Journal of Mammalian Evolution

, Volume 22, Issue 4, pp 583–595 | Cite as

Phylogenetic Relationships of Apodemus Kaup, 1829 (Rodentia: Muridae) Species in the Eastern Mediterranean Inferred from Mitochondrial DNA, with Emphasis on Iranian Species

  • Jamshid Darvish
  • Zeinolabedin Mohammadi
  • Fatemeh Ghorbani
  • Ahmad Mahmoudi
  • Sylvain Dubey
Original Paper


Wood mice of the genus Apodemus are widely distributed in Eurasia, with the Eastern Mediterranean being considered as a hotspot. Indeed, numerous species have been documented in Iran, including A. witherbyi, A. hyrcanicus, A. uralensis, A. avicennicus, A. hermonensis, and A. arianus. In this study, 129 specimens were collected from different Iranian localities and two specimens from Afghanistan. The animals were identified taxonomically and their phylogenetic relationships were investigated using cytochrome b mitochondrial DNA sequences. Five species of the genus Apodemus were identified in Iran, including A. hyrcanicus, A. witherbyi, A. cf. ponticus, A. uralensis, and A. mystacinus, beside, A. pallipes from Afghanistan. This study found no evidence of A. flavicollis or A. sylvaticus in Iran, despite their occurrence in Turkey, shedding doubt on the status of A. flavicollis in Iran, Asia Minor, and the Levant. Phylogenetic analyses imply that A. witherbyi has priority over A. avicennicus, A. hermonensis, and A. iconicus. Estimation of the divergence time for these taxa suggests a separation at around 7.2 Ma for the subgenera Karstomys (including A. mystacinus and A. epimelas) and Sylvaemus (including A. flavicollis, A. sylvaticus, A. uralensis, A. pallipes, A. hyrcanicus, A. witherbyi, and A. cf. ponticus). Within the subgenus Karstomys, the divergence times for A. mystacinus and A. epimelas were between 3.0 and 6.1 Ma, and divergence times within the subgenus Sylvaemus were between 5.2 and 6.9 Ma for A. witherbyi and other species in this subgenus. It is postulated that vicariance events including the uplifting of the Zagros Mountains and Anatolian Plateau in the middle Miocene and climate oscillations during the Messinian Salinity Crisis besides formation of the Hyrcanian tertiary forests during the Neogene probably played substantial roles in the radiation and distribution of the genus Apodemus in the Eastern Mediterranean.


Phylogeography Apodemus Cyt b Divergence time Iran 



This research was supported by grants from Pasteur Institute of Iran under project (No 92–242), Department of Environment of Yazd Province, Iran (No.121-32217), and Vector-borne Diseases Research Center, North Khorasan University of Medical Sciences, Bojnurd, Iran (No. 1.19727). The authors are indebted to Hitoshi Suzuki for providing two sequences (HS1102 and Mys 2) and Johan Michaux for his kind consultation.


  1. Ahmadzadeh F, Carretero MA, Rödder D, Harris DJ, Freitas SN, Perera A, Böhme W (2013) Inferring the effects of past climate fluctuations on the distribution pattern of Iranolacerta (Reptilia, Lacertidae): evidence from mitochondrial DNA and species distribution models. Zool Anz 252:141–148CrossRefGoogle Scholar
  2. Akgün F, Kayseri MS, Akkiraz MS (2007) Palaeoclimatic evolution and vegetational changes during the late Oligocene–Miocene period in Western and Central Anatolia (Turkey). Palaeogeogr Palaeoclimatol Palaeoecol 253:56–90CrossRefGoogle Scholar
  3. 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. Pak J Bot 42:231–258Google Scholar
  4. Aydar E, Çubukçu HE, Şen E, Akin L (2013) Central Anatolian Plateau, Turkey: incision and paleoaltimetry recorded from volcanic rocks. Turkish J Earth Sci 22:739–746CrossRefGoogle Scholar
