Mitochondrial genetic diversity and structuring of northern white-breasted hedgehogs from the Central Balkans

Mitochondrial genetic diversity and structuring of northern white-breasted hedgehogs from the Central Balkans

Even though the phylogeography of hedgehogs has been well studied, information on the genetic variability of the northernwhite-breasted hedgehogErinaceus roumanicusfrom the Balkans is lacking, since the previous studies were based on very limitedsampling across the Balkans. The aim of this study is to estimate the genetic diversity and population structuring ofE. roumanicusfromthe Central Balkans and to complement an already proposed phylogeographic scenario of this species. Tissue samples of 108 road-killednorthern white-breasted hedgehogs were collected across the Central Balkan countries of Serbia, Montenegro, Bosnia and Herzegovina,and Macedonia. A partial fragment of the mtDNA control region (CR) was amplified and sequenced. Nine of 13 haplotypes detectedin this study have not been previously published. The results indicate a moderate level of haplotype diversity ofE. roumanicusfrom theCentral Balkans and differentiation into four spatial groups, which are named after the approximate sampling localities as northwestern- central, northeastern, southwestern, and southeastern groups. The observed population structure in the Central Balkans remains lesspronounced in further phylogenetic and phylogeographic analyses of the dataset comprisingE. roumanicusandE. concolormtDNA CRsequences. The central position of Balkan haplotypes in a median-joining network indicated its role as a primary source population forpostglacial northward expansion.

