Mammalian Biology

, Volume 79, Issue 3, pp 202–207 | Cite as

Mitochondrial evidence uncovers a refugium for the fat dormouse (Glis glis Linnaeus, 1766) in Hyrcanian forests of northern Iran

  • Gholamreza Naderi
  • Mohammad KaboliEmail author
  • Toni Koren
  • Mahmoud Karami
  • Sara Zupan
  • Hamid R. Rezaei
  • Boris Krystufek
Original Investigation


Fat dormouse is a squirrel-like rodent which is closely tied to deciduous forest ecosystem in southwestern Eurasia. As such it is a valuable indicator of forest survival in refugia during glacial-interglacial periods. Previous phylogeographic analyses uncovered divergent fat dormouse lineages in southern refugia in Italy and the Balkans, but retrieved a surprisingly low overall genetic diversity across the majority of the species’ range. We explored 812 bp long fragment of a cytochrome b (cyt b) gene in ten fat dormice from refugial Hyrcanian forests in northern Iran. We identified 10 new cyt b haplotypes, which generated a total dataset of 28 fat dormouse haplotypes. The phylogenetic reconstruction clustered the new haplotypes into the Iranian lineage which hold a sister position against all other fat dormouse haplotypes from Europe and Asia Minor. The divergence between these lineages suggests a fragmentation event of an ancestral population at 5.76 mya (95% HPD = 3.21–8.92). This early evolutionary divergence was possibly triggered in the Middle East by dramatically divergent environmental conditions at the Messinian Salinity Crisis. The divergence clearly exceeds the intraspecific divergence, and is well within the range between congeneric rodent species. We suggest a long-term persistence of the Iranian lineage in the Hyrcanian refugium which is consitent with a high number of endemics along the southern Caspian coastal areas.