  5. Balakirev AE, Baskevich MI, Gmyl AP, Okulova NM, Andreeva TA, Sokolenko OV, Malygin VM, Khlyap LA, Oparin ML, Orlov VN (2007) On the taxonomic rank of ciscaucasicus and its relationships with the pygmy wood mouse Sylvaemus uralensis inferred from the mtDNA cytochrome b gene sequence. Genetika 43:1651–1666PubMedGoogle Scholar
  6. Barčiová L, Macholán M (2009) Morphometric key for the discrimination of two wood mice species, Apodemus sylvaticus and A. flavicollis. Acta Zool Acad Sci Hung 55:31–38Google Scholar
  7. Barry JC, Johnson NM, Raza SM, Jacobs LL (1985) Neogene mammalian faunal change in southern Asia: correlations with climatic, tectonic, and eustatic events. Geology 13:637–640CrossRefGoogle Scholar
  8. Bellinvia E (2004) A phylogenetic study of the genus Apodemus by sequencing the mitochondrial DNA control region. J Zool Syst Evol Res 42:289–297CrossRefGoogle Scholar
  9. Blanford WT (1875) Descriptions of new Mammalia from Persia and Baluchistan. Ann Mag Nat Hist London, 4th Series, 16:309–313Google Scholar
  10. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLoS Comput Biol 10: e1003537PubMedCentralCrossRefPubMedGoogle Scholar
  11. Brachert TC, Reuter M, Felis T, Kroeger KF, Lohmann G, Micheels A, Fassoulas C (2006) Porites corals from Crete (Greece) open a window into late Miocene (10 Ma) seasonal and interannual climate variability. Earth Planet Sci Lett 245:81–94CrossRefGoogle Scholar
  12. Bruford MW, Hanotte O, Brokfield JFY, Burke T (1992) Single-locus and multilocus DNA fingerprinting. In: Hoelzel AR (ed) Molecular Genetic Analysis of Populations: A Practical Approach. Oxford University Press, New York, pp 225–269Google Scholar
  13. Bugarski-Stanojevic V, Blagojevic J, Adna–devic T, Jojic V, Vujosevic M (2008) Molecular phylogeny and distribution of three Apodemus species (Muridae, Rodentia) in Serbia. J Zool Syst Evol Res 46:278–286CrossRefGoogle Scholar
  14. Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158CrossRefGoogle Scholar
  15. Chelomina GN, Atopkin DM (2010) Molecular genetic evidence of a deep phylogenetic discontinuity between the Asian and European races of pygmy wood mouse based on the mitochondrial cytochrome b gene variation. Mol Biol 44:699–708CrossRefGoogle Scholar
  16. Chevret P, Veyrunes F, Britton-Davidian J (2005) Molecular phylogeny of the genus Mus (Rodentia: Muridae) based on mitochondrial and nuclear data. Biol J Linn Soc 84:417–427CrossRefGoogle Scholar
  17. Cheylan M (1995) Les reptiles du Pale´artique occidental. Diversite´ et Conservation. Doctoral dissertation (unpublished), Laboratoire de Bioge´ographie et Ecologie des Verte´bre´ s, Montpellier, pp 339Google Scholar
  18. Clauzon G, Suc JP, Gautier F, Berger A, Loutre MR (1996) Alternate interpretation of the Messinian salinity crisis: controversy resolved? Geology 24:363–366CrossRefGoogle Scholar
  19. Corbet GB (1978) The Mammals of the Palaearctic Region, A Taxonomic Review. British Museum (Natural History), LondonGoogle Scholar
  20. Darviche D, Benmehdi F, Britton-Davidian J, Thaler L (1979) Donnees preliminaries sur la systematique biochimique des genres Mus et Apodemus en Iran. Mammalia 43:427–430Google Scholar
  21. Darvish J, Akbary Rad S, Siahsarvieh R, HosseinPour Feizi MA, Ghorbani F (2010) New record on pigmy field mouse (Muridae, Rodentia) from Northeast Iran. Hystrix 21:115–126Google Scholar
  22. Darvish J, Javidkar M, Siahsarvie R (2006) New species of wood mouse of genus Apodemus (Rodentia: Muridae) from Iran. Zool Middle East 38:5–16CrossRefGoogle Scholar
  23. Darvish J, Mohammadi Z, Ghorbani F, Mostafavi E (2014) Morphological morphometric characterisation of the eastern broad-toothed field mouse Apodemus mystacinus (Rodentia: Muridae) from Zagros Mountains, north-western Iran. Acta zool bulg 66:461–468Google Scholar
  24. De Bonis L, Brunet M, Heintz E, Sen S (1993) La province Greco-irano-afgane et la repartition des faunes mammaliennes au Miocene superieur. Paleontol Evol 24–25:96–106Google Scholar
