Genetic Divergence and Evolution of Reproductive Isolation in Eastern Mediterranean Water Frogs

  • Jörg PlötnerEmail author
  • Thomas Uzzell
  • Peter Beerli
  • Çiğdem Akın
  • C. Can Bilgin
  • Cornelia Haefeli
  • Torsten Ohst
  • Frank Köhler
  • Robert Schreiber
  • Gaston-Denis Guex
  • Spartak N. Litvinchuk
  • Rob Westaway
  • Heinz-Ulrich Reyer
  • Nicolas Pruvost
  • Hansjürg Hotz


Water frogs [genus Pelophylax (Rana)] that occur around the eastern Mediterranean Sea provide an opportunity to study early stages of speciation. The geography of the eastern Mediterranean region has changed dramatically since the Middle Miocene as a result of motions of adjoining lithospheric plates and regional-scale vertical crustal motions (uplift and subsidence). For several hundred thousand years between 6 and 5 million years ago (Mya), the Mediterranean basin was isolated from the Atlantic Ocean, and became desiccated (the Messinian Salinity Crisis; MSC). Geological data suggest that the endemic water frog lineage on Cyprus was isolated by the flooding of the Mediterranean basin by salt water at the end of the MSC, circa 5.5–5.3 Mya. This suggests a rate of uncorrected genetic divergence of approximately 1.1% per million years (My). Divergence time estimates based on this rate are in good agreement with the chronology of events in the history of crustal deformation and landscape development in the eastern Mediterranean region.

Despite a high similarity in morphology, eastern Mediterranean water frogs show considerable genetic divergence, indicating the existence of several evolutionary species at varied levels of differentiation. Based on two mitochondrial (mt) genes (ND2 and ND3), several lineages have been identified: Pelophylax bedriagae, P. cretensis, P. epeiroticus, P. ridibundus (Europe), six Anatolian lineages, all provisionally subsumed under the name P. cf. bedriagae, and a distinct lineage restricted to Cyprus. Genetic data from transition zones in eastern Greece/western Anatolia, south-western Anatolia, and south-eastern Anatolia, in concert with the results of female choice experiments, indicate that antihybridization mechanisms are only weakly developed in eastern Mediterranean water frogs. Genetic incompatibility, as expressed by average hatching rate of heterospecific crosses, increases with genetic divergence measured by uncorrected distance estimated from mtDNA sequences. Hatching rates of heterospecific crosses show an extremely high variability, however, and viable F1 hybrids originated from almost all crosses. We conclude that speciation in eastern Mediterranean water frogs follows the allopatric model and has been closely associated with the geodynamic evolution of the Mediterranean since the Middle Miocene (i.e., since ∼11 Mya).


Water frogs Pelophylax (Rana) Eastern mediterranean Genetic diversity Geology Divergence time Genetic incompatibilities Antihybridization mechanisms Speciation 



We thank Rainer Günther (Berlin) for constructive comments on the manuscript. Grateful thanks are due to Metin Bilgin (Urbana-Champaign) for DNA sequencing and the development of a new DNA extraction protocol. We thank Christina Scheib (Eberswalde), Sylvia Glaser (Berlin), Kai-Joachim Schultze (Berlin), and Ronny Knop (Berlin) for technical assistance. For providing water frog samples, we thank Wolfgang Böhme (Bonn), Petr Kotlik (Libechov), Peter Mikuliček (Prague), and Mathias Stöck (Lausanne). Tissue samples from Greece were made available by the Greek Ministry of Rural Development and Food, kindly mediated by Doris Tippmann (Embassy of the FRG, Athens). This research was supported by the Deutsche Forschungsgemeinschaft (grants PL 213/3-1, 3-2, 3-3) and the Swiss National Fund (grants 31-37579.93, 31-59144.99, 31-103903/1 and 31-64004.00). Çiğdem Akın and Can Bilgin were supported by METU Research Fund (BAP-08-11-DPT-2002K120510). Peter Beerli was partly supported by the joint NSF/NIGMS Mathematical Biology programme under NIH grant R01 GM 078985 and by NSF grant DEB 0822626. Spartak N. Litvinchuk was partly supported by a DAAD grant under A/03/06782.


