Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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).

  • 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: https://doi.org/www.iucnredlist.org (accessed on 25.03.13).

  • Avise, J.C., 2000. Phylogeography: The History of Formation of Species. Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Baker, R.J., Bradley, R.D., 2006. Speciation in mammals and the genetic species concept. Journal of Mammalogy 87, 643–662.

    Article  PubMed  Google Scholar 

  • Bandelt, H.J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bernatchez, L., Wilson, C.C., 1998. Comparative phylogeography of nearctic and palearctic fishes. Molecular Ecology 7, 431–452.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bright, P.W., Morris, P.A., 1993. Foraging behaviour of dormice Muscardinus avellanarius intwo contrasting habitats. Journal of Zoology 230, 69–85.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Conroy, C.J., Cook, J.A., 2000. Molecular systematics of a holarctic rodent (Microtus: Muridae). Journal of Mammalogy 81, 344–359.

    Article  Google Scholar 

  • 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 

  • Drummond, A., Rambaut, A., 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Guindon, S., Gascuel, O., 2003. A simple, fast, and accurate algorithm to estimate phylogenies by maximum likelihood. Systematic Biology 52, 696–704.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hewitt, G.M., 1999. Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society 68, 87–112.

    Article  Google Scholar 

  • Hewitt, G.M., 2000. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913.

    Article  CAS  PubMed  Google Scholar 

  • Hewitt, G.M., 2004. The structure of biodiversity ‒ insight from molecular phylogeography. Frontiers in Zoology 1, 4 (26.10.04).

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck, J.P., Ronquist, F., 2001. MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Jaarola, M., Searle, J.B., 2002. Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Molecular Ecology 11, 2613–2621.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kowalski, K., 2001. Pleistocene rodents of Europe. Folia Quaternaria 72, 3–389.

    Google Scholar 

  • Krystufek, B., 2010. Glis glis (Rodentia: Gliridae). Mammalian Species 42 (865), 195–206.

    Article  Google Scholar 

  • Krystufek, B., Vohralík, V., 2005. Mammals of Turkey and Cyprus. Rodentia I: Sciuridae, Dipodidae, Gliridae, Arvicolinae. Založba Annales, Koper.

    Google Scholar 

  • 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 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • McKenzie, J.A., 1999. From desert to deluge in the Mediterranean. Nature 400, 613–614.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Nylander, J.A.A., 2004. Mrmodeltes, Version 2.2. Uppsala University, Department of Systematic Zoology, Uppsala.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Posada, D., 2008.JModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  • Posada, D., Crandall, K.A., 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.

    Article  CAS  PubMed  Google Scholar 

  • Rambaud, A., Drummond, A.J., 2007. TRACER, Version 1.4, Available at: https://doi.org/beast.bio.ed.ac.uk/Software/Tracer

  • Rambaut, A., Drummond, A.J., 2009. TRACER v1.5, Available at: https://doi.org/beast.bio.ed.ac.uk/Software/Tracer

  • 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 

  • Ronquist, F., Huelsenbeck, J.P., 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Shimodaira, H., Hasegawa, M., 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114–1116.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Swofford, D.L., 2002. PAUP*. Phylogenetic Analysis using Parsimony (*and Other Methods). Version 4.0b10. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

  • West, R.G., 1977. Pleistocene Geology and Biology with Special Reference to the British Isles. Longman, London.

  • Yannic, G., Burri, R., Malikov, V.G., Vogel, P., 2012. Systematics of snow voles (Chionomys, Arvicolinae) revisited. Molecular Phylogenetics and Evolution 62, 806–815.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Fisheries and Environmental Sciences, Faculty of Natural Resources, University of Tehran, Karaj, Iran

    Gholamreza Naderi, Mohammad Kaboli & Mahmoud Karami

  2. University of Primorska, Science and Research Center Koper, Institute for Biodiversity Studies, Si-6000, Koper, Slovenia

    Toni Koren, Sara Zupan & Boris Krystufek

  3. Environmental Science Department, Gorgan University of Agricultural, Sciences and Natural Resources, Gorgan, Iran

    Hamid R. Rezaei

Authors
  1. Gholamreza Naderi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohammad Kaboli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Toni Koren
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mahmoud Karami
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sara Zupan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hamid R. Rezaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Boris Krystufek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mohammad Kaboli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Naderi, G., Kaboli, M., Koren, T. et al. Mitochondrial evidence uncovers a refugium for the fat dormouse (Glis glis Linnaeus, 1766) in Hyrcanian forests of northern Iran. Mamm Biol 79, 202–207 (2014). https://doi.org/10.1016/j.mambio.2013.12.001

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2013.12.001

Keywords

Search

Navigation