Skip to main content
SpringerLink
Log in

Phylogeographic patterns of genetic diversity in the common spadefoot toad, Pelobates fuscus (Anura: Pelobatidae), reveals evolutionary history, postglacial range expansion and secondary contact

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

Based on allozyme variation of 410 newly collected individuals from 52 localities, we reconstructed range-wide phylogeography of the widespread Western Palearctic anuran, Pelobates fuscus. To study genetic diversity, evolutionary history, postglacial range expansion and secondary contact zones, we used a multidisciplinary approach combining information from various genetic analyses and ecological niche modeling. We confirmed the presence of two main groups in P. fuscus, initially revealed by genome size variation. Pelobates f. vespertinus presents a monomorphic group, but two main groups can be identified in P. f. fuscus: an East European and a West European group. We suggest the existence of at least four different Last Glacial refugia for P. fuscus: (1) the area between the Caspian and Azov Seas as the origin for the expansion of P. f. vespertinus; (2) the northwestern part of the Black Sea area for the East European P. f. fuscus; (3) the southwestern part of the Pannonian Plain and (4) the Po Plain for the West European P. f. fuscus. The routes of postglacial range expansions from the refugia are discussed. We newly identified a hybrid zone between P. f. fuscus and P. f. vespertinus. The width of this zone is about 12.5 km. In light of these findings, the two subspecies of P. fuscus constitute distinct evolutionary lineages and merit recognition as separate species. Our data do not provide support for the validity of P.f. insubricus. We therefore propose to synonymize this subspecies with P. f. fuscus.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Akın, C., Bilgin, C. C., Beerli, P., Westaway, R., Ohst, T., Litvinchuk, S. N., et al. (2010). Phylogeographic patterns of genetic diversity in eastern Mediterranean water frogs were determined by geological processes and climate change in the Late Cenozoic. Journal of Biogeography, 37, 2111–2124.

    Article  PubMed  Google Scholar 

  • Anderson, E. C., & Thompson, E. A. (2002). A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217–1229.

    PubMed  CAS  Google Scholar 

  • Arntzen, J. W., & Wielstra, B. (2010). Where to draw the line? A nuclear genetic perspective on proposed range boundaries of the crested newts Triturus karelinii and T. arntzeni. Amphibia-Reptilia, 31, 311–322.

    Article  Google Scholar 

  • Avise, J. C. (2000). Phylogeography: The history and formation of species. Cambridge: Harvard University Press.

    Google Scholar 

  • Babik, W., Branicki, W., Sandera, M., Litvinchuk, S., Borkin, L. J., Irwin, J. T., et al. (2004). Mitochondrial phylogeography of the moor frog, Rana arvalis. Molecular Ecology, 13, 1469–1480.

    Article  PubMed  CAS  Google Scholar 

  • Babik, W., Branicki, W., Crnobrnja-Isailović, J., Cogălniceanu, A., Sas, I., Olgun, K., et al. (2007). Phylogeography of two European newt species-discordance between mtDNA and morphology. Molecular Ecology, 14, 2475–2491.

    Article  CAS  Google Scholar 

  • Ballard, J. W. O., & Whitlock, M. C. (2004). The incomplete natural history of mitochondria. Molecular Ecology, 13, 729–744.

    Article  PubMed  Google Scholar 

  • Bandi, C., Damiani, G., Magrassi, L., Grigolo, A., Fani, R., & Sacchi, L. (1994). Flavobacteria as intracellular symbionts in cockroaches. Proceedings of the Royal Society of London B: Biological Sciences, 257, 43–48.

    Article  CAS  Google Scholar 

  • Barton, N. H., & Hewitt, G. M. (1985). Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16, 113–148.

    Article  Google Scholar 

  • Böhme, G. (1983). Skelettreste von Amphibien (Urodela, Salientia) aus dem fossilen Tierbautensystem von Pisede bei Malchin. Teil 1: Taxonomie und Biostrationomie. Wissenschaftliche Zeitschrift der Humboldt-Universität zu Berlin, Mathematisch-Naturwissenschaftliche Reihe, 32(6), 657–670.