___

  • Alexandri P, Triantafyllidis A, Papakostas S, Chatzinikos E, Platis P, Papageorgiou N, Larson G, Abatzopoulos TJ, Triantaphyllidis C (2012). The Balkans and the colonization of Europe: the post-glacial range expansion of the wild boar, Sus scrofa. J Biogeogr 39: 713-723.
  • Avise JC (2004). Molecular Markers: Natural History and Evolution. 2nd ed. Sunderland, MA, USA: Sinauer Associates.
  • Bandelt HJ, Forster P, Röhl A (1999). Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37-48.
  • Bannikova AA, Lebedev VS, Abramov AV, Rozhnov VV (2014). Contrasting evolutionary history of hedgehogs and gymnures (Mammalia: Erinaceomorpha) as inferred from a multigene study. Biol J Linn Soc 112: 499-519.
  • Berggren KT, Ellegren H, Hewitt GM, Seddon JM (2005). Understanding the phylogeographic patterns of European hedgehogs, Erinaceus concolor and E. europaeus using the MHC. Heredity 95: 84-90.
  • Bolfíková B, Hulva P (2012). Microevolution of sympatry: landscape genetics of hedgehogs Erinaceus europaeus and E. roumanicus in Central Europe. Heredity 108: 248-255.
  • Durka W, Babik W, Ducroz JF, Heidecke D, Rosell F, Samjaa R, Saveljev AP, Stubbe A, Ulevicius A, Stubbe M (2005). Mitochondrial phylogeography of the Eurasian beaver Castor fiber . Mol Ecol 14: 3843-3856.
  • Djan M, Maletić V, Trbojević I, Popović D, Veličković N, Burazerović J, Ćirović D (2014). Genetic diversity and structuring of the grey wolf population from the Central Balkans based on mitochondrial DNA variation. Mamm Biol 79: 277-282.
  • Excoffier L, Lischer H (2010). Arlequin suite v. 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564-567.
  • François O, Durand E (2010). Spatially explicit Bayesian clustering models in population genetics. Mol Ecol Resour 10: 773-784.
  • Guillot G, Mortier F, Estoup A (2005). GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5: 712-715.
  • Hall TA (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucl Acid S 41: 95-98.
  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68: 87-112.
  • Hewitt GM (2000). The genetic legacy of the Quaternary ice ages. Nature 405: 907-913.
  • Hewitt GM (2001). Speciation, hybrid zones and phylogeography: or seeing genes in space and time. Mol Ecol 10: 537-549.
  • Hewitt GM (2004). Genetic consequences of climatic oscillations in the Quaternary. Philos T R Soc B 359: 183-195.
  • Hirata D, Mano T, Abramov AV, Baryshnikov GF, Kosintsev PA, Vorobiev AA, Raichev EG, Tsunoda H, Kaneko Y, Murata K et al. (2013). Molecular phylogeography of the brown bear ( Ursus arctos ) in northeastern Asia based on analyses of complete mitochondrial DNA sequences. Mol Biol Evol 30: 1644-1645.
  • Huntley B (1999). Climatic change and reconstruction. Quat Proc 7: 513-520.
  • Hutterer R (2005). Order Erinaceomorpha. In: Wilson DE, Reeder DM, editors. Mammal Species of the World: A Taxonomic and Geographic Reference. Baltimore, MD, USA: Johns Hopkins University Press, pp. 212-219.
  • Kocher TD, Thomas WK, Meyer A (1989). Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. P Natl Acad Sci USA 86: 6196-6200.
  • Kryštufek B (2002). Cranial variability in the Eastern hedgehog Erinaceus concolor (Mammalia: Insectivora). J Zool 258: 365- 373.
  • Kryštufek B, Reed JM (2004). Pattern and process in Balkan biodiversity: an overview. In: Griffiths H, Kryštufek B, Reed JM, editors. Balkan Biodiversity: Pattern and Process in the European Hotspot. Dordrecht, the Netherlands: Springer, pp. 1-8.
  • Kryštufek B, Tvrtković N, Paunović M, Ozkan B (2009). Size variation in the northern white-breasted hedgehog Erinaceus roumanicus : latitudinal cline and the island rule. Mammalia 73: 299-306.
  • Librado P, Rozas J (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451- 1452.
  • Miller MA, Pfeiffer W, Schwartz T (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE); 14 November 2010; New Orleans, LA, USA. Piscataway, NJ, USA: IEEE, pp. 1-8.
  • Palsbøll PJ, Berube M, Allendorf FW (2007). Identification of management units using population genetic data. Trends Ecol Evol 22:11-16.
  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012).
  • MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61: 539-542.
  • Santucci F, Emerson BC, Hewitt GM (1998). Mitochondrial DNA phylogeography of European hedgehogs. Mol Ecol 7: 1163- 1172.
  • Savić IR (2008). Diversification of the Balkan fauna: its origin, historical development and present status. In: Makarov SE, Dimitrijević RN, editors. Advances in Arachnology and Developmental Biology: Papers Dedicated to Professor Božidar P. M. Ćurčić. Belgrade, Serbia: SASA & UNESCO MAB Serbia, pp. 57-78.
  • Schaschl H, Lymberakis P, Suchentrunk F (2002). On allozyme and cyt-b gene characteristics of Cretan hedgehogs, Erinaceus concolor nesiotes Bate, 1906. Mamm Biol 67: 257-267.
  • Schmitt T (2007). Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Front Zool 4: 11.
  • Schmitt T, Varga Z (2012). Extra-Mediterranean refugia: the rule and not the exception? Front Zool 9: 22.
  • Schwartz MK, Luikart G, Waples RS (2007.) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22: 25-33.
  • Seddon JM, Santucci F, Reeve NJ, Hewitt GM (2001). DNA footprints of European hedgehogs, Erinaceus europaeus and E. concolor : Pleistocene refugia, postglacial expansion and colonization routes. Mol Ecol 10: 2187-2198.
  • Seddon JM, Santucci F, Reeve N, Hewitt GM (2002). Caucasus Mountains divide postulated postglacial colonization routes in the white-breasted hedgehog, Erinaceus concolor . J Evolution Biol 15: 463-467.
  • Sommer RS (2007). When east met west: the sub-fossil footprints of the west European hedgehog and the northern white-breasted hedgehog during the Late Quaternary in Europe. J Zool 273: 82-89.
  • Stefanović M, Veličković N, Ćosić N, Ćirović D, Đan M (2016). Genetic variability of Northern white-breasted hedgehog ( Erinaceus roumanicus ) from Serbia. Balkan Journal of Wildlife Research 3: 1-6.
  • Suchentrunk F, Haiden A, Hartl GB (1998). On biochemical genetic variability and divergence of the two hedgehog species Erinaceus europaeus and E. concolor in central Europe. Z Saugetierkunde 63: 257-265.
  • Taberlet P, Fumagalli L, Wust-Saucy AG, Cossons JF (1998). Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7: 453-464.
  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30: 2725-2729.
  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997). The Clustal W windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
  • Veličković N, Djan M, Ferreira E, Stergar M, Obreht D, Maletić V, Fonseca C (2015). From north to south and back: the role of the Balkans and other southern peninsulas in the recolonization of Europe by wild boar. J Biogeogr 42: 716-728.
  • Zachos FE, Hartl GB (2011). Phylogeography, population genetics and conservation of the European red deer Cervus elaphus. Mammal Rev 41: 138-150.