  1. Aguirre E, Pasini G (1985) The pliocene-pleistocene boundary. Episodes 8:116–120Google Scholar
  2. Akef MSA, Schneider H (1989) The eastern form of Rana ridibunda (Anura: Ranidae) inhabits the Nile delta. Zool Anz 223:129–138Google Scholar
  3. Akın Ç (2007) Detection of species boundaries in the Rana ridibunda complex of southwestern Turkey using mitochondrial ND3 marker. M. Sc. Thesis, Middle East Technical University, Ankara, TurkeyGoogle Scholar
  4. Akın Ç, Bilgin M, Bilgin CC (2010) Discordance between ventral colour and mtDNA haplotype in the water frog Rana (ridibunda) caralitana, 1988 Arıkan. Amphibia-Reptilia 31:9–20CrossRefGoogle Scholar
  5. Akın Ç, Bilgin CC, Beerli P, Westaway R, Ohst T, Litvinchuk SN, Uzzell T, Bilgin M, Hotz H, Guex G-D, Plötner J (in press) Phylogeographic patterns of genetic diversity in eastern Mediterranean water frogs have been determined by geological processes and climate change in the Late Cenozoic. J BiogeographyGoogle Scholar
  6. Alpagut Keskin N, Falakalı Mutaf B (2006) Rod-shaped bivalents indicate assemblage among Anatolian water frog populations. Amphibia-Reptilia 27:47–53CrossRefGoogle Scholar
  7. Baak EJ, Rieseberg LH (2007) A genomic view of introgression and hybrid speciation. Cur Opin Gen Dev 17:513–518CrossRefGoogle Scholar
  8. Beerli P (1994) Genetic isolation and calibration of an average protein clock in the western Palearctic water frogs of the Aegean region. PhD thesis, University of Zurich, SwitzerlandGoogle Scholar
  9. Beerli P, Hotz H, Uzzell T (1996) Geological dated sea barriers calibrate a protein clock for Aegean water frogs. Evolution 50:1676–1687CrossRefGoogle Scholar
  10. Beerli P, Hotz H, Tunner HG, Heppich S, Uzzell T (1994) Two new water frog species from the Aegean Islands Crete and Karpathos (Amphibia, Salientia, Ranidae). Notulae Naturae 470:1–9Google Scholar
  11. Bergen K, Semlitsch RD, Reyer H-U (1997) Hybrid female mating are directly related to the availability of Rana lessonae and Rana esculenta males in experimental populations. Copeia 1997:275–283CrossRefGoogle Scholar
  12. Berger L (1999) Relationships of western Palearctic water frog taxa based on crossing experiments. In: III. International symposium on genetics, systematics and ecology of western Palearctic water frogs, Berlin, Abstract (unpublished)Google Scholar
  13. Berger L, Uzzell T (1980) The eggs of European water frogs (Rana esculenta complex) and their hybrids. Folia Biol (Kraków) 28:3–25Google Scholar
  14. Berger L, Uzzell T, Hotz H (1982) Crossing experiments between some western Palearctic species of water frogs (Salientia: Ranidae). Vertebr Hung 21:33–45Google Scholar
  15. Berger L, Uzzell T, Hotz H (1994) Postzygotic reproductive isolation between Mendelian species of European water frogs. Zool Pol 39:209–242Google Scholar
  16. Bolnick DI, Fitzpatrick BM (2007) Sympatric speciation: models and empirical evidence. Annu Rev Ecol Evol Syst 38:459–487CrossRefGoogle Scholar
  17. Bridgland DR, Westaway R (2007a) Climatically controlled river terrace staircases: a worldwide Quaternary phenomenon. Geomorphology 98:285–315CrossRefGoogle Scholar
  18. Bridgland DR, Westaway R (2007b) Preservation patterns of late Cenozoic fluvial deposits and their implications: results from IGCP 449. Quatern Int 189:5–38CrossRefGoogle Scholar
  19. Bullini L (1994) Origin and evolution of animal hybrid species. Trends Ecol Evol 9:422–425PubMedCrossRefGoogle Scholar
  20. Carson HL, Templeton AR (1984) Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annu Rev Ecol Syst 15:97–131CrossRefGoogle Scholar
