Conservation Genetics

, Volume 14, Issue 2, pp 345–354 | Cite as

Do rivers and human-induced habitat fragmentation affect genetic diversity and population structure of the European ground squirrel at the edge of its Pannonian range?

  • Nada Ćosić
  • Štěpánka Říčanová
  • Josef Bryja
  • Aleksandra Penezić
  • Duško Ćirović
Research Article

Abstract

The European ground squirrel (EGS) (Spermophilus citellus) populations of Vojvodina (Serbia) represent the southernmost part of its distribution in the Pannonian lowland. For species with low dispersal abilities a presence of even weak barriers can have significant influence on genetic structure among adjacent populations. We examined here the effects of habitat fragmentation and river barriers on the genetic structure of the EGS based on 12 microsatellite loci. Bayesian clustering methods were used as additions to classical population genetic approaches. We found that EGS populations in Vojvodina are highly fragmented, but their genetic variation is still higher than in peripheral populations in Central Europe. Populations in Vojvodina consistently grouped into three genetic clusters. The Danube, but not the Tisza River, represents an important barrier to gene flow. EGS populations in the studied area did not show the signs of recent genetic bottlenecks, as would be expected from observations of recent population declines. Conservation strategy should be focused on maintenance of remained suitable habitats and optimal population sizes.

