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

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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).

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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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Authors and Affiliations

  1. Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Humboldt-Universität zu Berlin, Invalidenstraße 43, 10115, Berlin, Germany

    Jörg Plötner, Torsten Ohst, Frank Köhler, Robert Schreiber & Hansjürg Hotz

  2. Laboratory for Molecular Systematics and Ecology, Academy of Natural Sciences, 1900 B. F. Parkway, Philadelphia, PA, 19103, USA

    Thomas Uzzell

  3. Department of Scientific Computing, Florida State University, Tallahassee, FL, 32306-4120, USA

    Peter Beerli

  4. Department of Biology, Biodiversity and Conservation Laboratory, Middle East Technical University, 06531, Ankara, Turkey

    Çiğdem Akın & C. Can Bilgin

  5. Institut für Evolutionsbiologie und Umweltwissenschaften, Universität Zürich-Irchel, Winterthurerstrasse 190, 8057, Zurich, Switzerland

    Cornelia Haefeli, Gaston-Denis Guex, Heinz-Ulrich Reyer & Hansjürg Hotz

  6. Department of Research, Australian Museum, 6 College Street, Sydney, 2010, NSW, Australia

    Frank Köhler & Nicolas Pruvost

  7. Institute of Cytology, Russian Academy of Sciences, Tikhoretsky prospekt 4, 194064, St. Petersburg, Russia

    Spartak N. Litvinchuk

Authors
  1. Jörg Plötner
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  2. Thomas Uzzell
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  3. Peter Beerli
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  4. Çiğdem Akın
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  5. C. Can Bilgin
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  6. Cornelia Haefeli
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  7. Torsten Ohst
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  8. Frank Köhler
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  9. Robert Schreiber
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  10. Gaston-Denis Guex
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  11. Spartak N. Litvinchuk
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  12. Rob Westaway
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  13. Heinz-Ulrich Reyer
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  14. Nicolas Pruvost
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  15. Hansjürg Hotz
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Corresponding author

Correspondence to Jörg Plötner .

Editor information

Editors and Affiliations

  1. Museum für Naturkunde, Humboldt Universität Berlin, Invalidenstraße 43, Berlin, 10115, Germany

    Matthias Glaubrecht

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Plötner, J. et al. (2010). Genetic Divergence and Evolution of Reproductive Isolation in Eastern Mediterranean Water Frogs. In: Glaubrecht, M. (eds) Evolution in Action. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12425-9_18

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