  21. Cosentino D, Gliozzi E, Pipponzi G (2007) The late Messinian Lago-Mare episode in the Mediterranean Basin: preliminary report on the occurrence of Paratethyan ostracod fauna from central Crete (Greece). Geobios 40:339–349CrossRefGoogle Scholar
  22. Coyne JA, Orr HA (1998) The evolutionary genetics of speciation. Philos Trans R Soc Lond B 353:287–305CrossRefGoogle Scholar
  23. Demir T, Seyrek A, Westaway R, Bridgland D, Beck A (2008) Late Cenozoic surface uplift revealed by incision by the River Euphrates at Birecik, southeast Turkey. Quatern Int 186:132–163CrossRefGoogle Scholar
  24. Demir T, Westaway R, Bridgland D, Pringle M, Yurtmen S, Beck A, Rowbotham G (2007) Ar-Ar dating of Late Cenozoic basaltic volcanism in northern Syria: implications for the history of incision by the river Euphrates and uplift of the northern Arabian platform. Tectonics 26,  10.1029/2006TC001959
  25. Dobzhansky T (1940) Speciation as a stage in evolutionary divergence. Am Nat 74:312–321CrossRefGoogle Scholar
  26. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. doi: 10.1186/1471-2148-7-214 PubMedCrossRefGoogle Scholar
  27. Dubois A, Ohler A (1994) Frogs of the subgenus Pelophylax (Amphibia, Anura, Genus Rana): a catalogue of available scientific names, with comments on name-bearing types, complete synonymies, proposed common names, and maps showing all type localities. Zool Pol 39:139–204Google Scholar
  28. Ehlers J, Gibbard PL (2007) The extent and chronology of Cenozoic global glaciation. Quatern Int 164–165:6–20CrossRefGoogle Scholar
  29. Frost DR (2008) Amphibian species of the world: an online reference. Version 5.2 (15 July 2007). Electronic database available via American Museum of Natural History, New York, USA
  30. Gosner KL (1960) A simplified table for staging anuran embryos with notes on identification. Herpetologica 16:183–196Google Scholar
  31. Günther R (1973) Über die verwandtschaftlichen Beziehungen zwischen den europäischen Grünfröschen und den Bastardcharakter von Rana esculenta L. (Anura). Zool Anz 190:250–285Google Scholar
  32. Günther R (1982) Ergebnisse experimenteller Kreuzungen zwischen Wasserfröschen (Anura, Ranidae) aus verschiedenen Ländern Europas und Mittelasiens. Vertebr Hung 21:157–167Google Scholar
  33. Günther R, Plötner J, Tetzlaff I (1991) Zu einigen Merkmalen der Wasserfrösche (Rana synkl. esculenta) des Donau-Deltas. Salamandra 27:246–265Google Scholar
  34. Guex GD, Hotz H, Semlitsch R (2002) Deleterious alleles and differential viability in progeny of natural hemiclonal frogs. Evolution 56:1036–1044PubMedGoogle Scholar
  35. Guex GD, Hotz H, Uzzell T, Semlitsch R, Beerli P, Pascolini R (2001) Developmental disturbances in Rana esculenta tadpoles and metamorphs. Mitt Mus Nat kd Berl, Zool Reihe, 77:79–86Google Scholar
  36. Haefeli C (2005) Variation in advertisement calls among geographically isolated water frogs. Diploma Thesis, University ZurichGoogle Scholar
  37. Haefeli C, Hotz H, Guex G-D, Uzzell T, Beerli P, Plötner J, Reyer H-U (unpublished manuscript) Advertisement calls and genetic divergence among water frog species in the eastern MediterraneanGoogle Scholar
  38. Head MJ, Gibbard PL (2005) Early-Middle Pleistocene transitions: the land and ocean evidence. Geol Soc Lond Spec Publ 247:1–18CrossRefGoogle Scholar
  39. Insert Head MJ, Gibbard PL Heinicke MP, Duellmann WE, Hedges SB (2007) Major Caribbean and Central American frog faunas originated by ancient oceanic dispersals. Proc Natl Acad Sci USA 104:9913–10294CrossRefGoogle Scholar
