selonen, V., Painter, J.N., Hanski, I.K., 2005. Microsatellite variation in the Siberian flying squirrel in Finland. Ann. Zool. Fenn. 42, 505–511.Google Scholar
  61. Shibata, K., Bandoh, K., Yaekashiwa, N., Matsuzaka, T., Tamate, H.B., 2003. A simple method for isolation of microsatellites from the Japanese squirrel, Sciurus lis, without constructing a genomic library. Mol. Ecol. 3, 657–658.CrossRefGoogle Scholar
  62. Shriver, L., Jin, L., Chakraborty, R., Boerwinkle, E., 1993. VNTR allele frequency distributions under the stepwise mutation model: a computer simulation approach. Genetics 134, 983–993.PubMedPubMedCentralGoogle Scholar
  63. Spitzenberger, F., Bauer, K., 2001. Ziesel Spermophilus citellus (Linnaeus, 1766). In: Spitzenberger, F. (Ed.), Die Säugetierfauna Österreichs. Grüne Reihe des Bun-desministeriums für Land- u. Forstwirtschaft, Umwelt und Wasserwirtschaft, vol. 13. Austria Medien Service Gmbh, Graz, pp. 356–365.Google Scholar
  64. S-PLUS 6.2: Copyright (c) 1988, 2003. Insightful Corp.: Copyright Lucent Technologies, Inc.Google Scholar
  65. SPSS 10.0.1 ©. SPSS company, Inc.Google Scholar
  66. Srikawan, S., Woodruff, D.S., 2000. Genetic erosion in isolated small-mammal populations following rainforest fragmentation. In: Young, A.G., Clarke, G.M. (Eds.), Genetics, Demography and Viability of Fragmented Populations. CambridgeUniversity Press, Cambridge, pp. 149–172.CrossRefGoogle Scholar
  67. Stevens, S., Coffin, J., Strobeck, C., 1997. Microsatellite loci in Columbian ground squirrels Spermophilus columbianus. Mol. Ecol. 6, 493–495.PubMedCrossRefGoogle Scholar
  68. Trizio, I., Crestanello, B., Galbusera, P., Wauters, L.A., Tosi, G., Matthysen, E., Hauffe, H.C., 2005. Geographical distance and physical barriers shape the genetic structure of Eurasian red squirrels (Sciurus vulgaris) in the Italian Alps. Mol. Ecol. 14, 469–481.PubMedCrossRefGoogle Scholar
  69. Turrini, T., Brenner, M., Millesi, E., Hoffmann, I.E., 2008. Home ranges of European ground squirrels (Spermophilus citellus) in two habitats exposed to different degree of human impact. Lynx 39, 333–342.Google Scholar
  70. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538.CrossRefGoogle Scholar
  71. Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2011

Authors and Affiliations

  • Hichem Ben Slimen
    • 1
  • Csongor I. Gedeon
    • 2
  • Ilse E. Hoffmann
    • 3
  • Franz Suchentrunk
    • 1
    Email author
  1. 1.Research Institute of Wildlife EcologyUniversity of Veterinary Medicine ViennaViennaAustria
  2. 2.Department of EthologyEötvös Loránd UniversityBudapestHungary
  3. 3.Department of Behavioural BiologyUniversity of ViennaViennaAustria

Personalised recommendations