  25. Dercourt J, Ricou LE, Vrielynck B (1993) Atlas Tethys Paleoenvironmental Maps. Gauthiers-Villars, ParisGoogle Scholar
  26. Djamali M (2008) Palaeoenvironmental changes in Iran during the last two climatic cycles (vegetation-climate-anthropisation). PhD thesis, Université Paul Cézanne (Aix-Marseille), Faculté des Sciences et TechniquesGoogle Scholar
  27. Drummond AJ, Ho SYW, Rawlence N, Rambaut A (2007) A rough guide to BEAST 1.4. Available at: Scholar
  28. Dubey S, Cosson JF, Vohralik V, Kryštufek B, Diker E, Vogel P (2007) Molecular evidence of Pleistocene bidirectional faunal exchange between Europe and the Near East: the case of the bicoloured shrew (Crocidura leucodon, Soricidae). J Evol Biol 20:1799–1808CrossRefPubMedGoogle Scholar
  29. Ellerman JR, Morrison-Scott TCS (1951) Checklist of Palaearctic and Indian Mammals 1758 to 1946. Trustees of the British Museum (Natural History), LondonGoogle Scholar
  30. Etemad E (1978) The Mammals of Iran. Rodents and Key to Their Classification (Vol. 1). National Society for Protection of Natural Resources and Human Environment, Teheran (in Farsi, with a summary in English)Google Scholar
  31. Fauquette S, Clauzon G, Suc JP, Zheng Z (1999) A new approach for palaeoaltitude estimates based on pollen records: example of the Mercantour massif (southeastern France) at the earliest Pliocene. Earth Planet Sci Lett 170:35–47CrossRefGoogle Scholar
  32. Fauquette S, Guiot J, Suc JP (1998) A method for climatic reconstruction of the Mediterranean Pliocene using pollen data. Palaeogeogr Palaeoclimatol Palaeoecol 144:183–201CrossRefGoogle Scholar
  33. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  34. Filippucci MG, Simson S, Nevo E (1989) Evolutionary biology of the genus Apodemus Kaup, 1829 in Israel. Allozymic and biometric analyses with description of a new species: Apodemus hermonensis (Rodentia, Muridae). Monit Zool 56:361–376Google Scholar
  35. Firouz E (2008) A Guide to the Fauna of Iran (Vertebrates). Iran University Press, Tehran (in Farsi)Google Scholar
  36. Fortelius M, Eronen J, Liu L, Pushkina D, Tesakov A, Vislobokova I, Zhang Z (2006) Late Miocene and Pliocene large land mammals and climatic changes in Eurasia. Palaeogeogr Palaeoclimatol Palaeoecol 238:219–227CrossRefGoogle Scholar
  37. Ghorbani F, Darvish J, Kami HG, Mirshamsi O (2010) Rodent fauna of the western Golestan Province in northeast Iran. IJAB 6:37–48Google Scholar
  38. Golonka J (2004) Plate tectonic evolution of the southern margin of Eurasia in the Mesozoic and Cenozoic. Tectonophysics 381:235–273CrossRefGoogle Scholar
  39. Goodwin GG (1940) Mammals collected by the Legendre 1938 Iran expedition. American Museum Novitates 1082:1–17Google Scholar
  40. Guest B, Guest A, Axen G (2007) Late Tertiary tectonic evolution of northern Iran: a case for simple crustal folding. Global Planet Change 58:435–453CrossRefGoogle Scholar
  41. Hadid Y, Nemeth A, Snir S, Pavlıcek T, Csorba G, Kazmer M, Major A, Mezhzherin S, Rusin M, Coskun Y, Nevo E (2012) Is evolution of blind mole rats determined by climate oscillations? PLoS ONE 7:e30043PubMedCentralCrossRefPubMedGoogle Scholar
  42. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95⁄98⁄NT. Nucleic Acids SympSer 41:95–98Google Scholar
  43. Hoofer SR, Gaschak S, Dunina-Barkovskaya Y, Makluk J, Meeks HN, Wickliffe JK, Baker RJ (2007) New information for systematics, taxonomy, and phylogeography of the rodent genus Apodemus (Sylvaemus) in Ukraine. J Mammal 88:330–342CrossRefGoogle Scholar
  44. Hsu KJ, Montadert L, Bernoulli D, Cita MB, Erickson A, Garrison RE, Kidd RB, Melieres F, Muller C, Wright R (1977) History of the Mediterranean salinity crisis. Nature 267:399–403CrossRefGoogle Scholar