  40. Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913PubMedCrossRefGoogle Scholar
  41. Hewitt GM (2004) Genetic consequences of climatic changes in the Quaternary. Philos Trans R Soc Lond B 359:183–195CrossRefGoogle Scholar
  42. Higgins DG, Bleasby AJ, Fuchs R (1992) CLUSTAL V: improved software for multiple sequence alignment. CABIOS 8:189–191PubMedGoogle Scholar
  43. Hilgen FJ, Kuiper K, Krijgsman W, Snel E, van der Laan E (2007) Astronomical tuning as the basis for high resolution chronostratigraphy: the intricate history of the Messinian salinity crisis. Stratigraphy 4:231–238Google Scholar
  44. Hillis DM (1984) Misuse and modification of Nei’s genetic distance. Syst Zool 33:238–240CrossRefGoogle Scholar
  45. Holsbeek G, Mergeay J, Hotz H, Plötner J, Volckaert M, de Meester L (2008) A cryptic invasion within an invasion and widespread introgression in the European water frog complex: consequences of uncontrolled commercial trade and weak international legislation. Mol Ecol 17:5023–5035PubMedCrossRefGoogle Scholar
  46. Hotz H, Uzzell T (1982) Biochemically detected sympatry of two water frog species: two different cases in the Adriatic Balkans (Amphibia: Ranidae). Proc Acad Nat Sci Phila 134:50–79Google Scholar
  47. Hotz H, Mancino G, Bucci-Innocenti S, Ragghiati M, Berger L, Uzzell T (1985) Rana ridibunda varies geographically in inducing clonal gametogenesis in interspecies hybrids. J Exp Zool 236:199–210CrossRefGoogle Scholar
  48. Hrbek T, Küçük F, Frickey T, Stölting KN, Wildekamp RH, Meyer A (2002) Molecular phylogeny and historical biogeography of the Aphanius (Pisces, Cyprinodontiformes) species complex of central Anatolia, Turkey. Mol Phyl Evol 25:125–137CrossRefGoogle Scholar
  49. Hrbek T, Stölting KN, Bardakçı F, Küçük F, Wildekamp RH, Meyer A (2004) Plate tectonics and biogeographical patterns of the Pseudophoxinus (Pisces: Cypriniformes) species complex of central Anatolia, Turkey. Mol Phyl Evol 32:297–308CrossRefGoogle Scholar
  50. Huelsenbeck JP, Ronquist F (2005) Bayesian analysis of molecular evolution using MrBayes. In: Nielsen R (ed) Statistical methods in molecular evolution. Springer, New York, pp 183–232CrossRefGoogle Scholar
  51. Jaffey N, Robertson A (2005) Non-marine sedimentation associated with oligocene-recent exhumation and uplift of the central taurus mountains, S Turkey. Sediment Geol 173:53–89CrossRefGoogle Scholar
  52. Jdeidi T (2000) Enzyme polymorphism, morphometric and bioacoustic studies in water frog complex in Turkey. PhD thesis, Middle East Technical University, Ankara, TurkeyGoogle Scholar
  53. Jdeidi T, Bilgin CC, Kence M (2001) New localities extend the range of Rana bedriagae caralitana Arıkan, 1988 (Anura: Ranidae) further west and suggest specific status. Turk J Zool 25:153–158Google Scholar
  54. Joger U, Hermann H-W, Nilson G (1992) Molecular phylogeny and systematics of viperine snakes. II. A revision of the Vipera ursinii complex. In: Korsos Z, Kiss J (eds) Proc sixth ordinary general meeting SEH. Hungarian Natural History Museum, Budapest, pp 239–244Google Scholar
  55. Joermann G, Baran I, Schneider H (1988) The mating call of Rana ridibunda (Amphibia: Anura) in western Turkey: bioacoustic analysis and taxonomic consequences. Zool Anz 220:225–232Google Scholar
  56. Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Ass 90:773–795CrossRefGoogle Scholar
  57. Kawamura T, Nishioka M (1979) Isolating mechanisms among the water frog species distributed in the Palearctic region. Mitt Zool Mus Berlin 55:171–185Google Scholar