    Google Scholar 

  • Bonato, L., & Steinfartz, S. (2005). Evolution of the melanistic colour in the Alpine salamander Salamandra atra as revealed by a new subspecies from the Venetian Prealps. Italian Journal of Zoology, 72, 253–260.

    Article  Google Scholar 

  • Borkin, L. J. (1984). The European-Far Eastern disjunctions in distribution of amphibians: a new analysis of the problem. Proceedings of Zoological Institute of RAS, Leningrad, 124, 55–88.

    Google Scholar 

  • Borkin, L. J., Litvinchuk, S. N., Milto, K. D., Rosanov, J. M., & Khalturin, M. D. (2001). Cryptic speciation in Pelobates fuscus (Anura, Pelobatidae): cytometrical and biochemical evidences. Doklady Biological Sciences, 376, 86–88.

    Article  Google Scholar 

  • Borkin, L. J., Litvinchuk, S. N., Rosanov, J. M., & Milto, K. D. (2002 [2001]). Cryptic speciation in Pelobates fuscus (Anura, Pelobatidae): evidence from DNA flow cytometry. Amphibia-Reptilia, 22, 387–396.

  • Borkin, L. J., Litvinchuk, S. N., Rosanov, J. M., Khalturin, M. D., Lada, G. A., Borissovsky, A. G., et al. (2003). New data on the distribution of two cryptic forms of the common spadefoot toad (Pelobates fuscus) in Eastern Europe. Russian Journal of Herpetology, 10, 115–122.

    Google Scholar 

  • Borkin, L. J., Litvinchuk, S. N., Rosanov, J. M., & Skorinov, D. V. (2004). On cryptic species (from the example of amphibians). Entomological Review, 84(Suppl. 1), S75–S98.

    Google Scholar 

  • Bossuyt, F., & Milinkovitch, M. C. (2000). Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proceedings of the National Academy of Science of the United States of America, 97, 6585–6590.

    Article  CAS  Google Scholar 

  • Busack, S. D., Maxson, L. R., & Wilson, M. A. (1985). Pelobates varaldii (Anura: Pelobatidae): a morphologically conservative species. Copeia, 1985, 107–112.

    Article  Google Scholar 

  • Canestrelli, D., & Nascetti, G. (2008). Phylogeography of the pool frog Rana (Pelophylax) lessonae in the Italian peninsula and Sicily: multiple refugia, glacial expansions and nuclear–mitochondrial discordance. Journal of Biogeography, 35, 1923–1936.

    Article  Google Scholar 

  • Canestrelli, D., Cimmaruta, R., & Nascetti, G. (2007). Phylogeography and historical demography of the Italian treefrog, Hyla intermedia, reveals multiple refugia, population expansions and secondary contacts within peninsular Italy. Molecular Ecology, 16, 4808–4821.

    Article  PubMed  CAS  Google Scholar 

  • Canestrelli, D., Salvi, D., Maura, M., Bologna, M. A., & Nascetti, G. (2012). One species, three Pleistocene evolutionary histories: phylogeography of the Italian crested newt, Triturus carnifex. PLoS One, 7(7), e41754.

    Article  PubMed  CAS  Google Scholar 

  • Chepalyga, A. L. (1987). Climatic events in the cainozoic of parathetis. In Climates of the earth in a geological past (pp. 214–225). Moscow: Nauka.

    Google Scholar 

  • Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.

    Article  PubMed  CAS  Google Scholar 

  • Crochet, P.-A., & Dubois, A. (2004). Recent changes in the taxonomy of European amphibians and reptiles. In J. P. Gasc et al. (Eds.), Atlas of amphibians and reptiles in Europe (2nd ed., pp. 496–516). Paris: Societas Europaea Herpetologica & Museum National d’Histoire Naturelle.

    Google Scholar 

  • Crottini, A., Andreone, F., Kosuch, J., Borkin, L. J., Litvinchuk, S. N., Eggert, C., et al. (2007). Fossorial but widespread: the phylogeography of the common spadefoot toad (Pelobates fuscus), and the role of the Po Valley as a major source of genetic variability. Molecular Ecology, 16, 2734–2754.