Cytochrome b Phylogeography Quaternary history Hyrcanian refugium 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Akhani, H., Djamali, M., Ghorbanalizadeh, A., Ramezani, E., 2010. Plant biodiversity of Hyrcanian relict forests, N Iran: an overview of the flora, vegetation, palaeoecology and conservation. PakistanJournal of Botany 42, 231–258 (Special Issue).Google Scholar
  2. Amori, G., Hutterer, R., Krystufek, B., Yigit, N., Mitsain, G., Munoz, L.J.P., Meinig, H., Juskaitis, R., 2008. Glis glis. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2, Available at: (accessed on 25.03.13).
  3. Avise, J.C., 2000. Phylogeography: The History of Formation of Species. Harvard University Press, Cambridge, MA.Google Scholar
  4. Baker, R.J., Bradley, R.D., 2006. Speciation in mammals and the genetic species concept. Journal of Mammalogy 87, 643–662.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bandelt, H.J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bentz, S., Montgelard, C., 1999. Systematic position of the African dormouse Graphiurus (Rodentia, Gliridae) assessed from cytochrome b and 12S rRNA mitochondrial genes. Journal of Mammalian Evolution 6, 67–83.CrossRefGoogle Scholar
  7. Bernatchez, L., Wilson, C.C., 1998. Comparative phylogeography of nearctic and palearctic fishes. Molecular Ecology 7, 431–452.CrossRefGoogle Scholar
  8. Bilton, D.T., Mirol, P.M., Mascheretti, S., Fredga, J., Zima, J., Searle, J.B., 1998. Mediterranean Europe as anareaofendemism for small mammals rather than a source for northwards postglacial colonization. Proceedings of the Royal Society B, Biological Sciences 265, 1219–1226.PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bright, P.W., Morris, P.A., 1993. Foraging behaviour of dormice Muscardinus avellanarius intwo contrasting habitats. Journal of Zoology 230, 69–85.CrossRefGoogle Scholar
  10. Castiglia, R., Annesi, F., Cattaneo, C., Grano, M., Milana, G., Amori, G., 2012. A new mitochondrial lineage in the edible dormouse, Glis glis (Rodentia: Gliridae), from Alonissos island (Sporades archipelago, Greece). Folia Zoologica 61, 177–180.CrossRefGoogle Scholar
  11. Conroy, C.J., Cook, J.A., 2000. Molecular systematics of a holarctic rodent (Microtus: Muridae). Journal of Mammalogy 81, 344–359.CrossRefGoogle Scholar
  12. Daams, R., de Bruijn, D., 1995. A classification of the Gliridae (Rodentia) on the basis of dental morphology. Hystrix (N. S.) 6, 3–50.Google Scholar
  13. Drummond, A., Rambaut, A., 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Eastwood, W.J., 2004. East Mediterranean vegetation and climate change. In: Griffiths, H.I., Krystufek, B., Reed, J.M. (Eds.), Balkan Biodiversity: Pattern and Process in the European Hotspot. Kluwer Academic Publishers, Dordrecht, pp. 25–48.CrossRefGoogle Scholar
  15. Ewing, B., Hillier, L., Wendl, M.C., Green, P., 1998. Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Research 8, 175–185.PubMedCrossRefPubMedCentralGoogle Scholar
  16. Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin version 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
  17. Gautier, F., Clauzon, G., Suc, J.P., Cravatte, J., Violanti, D., 1994. Age and duration of the Messinian salinity crisis. Comptes Rendus de l’Académie des Sciences, Paris (IIA) 318, 1103–1109.Google Scholar
  18. Graur, D., Martin, W., 2004. Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends in Genetics 20 (2), 80–86.PubMedCrossRefGoogle Scholar
  19. Guindon, S., Gascuel, O., 2003. A simple, fast, and accurate algorithm to estimate phylogenies by maximum likelihood. Systematic Biology 52, 696–704.PubMedCrossRefPubMedCentralGoogle Scholar
  20. Haynes, S., Jaarola, M., Searle, J.B., 2003. Phylogeography of the common vole (Microtus arvalis) with particular emphasis on the colonization of the Orkney archipelago. Molecular Ecology 12, 951–956.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Helvaci, Z., Renaud, S., Ledevin, R., Adriaens, D., Michaux, J., Colak, R., Kankilic, T., Kandemir, I., Yigit, N., Colak, E., 2012. Morphometric and genetic structure of the edible dormouse (Glis glis): a consequence of forest fragmentation in Turkey. Biological Journal of the Linnean Society 107, 611–623.CrossRefGoogle Scholar
  22. Hewitt, G.M., 1999. Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society 68, 87–112.CrossRefGoogle Scholar
  23. Hewitt, G.M., 2000. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Hewitt, G.M., 2004. The structure of biodiversity ‒ insight from molecular phylogeography. Frontiers in Zoology 1, 4 (26.10.04).PubMedPubMedCentralCrossRefGoogle Scholar
  25. Ho, S.Y.W., Phillips, M.J., Cooper, A., Drummond, A.J., 2005. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Molecular Biology and Evolution 22, 1561–1568.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Huelsenbeck, J.P., Ronquist, F., 2001. MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.CrossRefGoogle Scholar
  27. Hürner, H., Krystufek, B., Sarà, M., Ribas, A., Ruch, T., Sommer, R., Ivashkina, V., Michaux, J.R., 2010. Mitochondrial phylogeography of the edible dormouse (Glis glis) in the Western Palearctic Region. Journal of Mammalogy 91, 233–242.CrossRefGoogle Scholar
  28. Jaarola, M., Searle, J.B., 2002. Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Molecular Ecology 11, 2613–2621.PubMedCrossRefPubMedCentralGoogle Scholar