  58. Kawamura T, Nishioka M (1986) Hybridization experiments among Rana lessonae, Rana ridibunda and Rana esculenta, with special reference to hybridogenesis. Sci Rep Lab Amphibian Biol Hiroshima Univ 8:117–271Google Scholar
  59. Kawamura T, Nishioka M, Kuramoto M (1972) Interspecific hybrids between Japanese and European pond frogs. Sci Rep Lab Amphibian Biol, Hiroshima Univ 1:277–301Google Scholar
  60. Kordges T (1988) Beobachtungen am Epirusfrosch (Rana epeirotica), dem neuen griechischen Wasserfrosch. In: Günther R, Klewen R (eds) Beiträge zur Biologie und Bibliographie (1960–1987) der europäischen Wasserfrösche. Jb Feldherp, Beiheft 1:135–143Google Scholar
  61. Kosswig C (1955) Zoogeography of the near East. Syst Zool 4:49–73CrossRefGoogle Scholar
  62. Krijgsman W, Hilgen FJ, Raffi I, Sierro FJ, Wilson DS (1999a) Chronology, causes and progression of the Messinian salinity crisis. Nature 400:652–655CrossRefGoogle Scholar
  63. Krijgsman W, Langereis CG, Zachariasse WJ, Boccaletti M, Moratti G, Gelati R, Iaccarino S, Papani G, Villa G (1999b) Late neogene evolution of the Taza-Guercif Basin (Rifian Corridor, Morocco) and implications for the Messinian Salinity Crisis. Mar Geol 153:147–160CrossRefGoogle Scholar
  64. Kvasov DD (1983) Causes of the marked regression of the Black and Caspian seas about five million years ago. Oceanology 23:331–335Google Scholar
  65. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. doi: 10.1093/bioinformatics/btp187 PubMedGoogle Scholar
  66. Loget N, van den Driessche J, Davy P (2005) How did the Messinian Salinity Crisis end ? Terra Nova 17:414–419CrossRefGoogle Scholar
  67. Öztürk M, Çelik A, Güvensen A, Hamzaoğlu A (2008) Ecology of tertiary relict endemic Liquidambar orientalis Mill. forests. For Ecol Manag 256:510–518CrossRefGoogle Scholar
  68. Orr HA (2005) The genetic basis of reproductive isolation: insights from Drosophila. Proc Natl Acad Sci USA 102(Suppl 1):6522–6526PubMedCrossRefGoogle Scholar
  69. Ohst T (2001) Untersuchungen zur stammesgeschichtlichen Entwicklung des westpaläarktischen Wasserfroschkomplexes (Anura, Ranidae) auf der Grundlage von DNA-Sequenzen des mitochondrialen ND2- und ND3-Gens. Diplomarbeit, Humboldt-Universität, BerlinGoogle Scholar
  70. Ohst T (2008) Genetische Einflüsse allochthoner Wasserfrösche auf endemische Wasserfroschpopulationen (R. kl. esculenta Komplex). Diss, Humboldt-Universität, BerlinGoogle Scholar
  71. Plötner J (1998) Genetic diversity in mitochondrial 12S rDNA of western Palearctic water frogs (Anura, Ranidae) and implications for their systematics. J Zool Syst Evol Res 36:191–201CrossRefGoogle Scholar
  72. Plötner J (2005) Die westpaläarktischen Wasserfrösche. Von Märtyrern der Wissenschaft zur biologischen Sensation. Z f Feldherpetologie, Beiheft 9, Laurenti, BielefeldGoogle Scholar
  73. Plötner J, Ohst T (2001) New hypothesis on the systematics of the western Palearctic water frog complex (Anura: Ranidae). Mitt Mus Nat kd Berl, Zool Reihe 77:5–21Google Scholar
  74. Plötner J, Ohst T, Böhme W, Schreiber R (2001) Divergence in mitochondrial DNA of Near Eastern water frogs with special reference to the systematic status of Cypriote and Anatolian populations (Anura, Ranidae). Amphibia-Reptilia 22:397–412CrossRefGoogle Scholar
  75. Plötner J, Uzzell T, Beerli P, Spolsky C, Ohst T, Litvinchuk SN, Guex G-D, Reyer H-U, Hotz H (2008) Widespread unidirectional transfer of mitochondrial DNA: a case in western Palearctic water frogs. J Evol Biol 21:668–681PubMedCrossRefGoogle Scholar