    Article  PubMed  Google Scholar 

  • Currat, M., Ruedi, M., Petit, R. J., & Excoffer, L. (2008). The hidden side of invasions: massive introgression by local genes. Evolution, 62, 1908–1920.

    PubMed  Google Scholar 

  • de Queiroz, K. (2005). Ernst Mayr and the modern concept of species. Proceedings of the National Academy of Sciences of the United States of America, 102, 6600–6607.

    Article  PubMed  CAS  Google Scholar 

  • Džukić, G., Beškov, V., Sidorovska, V., Cogălniceanu, D., & Kalezić, M. L. (2008). Contemporary chorology of the spadefoot toads (Pelobates spp.) in the Balkan Peninsula. Zeitschrift für Feldherpetologie, 15, 61–78.

    Google Scholar 

  • Earl, D. A., & vonHoldt, B. M. (2012). Structure Harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361.

    Article  Google Scholar 

  • Eggert, C. (2002). Use of fluorescent pigments and implantable transmitters to track a fossorial toad (Pelobates fuscus). Herpetological Journal, 12, 69–74.

    Google Scholar 

  • Eggert, C., Coaglniceanu, D., Veith, M., Dzukic, G., & Taberlet, P. (2006). The declining Spadefoot toad, Pelobates fuscus (Pelobatidae): Paleo and recent environmental changes as a major influence on current population structure and status. Conservation Genetics, 7, 185–195.

    Article  Google Scholar 

  • Elith, J. (2002). Quantitative methods for modeling species habitat: Comparative performance and an application to Australian plants. In S. Ferson & M. Burgman (Eds.), Quantitative methods for conservation biology (pp. 39–58). New York: Springer.

    Google Scholar 

  • Elith, J., Kearney, M., & Phillips, S. J. (2010). The art of modeling range shifting species. Methods in Ecology and Evolution, 1, 330–342.

    Article  Google Scholar 

  • Elith, J., Phillips, S. J., Hastie, T., Dudík, M., Chee, Y. E., & Yates, C. J. (2010). A statistical explanation of MaxEnt for ecologists. Diversity and Distributions, 17, 43–57.

    Article  Google Scholar 

  • Endler, J. A. (1977). Geographic Variation, Speciation, and Clines. Princeton: Princeton University Press.

    Google Scholar 

  • ESRI. (2011). ArcGIS, version 10. Redlands, CA: Environmental Systems Research Institute.

    Google Scholar 

  • Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software Structure: a simulation study. Molecular Ecology, 14, 2611–2620.

    Article  PubMed  CAS  Google Scholar 

  • Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.

    Article  PubMed  Google Scholar 

  • Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.

    PubMed  CAS  Google Scholar 

  • Falush, D., Stephens, M., & Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567–1587.

    PubMed  CAS  Google Scholar 

  • Felsenstein, J. (2004). PHYLIP v. 3.6b. Seattle: University of Washington.

    Google Scholar 

  • Fijarczyk, A., Nadachowska, K., Hofman, S., Litvinchuk, S. N., Babik, W., Stuglik, M., et al. (2011). Nuclear and mitochondrial phylogeography of the European fire-bellied toads Bombina bombina and B. variegata supports their independent histories. Molecular Ecology, 20, 3381–3398.

    Article  PubMed  Google Scholar 

  • Fromhage, L., Vences, M., & Veith, M. (2004). Testing alternative vicariance scenarios in Western Mediterranean discoglossid frogs. Molecular Phylogenetics and Evolution, 31, 308–322.

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Porta, J., Litvinchuk, S. N., Crochet, P. A., Romano, A., Geniez, P., Lo-Valvo, M., et al. (2012). Molecular phylogenetics and historical biogeography of the west-palearctic common toads (Bufo bufo species complex). Molecular Phylogenetics and Evolution, 63, 113–130.

    Article  PubMed  CAS  Google Scholar 

  • Giovanelli, J. G. R., Ferreira de Siquera, M., Haddad, C. F. B., & Alexandrini, J. (2010). Modeling a spatially restricted distribution in the Netropics: How the size of calibration area affects the performance of five presence-only methods. Ecological Modeling, 221, 215–224.