  45. Huelsenbeck JP, Ronquist FR, Teslenko M (2011) MRBAYES: Bayesian inference of phylogeny.
  46. Jangjoo M, Darvish J, Vigne JD (2011) Application of outline analysis on fossil and modern specimens of Apodemus. IJAB 7:143–155Google Scholar
  47. Javidkar M, Darvish J, RiahiBakhtiari A (2005) Discriminate analysis of dental and cranial characteristics in Apodemus hyrcanicus and A. hermonensis (Rodentia, Muridae) from Iran. Zool Middle East 35:5–12CrossRefGoogle Scholar
  48. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Mol Evol 15:111–120CrossRefGoogle Scholar
  49. Koufos GD, Konidaris GE (2011) Late Miocene carnivores of the Greco-Iranian Province: composition, guild structure and palaeoecology. Palaeogeogr Palaeoclimatol Palaeoecol 305:215–226CrossRefGoogle Scholar
  50. Koufos GD, Kostopoulos DS, Vlachou TD (2005) Neogene/Quaternary mammalian migrations in Eastern Mediterranean. Belg J Zool 135:181–190Google Scholar
  51. Kovar-Eder J, Kvaček Z, Martinetto E, Roiron P (2006) Late Miocene to early Pliocene vegetation of southern Europe (7–4Ma) as reflected in the megafossil plant record. Palaeogeogr Palaeoclimatol Palaeoecol 238:321–339CrossRefGoogle Scholar
  52. Krijgsman W, Hilgen FJ, Raffi I, Sierro FJ, Wilson DS (1999) Chronology, causes and progression of the Messinian salinity crisis. Nature 400:652–655CrossRefGoogle Scholar
  53. Kryštufek B (2002) Identity of four Apodemus (Sylvaemus) types from the Eastern Mediterranean and the Middle East. Mammalia 66:43–51Google Scholar
  54. Kryštufek B, Hutterer R (2006) The Ural field mouse Apodemus uralensis–a mammal species new to Iran. Zool Middle East 38:111–112CrossRefGoogle Scholar
  55. Kryštufek B, Mozetic Francky B (2005) Mt. Hermon field mouse Apodemus iconicus is a member of the European mammal fauna. Folia Zool 54:69–74Google Scholar
  56. Kryštufek B, Vohralik V (2009) Mammals of Turkey and Cyprus. Rodentia II: Cricetinae, Muridae, Spalacidae, Calomyscidae, Capromyidae, Hystricidae, Castoridae. Knjižnica Annales MajoraGoogle Scholar
  57. Kryštufek B, Vohralík V, Obuch J (2009) Endemism, vulnerability and conservation issues for small terrestrial mammals from the Balkans and Anatolia. Folia Zool 58: 291–302Google Scholar
  58. Lay DM (1967) A study of the mammals of Iran resulting from the Street Expedition of 1962–63. Fieldiana Zool 54:1–282Google Scholar
  59. Leestmans R (2005) Le refuge caspiens et son importance en biogéographie. Linn Belg 20:97–102Google Scholar
  60. Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  61. Macey JR, Schulte JA, Ananjeva NB, Larson A, Rastegar-Pouyani N, Shammakov SM, Papenfuss TJ (1998) Phylogenetic relationships among agamid lizards of the Laudakia caucasia species group: testing hypotheses of biogeographic fragmentation and an area cladogram for the Iranian Plateau. Mol Phylogenet Evol 10:118–131CrossRefPubMedGoogle Scholar
  62. Macholán M, Filippucci MG, Benda P, Frynta D, Sádlová J (2001) Allozyme variation and systematics of the genus Apodemus (Rodentia: Muridae) in Asia Minor and Iran. J Mammal 82:799–813CrossRefGoogle Scholar
  63. Manafzadeh S, Salvo G, Conti E (2013) A tale of migrations from east to west: the Irano-Turanian floristic region as a source of Mediterranean xerophytes. J Biogeogr doi: 10.1111/jbi.12185 Google Scholar