  76. Plötner J, Köhler F, Uzzell T, Beerli P, Schreiber R, Guex G-D, Hotz H (2009) Evolution of serum albumin intron-1 is shaped by a 5′ truncated non-long terminal repeat retrotransposon in western Palearctic water frogs (Neobatrachia). Mol Phyl Evol 53:784–791CrossRefGoogle Scholar
  77. Remington CL (1968) Suture-zones of hybrid interaction between recently joined biotas. Evol Biol 2:321–428CrossRefGoogle Scholar
  78. Robertson AHF (1998) Late Miocene paleoenvironments and tectonic setting of the southern margin of Cyprus and the Eratosthenes Seamount. Proc Ocean Drill Program Sci Results 160:453–463Google Scholar
  79. Robertson A, Ünlügenç ÜC, İnan N, Taşlı K (2004) The Misis-Andırın complex: a mid-tertiary melange related to late-stage subduction of the Southern Neotethys in S Turkey. J Asian Earth Sci 22:413–453CrossRefGoogle Scholar
  80. Roeseli M, Reyer H-U (2000) Male vocalization and female choice in the hybridogenetic Rana lessonae/Rana esculenta complex. Anim Behav 60:745–755CrossRefGoogle Scholar
  81. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  82. Rose J, Candy I, Moorlock BSP, Wilkins H, Lee JA, Hamblin RJO, Lee JR, Riding JB, Morigi AN (2002) Early and early Middle Pleistocene river, coastal and neotectonic processes, southeast Norfolk, England. Proc Geol Assoc 113:47–67CrossRefGoogle Scholar
  83. Schmeller DS, Pagano A, Plénet S, Veith M (2007) Introducing water frogs – Is there a risk for indigenous species in France? C R Biol 330:684–690PubMedCrossRefGoogle Scholar
  84. Schmidtler JF (1998) Verbreitungsstrukturen der Herpetofauna im Taurus-Gebirge, Türkei (Amphibia; Reptilia). Faunistische Abh Staatl Mus Tierkunde Dresden 21(Suppl):133–148Google Scholar
  85. Schneider H (1997) Calls and reproductive behaviour of the water frogs of Damascus, Syria (Amphibia: Anura: Rana bedriagae Camerano, 1882). Zool Middle East 15:51–66Google Scholar
  86. Schneider H (1999) Calls of the Levantine frog, Rana bedriagae, at Birket Ata, Israel (Amphibia: Anura). Zool Middle East 19:101–116Google Scholar
  87. Schneider H, Haxhiu I (1994) Mating-call analysis and taxonomy of the water frogs in Albania (Anura: Ranidae). Zool Jb Syst 121:248–262Google Scholar
  88. Schneider H, Sinsch U (1992) Mating call variation in lake frogs referred to as Rana ridibunda Pallas, 1771. Taxonomic implications. Z zool Syst Evol-forsch 30:297–315Google Scholar
  89. Schneider H, Sinsch U (1999) Taxonomic reassessment of Middle Eastern water frogs: bioacoustic variation among populations considered as Rana ridibunda, R. bedriagae or R. levantina. J Zool Syst Evol Res 37:57–65CrossRefGoogle Scholar
  90. Schneider H, Sinsch U (2007) Contribution of bioacoustics to the taxonomy of the Anura. In: Heathwole H (ed) Amphibian biology, vol 7. Surrey Beatty, Chipping Norton, pp 2893–2932Google Scholar
  91. Schneider H, Sofianidou TS, Kyriakopoulou-Sklavounou P (1984) Bioacoustic and morphometric studies in water frogs (genus Rana) of lake Ioannina in Greece, and description of a new species (Anura, Amphibia). Z zool Syst Evol-forsch 22:349–366CrossRefGoogle Scholar
  92. Schneider H, Sinsch U, Sofianidou TS (1993) The water frogs of Greece. Bioacoustic evidence for a new species. Z zool Syst Evol-forsch 31:47–63CrossRefGoogle Scholar
  93. Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207PubMedCrossRefGoogle Scholar