    Article  Google Scholar 

  • Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium, 41, 95–98.

    CAS  Google Scholar 

  • Hernandez, P. A., Graham, C. H., Master, L. L., & Albert, D. L. (2006). The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography, 29, 773–785.

    Article  Google Scholar 

  • Hewitt, G. M. (1999). Post-glacial recolonization 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  PubMed  CAS  Google Scholar 

  • Hewitt, G. M. (2011a). Mediterranean peninsulas: The evolution of hotspots. In F. E. Zachos & J. C. Habel (Eds.), Biodiversity hotspots. Part. 2 (pp. 123–147). Heidelberg: Springer.

    Chapter  Google Scholar 

  • Hewitt, G. M. (2011b). Quaternary phylogeography: the roots of hybrid zones. Genetica, 139, 617–638.

    Article  PubMed  Google Scholar 

  • Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978.

    Article  Google Scholar 

  • Hofman, S., Spolsky, C., Uzzell, T., Cogălniceanu, D., Babik, W., & Szymura, J. M. (2007). Phylogeography of the fire-bellied toads Bombina: independent Pleistocene histories inferred from mitochondrial genomes. Molecular Ecology, 16, 2301–2316.

    Article  PubMed  CAS  Google Scholar 

  • Jiménez-Valverde, A., Lobo, J. M., & Hortal, J. (2008). Not as good as they seem: the importance of concepts in species distribution modeling. Diversity and Distributions, 14, 885–890.

    Article  Google Scholar 

  • Jockusch, E. L., & Wake, D. B. (2002). Falling apart and merging: Diversification of slender salamanders (Plethodontidae: Batrachoseps) in the American West. Biological Journal of the Linnaean Society, 76, 361–391.

    Article  Google Scholar 

  • Khalturin, M. D., Litvinchuk, S. N., Borkin, L. J., Rosanov, J. M., & Milto, K. D. (2003). Genetic variation in two cryptic forms, with different genome size, of the common spadefoot toad, Pelobates fuscus (Pelobatidae, Anura, Amphibia). Tsitologia, St. Petersburg, 45, 308–323.

    CAS  Google Scholar 

  • Klicka, J., & Zink, R. M. (1997). The importance of recent ice ages in speciation: A failed paradigm. Science, 277, 1666–1669.

    Article  CAS  Google Scholar 

  • Kwet, A., & Nöllert, A. (2009). Von Rösel von Rosenhof zum Froschlurch des Jahres: Die Knoblauchkröte. Sekretär, 9, 71–78.

    Google Scholar 

  • Lada, G. A., Borkin, L. J., & Litvinchuk, S. N. (2005). Morphological variation in two cryptic forms of the common spadefoot toad (Pelobates fuscus) from eastern Europe. In N. Ananjeva, O. Tsinenko (Eds.), Herpetologia Petropolitana (pp. 53–56). St. Petersburg.

  • Laurenti, J. N. (1768). Josephi Nicolai Laurenti Austriaci Viennensis Specimen Medicum, exhibens Synopsin Reptilium emendatam cum experimentis circa venena et antidota reptilium austriacorum. Viennae: Typ. Joan. Thom. Nob. de Trattnern, Caes. Reg. Aulae Typogr. et Bibliop.

  • Litvinchuk, S. N. (2005). A record of the Danube newt, Triturus dobrogicus, from the Dnepr River Delta (Ukraine). Russian Journal of Herpetology, 12, 69–72.

    Google Scholar 

  • Litvinchuk, S. N., & Borkin, L. J. (2009). Evolution, Systematics and Distribution of the Crested Newts (Triturus cristatus complex) in the Territory of Russia and Adjacent Countries. St. Petersburg: Evropeyskiy Dom.

    Google Scholar 

  • Litvinchuk, S. N., Borkin, L. J., Džukić, G., Kalezić, M. L., Khalturin, M. D., & Rosanov, Y. M. (1999). Taxonomic status of Triturus karelinii on the Balkans, with some comments about other crested newt taxa. Russian Journal of Herpetology, 6, 153–163.

