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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
Chapter

Abstract

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).

Keywords

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

Notes

Acknowledgments

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.

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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

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