  94. Seyrek A, Demir T, Pringle M, Yurtmen S, Westaway R, Bridgland D, Beck A, Rowbotham G (2008a) Late Cenozoic uplift of the Amanos Mountains and incision of the middle Ceyhan river gorge, southern Turkey; Ar-Ar dating of the Düziçi basalt. Geomorphology 97:321–355CrossRefGoogle Scholar
  95. Seyrek A, Westaway R, Pringle M, Yurtmen S, Demir T, Rowbotham G (2008b) Timing of the Quaternary Elazığvolcanism, eastern Turkey, and its significance for constraining landscape evolution and surface uplift. Turkish J Earth Sci 17:497–541Google Scholar
  96. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  97. Uzzell T, Ashmole NP (1970) Suture-zones: an alternative view. Syst Zool 19:197–199CrossRefGoogle Scholar
  98. van der Laan E, Snel E, de Kaenel E, Hilgen FJ, Krijgsman W (2006) No major deglaciation across the Miocene-Pliocene boundary: integrated stratigraphy and astronomical tuning of the Loutja section (Bou Regreg area, NW Morocco). Paleoceanography 21:PA3011. doi: 10.1029/2005PA001193 CrossRefGoogle Scholar
  99. Vences M, Vieites DR, Glaw F, Brinkmann H, Kosuch J, Veith M, Meyer A (2003) Multiple overseas dispersals in amphibians. Proc R Soc Lond B 270:2435–2442CrossRefGoogle Scholar
  100. Veith M, Steinfartz S (2004) When non-monophyly results in taxonomic consequences - the case of Mertensiella within the Salamandridae (Amphibia: Urodela). Salamandra 40:67–80Google Scholar
  101. Veith M, Schmidtler F, Kosuch J, Baran Ü, Seitz A (2003) Paleoclimatic changes explain Anatolian mountain frog evolution: a test for alternating vicariance and dispersal events. Mol Ecol 12:185–189PubMedCrossRefGoogle Scholar
  102. Westaway R, Demir T, Seyrek A (2008) Geometry of the Turkey-Arabia and Africa-Arabia plate boundaries in the latest Miocene to Mid-Pliocene: the role of the Malatya-Ovacık Fault Zone in eastern Turkey. eEarth 3:27–35CrossRefGoogle Scholar
  103. Westaway R, Guillou H, Seyrek A, Demir T, Bridgland D, Scaillet S, Beck A (2009) Late Cenozoic surface uplift, basaltic volcanism, and incision by the river Tigris around Diyarbakır, SE Turkey. Int J Earth Sci 98:601–625CrossRefGoogle Scholar
  104. Wiley EO (1978) The evolutionary species concept reconsidered. Syst Zool 27:17–26CrossRefGoogle Scholar
  105. Wiley EO (1981) Phylogenetics: the theory and practice of phylogenetic systematics. Wiley, New YorkGoogle Scholar
  106. Wu C-I (2001) The genetic view of the process of speciation. J Evol Biol 14:851–865CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Jörg Plötner
    • 1
    Email author
  • Thomas Uzzell
    • 2
  • Peter Beerli
    • 3
  • Çiğdem Akın
    • 4
  • C. Can Bilgin
    • 4
  • Cornelia Haefeli
    • 5
  • Torsten Ohst
    • 1
  • Frank Köhler
    • 1
    • 6
  • Robert Schreiber
    • 1
  • Gaston-Denis Guex
    • 5
  • Spartak N. Litvinchuk
    • 7
  • Rob Westaway
  • Heinz-Ulrich Reyer
    • 5
  • Nicolas Pruvost
    • 6
  • Hansjürg Hotz
    • 1
    • 5
  1. 1.Museum für Naturkunde, Leibniz-Institut für Evolutions- und BiodiversitätsforschungHumboldt-Universität zu BerlinBerlinGermany
  2. 2.Laboratory for Molecular Systematics and EcologyAcademy of Natural SciencesPhiladelphiaUSA
  3. 3.Department of Scientific ComputingFlorida State UniversityTallahasseeUSA
  4. 4.Department of Biology, Biodiversity and Conservation LaboratoryMiddle East Technical UniversityAnkaraTurkey
  5. 5.Institut für Evolutionsbiologie und UmweltwissenschaftenUniversität Zürich-IrchelZurichSwitzerland
  6. 6.Department of ResearchAustralian MuseumSydneyAustralia
  7. 7.Institute of CytologyRussian Academy of SciencesSt. PetersburgRussia

Personalised recommendations