  64. Michaux J, Bellinvia E, Lymberakis P (2005a) Taxonomy, evolutionary history and biogeography of the broad-toothed field mouse (Apodemus mystacinus) in the Eastern Mediterranean area based on mitochondrial and nuclear genes. Biol J Linn Soc 85:53–63CrossRefGoogle Scholar
  65. Michaux J, Chevret P, Filippucci MG, Macholán M (2002) Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: Cytochrome b and 12S rRNA. Mol Phylogenet Evol 23:123–136CrossRefPubMedGoogle Scholar
  66. Michaux JR, Libois R, Filipucci MG (2005b) So close and so different: comparative phylogeography of two small mammal species, the yellow-necked field mouse (Apodemus flavicollis) and the wood mouse (Apodemus sylvaticus) in the western Palearctic region. Heredity 94:52–63CrossRefPubMedGoogle Scholar
  67. Michaux JR, Libois R, Paradis E, Filippucci MG (2004) Phylogeographic history of the yellow-necked field mouse (Apodemus flavicollis) in Europe and in the Near and Middle East. Mol Phylogenet Evol 32:788–798CrossRefPubMedGoogle Scholar
  68. Michaux JR, Magnanou E, Paradis E, Nieberding C, Libois R (2003) Mitochondrial phylogeography of the wood mouse (Apodemus sylvaticus) in the western Palearctic region. Mol Ecol 12:685–697CrossRefPubMedGoogle Scholar
  69. Mirzaie Ataabadi M (2007) Cenozoic mammal footprints of Iran and their significance. Cenozoic Vertebrate Tracks and Traces. Bull New Mexico Mus Nat Hist Sci 42:251–260Google Scholar
  70. Mohammadi Z, Darvish J, Ghorbani F, Mostafavi E (2014) First record of the Caucasus field mouse Apodemus ponticus Sviridenko, 1936 (Rodentia Muridae) from Iran. Biodiversity Journal 5:475–480Google Scholar
  71. Mohammadi Z, Darvish J, Haddad F, Ghorbani F (2012) A karyological study of some murid rodents (Rodentia: Muridae) of Iran. Prog Biol Sci 2:30–39Google Scholar
  72. Montgelard C, Bentz S, Tirard C, Verneau O, Catzeflis FM (2002) Molecular systematic of Sciurognathi (Rodentia): the mitochondrial cytochrome b and 12S rRNA genes support the Anomaluroidea (Peptidae and Anomaluridae). Mol Phylogenet Evol 22:220–233CrossRefPubMedGoogle Scholar
  73. Mouthereau F (2011) Timing of uplift in the Zagros belt/Iranian Plateau and accommodation of late Cenozoic Arabia–Eurasia convergence. Geol Mag 148:726–738CrossRefGoogle Scholar
  74. Musser GG, Carleton MD (2005) Superfamily Muroidea. In: Wilson DE, Reeder DM (eds) Mammal Species of the World: A Taqxonomic and Geographic Reference, 3rd edn. The Johns Hopkins University Press, Baltimore, pp 894–1531Google Scholar
  75. Naseri Z, Jalal R, Darvish J (2006) Genetic study on Apodemus avicennicus and Apodemus witherbyi by RAPD-PCR. IJAB 2:77–81Google Scholar
  76. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  77. Pound MJ, Haywood AM, Salzmann U, Riding JB, Lunt DJ, Hunter SJ (2011) A Tortonian (late Miocene, 11.61-7.25 Ma) global vegetation reconstruction. Palaeogeogr Palaeoclimatol Palaeoecol 300:29–45CrossRefGoogle Scholar
  78. Pour Feizi MH, Darvish J, Pouladi N, Akbari Rad S, Siahsarvie R (2009) Biosystematics study of steppe field mouse Apodemus witherbyi (Rodentia: Muridae) from North-West Iran. IJAB 5:47–58Google Scholar
  79. Rajaei Sh H, Rödder D, Weigand AM, Dambach J, Raupach MJ, Wägele JW (2013) Quaternary refugia in southwestern Iran: insights from two sympatric moth species (Insecta, Lepidoptera). Org Divers Evol 13:409–423CrossRefGoogle Scholar