    Google Scholar 

  • Litvinchuk, S. N., Rosanov, J. M., Borkin, L. J., & Skorinov, D. V. (2008). Molecular-biochemical and cytogenetic aspects of microevolution in anuran amphibians of the fauna of Russia and adjacent countries. In N. B. Ananjeva et al. (Eds.), The Problems of Herpetology (pp. 247–257). St. Petersburg.

  • Meissner, K. (1970). Obligatorisches Lernen im Funktionskreis der Vergrabehandlung von Pelobates fuscus fuscus Laur. (Anura). Ein Beitrag zur Ethometrie des Appetenzverhaltens. Zoologische Jahrbücher. Abteilung für allgemeine Zoologie und Physiologie der Tiere, 75, 423–469.

    Google Scholar 

  • Mertens, R., & Müller, L. (1928). Liste der Amphibien und Reptilien Europas. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, Frankfurt am Main, 41, 1–62.

    Google Scholar 

  • Mezhzherin, S. V., Morozov-Leonov, S. Y., Rostovskaya, O. V., & Sobolenko, L. Y. (2010). Reconstruction of species area recolonization based on the geographical variation analysis of Ldh-B allozymes of a pond frog Rana esculenta (= lessonae). Reports of the National Academy of Sciences of Ukraine, Kiev, 2, 164–169.

    Google Scholar 

  • Miller, M. P. (1997). Tools for Population Genetic Analyses (TFPGA) 1.3. http://www.marksgeneticsoftware.net/. Accessed 8 September 2012.

  • Moritz, C., Schneider, C. J., & Wake, D. B. (1992). Evolutionary relationships within the Ensatina eschscholtzii complex confirm the ring species interpretation. Systematic Biology, 41, 273–291.

    Google Scholar 

  • Nascetti, G., Zangari, F., & Canestrelli, D. (2005). The spectacled salamanders, Salamandrina terdigitata (Lacépède, 1788) and S. perspicillata (Savi, 1821): genetic differentiation and evolutionary history. Rendiconti Lincei. Scienze Fisiche e Naturali, 16, 159–169.

    Article  Google Scholar 

  • Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Proceedings of the National Academy of Sciences of the United States of America, 70, 3321–3323.

    Article  Google Scholar 

  • Nielsen, E. E., Bach, L. A., & Kotlicki, P. (2006). Hybridlab (version 1.0): a program for generating simulated hybrids from population samples. Molecular Ecology Notes, 6, 971–973.

    Article  Google Scholar 

  • Pallas, P. S. (1771). Reise durch verschiedene Provinzen des Rußischen Reichs. Erster Theil. St. Petersburg: Gedruckt bey der Kayserlichen Academie der Wissenschaften.

    Google Scholar 

  • Palo, J. U., Schmeller, D. S., Laurila, A., Primmer, C. R., Kuzmin, S. L., & Merilä, J. (2004). High degree of population subdivision in a widespread amphibian. Molecular Ecology, 13, 2631–2644.

    Article  PubMed  CAS  Google Scholar 

  • Phillips, S. J., & Dudík, M. (2008). Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography, 31, 161–175.

    Article  Google Scholar 

  • Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modeling, 190, 231–259.

    Article  Google Scholar 

  • Posada, D. (2008). jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25, 1253–1256.

    Article  PubMed  CAS  Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    PubMed  CAS  Google Scholar 

  • Provan, J., & Benett, K. D. (2008). Phylogeographic insights into cryptic glacial refugia. Trends in Ecology & Evolution, 23, 564–571.

    Article  Google Scholar 

  • Raes, N., Roos, M. C., Slik, J. W. F., Van Loon, E. E., & ter Steege, H. (2009). Botanical richness and endemicity patterns of Borneo derived from species distribution models. Ecography, 32, 180–192.

    Article  Google Scholar 

  • Rambaut, A., & Drummond, A. J. (2007). Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer. Accessed 8 September 2012.

  • Ratnikov, V. Y. (2009). Fossil remains of modern amphibian and reptile species as the material for studying of their areas history. Trudy Nauchno-Issledovatel’skogo Instituta Geologii Voronezhskogo Gosudarstvennogo Universiteta, Voronezh, 59, 1–91.