Keywords

Souslik Barriers Genetic structure Gene flow Microsatellites 

References

  1. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Montpellier: Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier (France)Google Scholar
  2. Bell KC, Matocq MD (2011) Regional genetic subdivision in the Mohave ground squirrel: evidence of historic isolation and ongoing connectivity in a Mojave Desert endemic. Anim Conserv 14:371–381CrossRefGoogle Scholar
  3. Bryja J, Granjon L, Dobigny G, Patzenhauerová H, Konečný A, Duplantier JM, Gauthier P, Colyn M, Durnez L, Lalis A, Nicolas V (2010) Plio-Pleistocene history of West African Sudanian savanna and the phylogeography of the Praomys daltoni complex (Rodentia): the environment/geography/genetic interplay. Mol Ecol 19:4783–4799PubMedCrossRefGoogle Scholar
  4. Busch JD, Waser PM, DeWoody JA (2007) Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Mol Ecol 16:2450–2462PubMedCrossRefGoogle Scholar
  5. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631PubMedCrossRefGoogle Scholar
  6. Ćirović D, Ćosić N (2011) Viability of the European ground squirrel (Spermophilus citellus L. 1766) populations in Serbia—final report. Ministry of Environment and Spatial Planing, Republic of SerbiaGoogle Scholar
  7. Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9:539PubMedCrossRefGoogle Scholar
  8. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  9. Coroiu C, Kryštufek B, Vohralík V, Zagorodnyuk I (2008) Spermophilus citellus. In: IUCN 2011. IUCN red list of threatened species. Version 2011.2. http://www.iucnredlist.org. Accessed 21 Oct 2011
  10. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc B 39:1–38Google Scholar
  11. Djan M, Obreht D, Vapa Lj (2006) Polymorphism of mtDNA regions in brown hare (Lepus europaeus) from Vojvodina (Serbia and Montenegro). Eur J Wildl Res 52:288–291CrossRefGoogle Scholar
  12. Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographic ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188PubMedCrossRefGoogle Scholar
  13. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  14. Excoffier L, Laval G, Schneider S (2005) ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  15. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  16. Fontaine MC, Baird SJE, Piry S, Ray N, Tolley KA, Duke S, Birkun A Jr, Ferreira M, Jauniaux T, Lavona A, Öztürk B, Öztürk AA, Ridoux V, Rogan E, Sequeira M, Siebert U, Vikingsson GA, Bouquegneau JM, Michaux JR (2007) Rise of oceanographic barriers in continuous populations of a cetacean: the genetic structure of harbour porpoises in Old World waters. BMC Biol 5(30):1–16Google Scholar
  17. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508CrossRefGoogle Scholar
  18. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  19. Garner A, Rachlow JL, Waits LP (2005) Genetic diversity and population divergence in fragmented habitats: conservation of Idaho ground squirrel. Conserv Genet 6:759–774CrossRefGoogle Scholar
  20. Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices. v 2.9.3.2, Institut d’Ecologie, Laboratorie de Zoologie, Lausanne, Switzerland. http://www.unil.ch/izea/softwares/fstat.html. Accessed 20 Sept 2008
  21. Guillot G, Estoup A, Mortier F, Cosson J (2005a) A spatial statistical model for landscape genetics. Genetics 170:1261–1280PubMedCrossRefGoogle Scholar
  22. Guillot G, Mortier F, Estoup A (2005b) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715CrossRefGoogle Scholar
  23. Hedrick PW (2005) Genetics of populations, 3rd edn. Jones & Bartlett Publishers, SudburyGoogle Scholar
  24. Helgen KM, Cole FR, Helgen LE, Wilson DE (2009) Generic revision in the Holarctic ground squirrel genus Spermophilus. J Mamm 90:270–305CrossRefGoogle Scholar
  25. Hulová Š, Sedláček F (2008) Population genetic structure of the European ground squirrel in the Czech Republic. Conserv Genet 9:615–625CrossRefGoogle Scholar
  26. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6: 13. http://ibdws.sdsu.edu/. Accessed 14 Dec 2012
  27. Keller FL, Jeffery JK, Arcese P, Beaumont AM, Hochachka MW, Smith NMJ, Bruford WM (2001) Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers. Proc R Soc Lond B 268:1387–1394CrossRefGoogle Scholar
  28. Kennis J, Nicolas V, Hulselmans J, Katuala PGB, Wendelen W, Verheyen E, Dudu AM, Leirs H (2011) The impact of the Congo River and its tributaries on the rodent genus Praomys: speciation origin or range expansion limit? Zool J Linn Soc 163:983–1002CrossRefGoogle Scholar
  29. Kirschning J, Zachos EF, Cirovic D, Radovic TI, Hmwe SS, Hartl BG (2007) Population genetic analysis of Serbian red foxes (Vulpes vulpes) by means of mitochondrial control region sequences. Biochem Genet 45:409–420PubMedCrossRefGoogle Scholar
  30. Knežev M (2006) Ecological research Tisza 2005. Tiski cvet, Novi Sad (in Serbian)Google Scholar
  31. Koshev YS, Kocheva MA (2007) Environmental factors and distribution of European ground squirrel (Spermophilus citellus) in Bulgaria. J Ecol Saf 1:277–287Google Scholar
  32. Lada H, Nally RM, Taylor AC (2008) Distinguishing past from present gene flow along and across a river: the case of the carnivorous marsupial (Antechinus flavipes) on southern Australian floodplains. Conserv Genet 9:569–580CrossRefGoogle Scholar
  33. Loxterman JL (2011) Fine scale population genetic structure of pumas in the Intermountain West. Conserv Genet 12:1049–1059CrossRefGoogle Scholar
  34. Lugon-Moulin N, Hausser J (2002) Phylogeographical structure, postglacial recolonization and barriers to gene flow in the distinctive Valais chromosome race of the common shrew (Sorex araneus). Mol Ecol 11:785–794PubMedCrossRefGoogle Scholar
  35. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  36. Luikart G, Amish SJ, Winnie J, Beja-Pereira A, Godinho R, Allendorf FW, Harris RB (2011) High connectivity among argali sheep from Afghanistan and adjacent countries: inferences from neutral and candidate gene microsatellites. Conserv Genet 12:921–931CrossRefGoogle Scholar
  37. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197CrossRefGoogle Scholar
  38. Matějů J, Nová P, Uhlíková J, Hulová Š, Cepáková E (2008) Distribution of the European ground squirrel (Spermophilus citellus) in the Czech Republic in 2002–2008. Lynx 39:277–294Google Scholar
  39. Mitchell-Jones AJ, Amori G, Bogdanowicz W, Kryštufek B, Reijnders PJH, Spitzenberger F, Stube M, Thissen JBM, Vohralík V, Zima J (1999) The atlas of European mammals. Academic, LondonGoogle Scholar
  40. Mossman CA, Waser PM (2001) Effects of habitat fragmentation on population genetic structure in the white-footed mouse (Peromyscus leucopus). Can J Zool 79:285–295Google Scholar
  41. Neumann K, Jansman H, Kayser A, Maak S, Gattermann R (2004) Multiple bottlenecks in threatened western European populations of the common hamster Cricetus cricetus (L.). Conserv Genet 5:181–193CrossRefGoogle Scholar
  42. Pertoldi C, Bijlsma R, Loeschcke V (2007) Conservation genetics in a globally changing environment: present problems, paradoxes and future challenges. Biodivers Conserv 16:4147–4163CrossRefGoogle Scholar
  43. Petrov MB (1992) Mammals of Yugoslavia, insectivores and rodents. Natural History Museum of Belgrade, BelgradeGoogle Scholar
  44. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  45. Puzović S (2008) Power transmission lines as structural factor in birds habitats. Dissertation, University of Novi Sad (in Serbian)Google Scholar
  46. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  47. Říčanová Š, Bryja J, Cosson JF, 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 12:1115–1129CrossRefGoogle Scholar
  48. Ružić A (1950) Contribution to the knowledge of ecology of the ground squirrel Citellus citellus L. Proc Inst Ecol Biogeogr 1:97–140 (in Serbian)Google Scholar
  49. Ružić A (1979) Decreasing number of the ground squirrel (Citellus citellus L.) populations in Yugoslavia in the period 1947–1977. Ecology 14:185–194 (in Serbian with the abstract in English)Google Scholar
  50. Segelbacher G, Cushman SA, Epperson BK, Fortin M-J, Francois O, Hardy OJ, Holderegger R, Taberlet P, Waits LP, Manel S (2010) Applications of landscape genetics in conservation biology: concepts and challenges. Conserv Genet 11:375–385CrossRefGoogle Scholar
  51. Slimen HB, Gedeon CI, Hoffmann IE, Suchentrunk F (2012) Dwindling genetic diversity in European ground squirrels? Mamm Biol 77:13–21Google Scholar
  52. Strijsktra AM, Daan S (1997) Sleep during arousal episodes as a function of prior torpor duration in hibernating European ground squirrel. J Sleep Res 6:36–43CrossRefGoogle Scholar
  53. Trizio I, Crestanello B, Galbusera P, Wauters LA, Tosi G, Matthysen E, Hauffe HC (2005) Geographical distance and physical barriers shape the genetic structure of Eurasian red squirrels (Sciurus vulgaris) in the Italian Alps. Mol Ecol 14:469–481PubMedCrossRefGoogle Scholar
  54. Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Nada Ćosić
    • 1
  • Štěpánka Říčanová
    • 2
    • 3
  • Josef Bryja
    • 3
    • 4
  • Aleksandra Penezić
    • 5
  • Duško Ćirović
    • 5
  1. 1.Institute for Biological Reasearch Siniša Stanković, University of BelgradeBelgradeSerbia
  2. 2.Department of Zoology, Faculty of ScienceUniversity of South BohemiaCeske BudejoviceCzech Republic
  3. 3.Department of Population BiologyInstitute of Vertebrate Biology, Academy of Sciences of the Czech RepublicBrnoCzech Republic
  4. 4.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  5. 5.Faculty of BiologyUniversity of BelgradeBelgradeSerbia

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