  29. Kelt, D.A., Brown, J.H., Heske, E.J., Marquet, P.A., Morton, S.R., Reid, J.R.W., Rogovin, K.A., Shenbrot, G., 1996. Community structure of desert small mammals: comparisons across four continents. Ecology 77, 746–761.CrossRefGoogle Scholar
  30. Kowalski, K., 2001. Pleistocene rodents of Europe. Folia Quaternaria 72, 3–389.Google Scholar
  31. Krystufek, B., 2010. Glis glis (Rodentia: Gliridae). Mammalian Species 42 (865), 195–206.CrossRefGoogle Scholar
  32. Krystufek, B., Vohralík, V., 2005. Mammals of Turkey and Cyprus. Rodentia I: Sciuridae, Dipodidae, Gliridae, Arvicolinae. Založba Annales, Koper.Google Scholar
  33. Lo Brutto, S., Sará, M., Arculeo, M., 2011. Italian Peninsula preserves an evolutionary lineage ofthe fat dormouse Glis glis L. (Rodentia: Gliridae). Biological Journal of the Linnean Society 102, 11–21.Google Scholar
  34. Maldonado, A., 1985. Evolution of the Mediterranean basins and a detailed reconstruction of the Cenozoic paleoceanography. In: Margalef, R. (Ed.), Key Environments. Western Mediterranean. Pergamon Press, Oxford, pp. 17–59.Google Scholar
  35. Martin, A.P., Palumbi, S.R., 1993. Protein evolution in different cellular environments: cytochrome b in sharks and mammals. Molecular Biology and Evolution 10, 873–891.PubMedPubMedCentralGoogle Scholar
  36. McKenzie, J.A., 1999. From desert to deluge in the Mediterranean. Nature 400, 613–614.CrossRefGoogle Scholar
  37. Michaux, J.R., Magnanou, E., Paradis, E., Nieberding, C., Libois, R., 2003. Mitochondrial phylogeography of the Woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Molecular Ecology 12, 685–697.PubMedCrossRefPubMedCentralGoogle Scholar
  38. Mouton, A., Grill, A., Sarà, M., Kryštufek, B., Randi, E., Amori, G., Juskaitis, R., Aloise, G., Mortelliti, A., Panchetti, F., Michaux, J., 2012. Evidence of a complex phylogeographic structure in the common dormouse, Muscardinus avellanarius (Rodentia: Gliridae). Biological Journal of the Linnean Society 105, 648–664.CrossRefGoogle Scholar
  39. Musser, G.G., Carleton, M.D., 2005. Superfamily Muroidea. In: Wilson, D.E., Reeder, DAM (Eds.), Mammal Species of the World. A Taxonomic and Geographic Reference, vol. 2, 3rd ed. John Hopkins University Press, Baltimore, CA, pp. 894–1531.Google Scholar
  40. Nylander, J.A.A., 2004. Mrmodeltes, Version 2.2. Uppsala University, Department of Systematic Zoology, Uppsala.Google Scholar
  41. Perez, G.C.L., Libois, R., Nieberding, C.M., 2013. Phylogeography ofthe garden dormouse Eliomys quercinus in the western Palearctic region. Journal of Mammalogy 94, 202–217.CrossRefGoogle Scholar
  42. Posada, D., 2008.JModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Posada, D., Crandall, K.A., 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Rambaud, A., Drummond, A.J., 2007. TRACER, Version 1.4, Available at:
  45. Rambaut, A., Drummond, A.J., 2009. TRACER v1.5, Available at:
  46. Röhrig, E., 1991. Deciduous forests of the Near East. In: Röhrig, E., Ulrich, B. (Eds.), Ecosystems of the World 7: Temperate Deciduous Forests. Elsevier, Amsterdam, pp. 527–537.Google Scholar
  47. Ronquist, F., Huelsenbeck, J.P., 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X., Rozas, R., 2003. DNASP, DNA polymorphism analyses by the coalescent and ot her methods. Bioinformatics 19, 2496–2497.CrossRefGoogle Scholar
  49. Shen, X.J., Tsudzuki, H., Nakamura, T., 1999. Primer design and sequence information forcytochrome b gene in the Chinese painted quail (Excalfactoria chinensis). Animal Science Journal 70, 240–242.Google Scholar
  50. Shimodaira, H., Hasegawa, M., 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114–1116.CrossRefGoogle Scholar
  51. Svenning, J.C., Normand, S., Kageyama, N., 2008. Glacial refugia of temperate trees in Europe: insights from species distribution modelling. Journal of Ecology 96, 1117–1127.CrossRefGoogle Scholar
  52. Swofford, D.L., 2002. PAUP*. Phylogenetic Analysis using Parsimony (*and Other Methods). Version 4.0b10. Sinauer Associates, Sunderland, MA.Google Scholar
  53. Tamura, T., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Tarkhnishvili, D., Gavashelishvili, A., Mumladze, L., 2012. Palaeoclimatic models help to understand current distribution of Caucasian forest species. Biological Journal ofthe Linnean Society 105, 231–248.CrossRefGoogle Scholar
  55. Ünay, E., 1994. Early Miocene rodent faunas from the eastern Mediterranean area: Part IV. The Gliridae. In: Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappe, Ser. B 97, pp. 445–490.Google Scholar
  56. West, R.G., 1977. Pleistocene Geology and Biology with Special Reference to the British Isles. Longman, London.Google Scholar
  57. Yannic, G., Burri, R., Malikov, V.G., Vogel, P., 2012. Systematics of snow voles (Chionomys, Arvicolinae) revisited. Molecular Phylogenetics and Evolution 62, 806–815.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2014

Authors and Affiliations

  • Gholamreza Naderi
    • 1
  • Mohammad Kaboli
    • 1
    Email author
  • Toni Koren
    • 2
  • Mahmoud Karami
    • 1
  • Sara Zupan
    • 2
  • Hamid R. Rezaei
    • 3
  • Boris Krystufek
    • 2
  1. 1.Department of Fisheries and Environmental Sciences, Faculty of Natural ResourcesUniversity of TehranKarajIran
  2. 2.University of Primorska, Science and Research Center KoperInstitute for Biodiversity StudiesKoperSlovenia
  3. 3.Environmental Science DepartmentGorgan University of Agricultural, Sciences and Natural ResourcesGorganIran

Personalised recommendations