  80. Reutter BA, Hausser J, Vogel P (1999) Discriminant analysis of skull morphometric characters in Apodemus sylvaticus, A. flavicollis, and A. alpicola (Mammlia; Rodentia) from the Alps. Acta Theriol 44:299–308CrossRefGoogle Scholar
  81. Rogl F (1999) Mediterranean and Paratethys. Facts and hypotheses of an Oligocene to Miocene paleogeography (short overview). Geol Carpath 50:339–349Google Scholar
  82. Ruddiman WF, Raymo ME (1988) Northern hemisphere climate regimes during the past 3 ma: possible tectonic connections. Phil Trans R Soc London B 318:411–430CrossRefGoogle Scholar
  83. Sengor AMC, Natalin BA (1996) Paleotectonics of Asia: fragment of a synthesis. In: Yin A, Harrison TM (ed) The Tectonics of Asia. Cambridge University Press, New York, pp 486–640Google Scholar
  84. Siahsarvie R, Darvish J (2008) Geometric morphometric analysis of Iranian wood mice of the genus Apodemus (Rodentia, Muridae). Mammalia 72:109–115CrossRefGoogle Scholar
  85. Suzuki H, Filippucci MG, Chelomina GN, Sato JJ, Serizawa K, Nevo E (2008) A biogeographic view of Apodemus in Asia and Europe inferred from nuclear and mitochondrial gene sequences. Biochem Genet 46:329–346CrossRefPubMedGoogle Scholar
  86. Suzuki H, Sato JJ, Tsuchiya K, Luo J, Zhang Y-P, Wang Y-X, Jiang X-L (2003) Molecular phylogeny of wood mice (Apodemus, Muridae) in East Asia. Biol J Linn Soc 80:469–481CrossRefGoogle Scholar
  87. Suzuki H, Tsuchiya K, Takezaki N (2000) A molecular phylogenetic framework for the Ryuku endemic rodents Tokudaia osimensis and Diplothrix legata. Mol Phylogenet Evol 5:15–24CrossRefGoogle Scholar
  88. Swofford DL (2000) PAUP: Phylogenetic analysis using parsimony (*and other methods). Version 4.0b4aGoogle Scholar
  89. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  90. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCentralCrossRefPubMedGoogle Scholar
  91. Weisrock DW, Macey RJ, Ugurtas IH, Larson A, Papenfuss TJ (2001) Molecular phylogenetics and historical biogeography among salamandrids of the “true” salamander clade: rapid branching of numerous highly divergent lineages in Mertensiella luschani associated with the rise of Anatolia. Mol Phylogenet Evol 18:434–448CrossRefPubMedGoogle Scholar
  92. Weiss S, Ferrand N (2007) Phylogeography of Southern European Refugia. University of Porto, PortugalCrossRefGoogle Scholar
  93. Wessels W (1955) Miocene rodent evolution and migration (Muroidea from Pakistan, Turkey and Northern Africa). Faculty of Geosciences, Utrecht UniversityGoogle Scholar
  94. Yılmaz Y, Guner Y, Saroglu F (1998) Geology of the Quaternary volcanic centers of the east Anatolia. J Volcanol Geotherm Res 85:173–210CrossRefGoogle Scholar
  95. Zohary M (1973) Geobotanical Foundation of the Middle East. Gustav Fische Verlag Stuttgart, AmsterdamGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Jamshid Darvish
    • 1
    • 2
  • Zeinolabedin Mohammadi
    • 1
  • Fatemeh Ghorbani
    • 1
  • Ahmad Mahmoudi
    • 1
  • Sylvain Dubey
    • 3
  1. 1.Department of Biology, Faculty of SciencesFerdowsi University of MashhadMashhadIran
  2. 2.Applied Animal Institute (AAI), Rodentology Research Department (RRD)Ferdowsi University of MashhadMashhadIran
  3. 3.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland

Personalised recommendations