    Google Scholar 

  • Rödder, D., & Engler, J. O. (2011). Quantitative metrics of overlaps in Grinnellian niches: advances and possible drawbacks. Global Ecology and Biogeography, 20, 915–927.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rousset, F. (2008). Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103–106.

    Article  PubMed  Google Scholar 

  • Sardà-Palomera, F., & Vieites, D. R. (2011). Modeling species’ climatic distributions under habitat constrains: a case study with Coturnix coturnix. Annales Zoologici Fennici, 48, 147–160.

    Article  Google Scholar 

  • Schmitt, T. (2007). Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in Zoology, 4, 11.

    Article  PubMed  Google Scholar 

  • Schoener, T. W. (1968). Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology, 49, 704–726.

    Article  Google Scholar 

  • Snell, C., Tetteh, J., & Evans, I. H. (2005). Phylogeography of the pool frog (Rana lessonae Camerano) in Europe: evidence for native status in Great Britain and for an unusual postglacial colonization route. Biological Journal of the Linnean Society, 85, 41–51.

    Article  Google Scholar 

  • Sotiropoulos, K., Eleftherakos, K., Džkić, G., Kalezić, M. L., Legakis, A., & Polymeni, R. M. (2007). Phylogeny and biogeography of the alpine newt Mesotriton alpestris (Salamandridae, Caudata), inferred from mtDNA sequences. Molecular Phylogenetics and Evolution, 45, 211–226.

    Article  PubMed  CAS  Google Scholar 

  • Stöck, M., Moritz, C., Hickerson, M., Frynta, D., Dujsebayeva, T., Eremchenko, V., et al. (2006). Evolution of mitochondrial relationships and biogeography of Palearctic green toads (Bufo viridis subgroup) with insights in their genomic plasticity. Molecular Phylogenetics and Evolution, 41, 663–689.

    Article  PubMed  CAS  Google Scholar 

  • Stöck, M., Dubey, S., Klütsch, C., Litvinchuk, S. N., Scheidt, U., & Perrin, N. (2008). Mitochondrial and nuclear phylogeny of circum-Mediterranean tree frogs from the Hyla arborea group. Molecular Phylogenetics and Evolution, 49, 1019–1024.

    Article  PubMed  CAS  Google Scholar 

  • Stöck, M., Dufresnes, C., Litvinchuk, S. N., Lymberakis, P., Biollay, S., Berroneau, M., et al. (2012). Cryptic diversity among Western Palearctic tree frogs: Postglacial range expansion, range limits, and secondary contacts of three European tree frog lineages (Hyla arborea group). Molecular Phylogenetics and Evolution, 65, 1–9.

    Article  PubMed  Google Scholar 

  • Swets, K. (1988). Measuring the accuracy of diagnostic systems. Science, 240, 1285–1293.

    Article  PubMed  CAS  Google Scholar 

  • Swofford, D. L., & Selander, R. B. (1999). BIOSYS-2: a computer program for the analysis of allelic variation in population genetics and biochemical systematics. Release 2.0. Urbana, IL: University of Illinois.

    Google Scholar 

  • Szymura, J. M., & Barton, N. H. (1986). Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and B. variegata near Cracow in southern Poland. Evolution, 40, 1141–1159.

    Article  Google Scholar 

  • Taberlet, P., Fumagalli, L., Wust-Saucy, A.-G., & Cosson, J.-F. (2008). Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology, 7, 453–464.

    Article  Google Scholar 

  • Tamura, K., 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  PubMed  CAS  Google Scholar 

  • Teacher, A. G. F., Garner, T. W. J., & Nichols, R. A. (2009). European phylogeography of the common frog (Rana temporaria): routes of postglacial colonization into the British Isles, and evidence for an Irish glacial refugium. Heredity, 102, 490–496.

    Article  PubMed  CAS  Google Scholar 

  • Templeton, A. R., Crandall, K. A., & Sing, C. F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–633.

    PubMed  CAS  Google Scholar 

  • Toews, D. P. L., & Brelsford, A. (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21, 3907–3930.

    Article  PubMed  CAS  Google Scholar 

  • Veith, M., Schmidtler, F. J., Kosuch, J., Baran, I., & Seitz, A. (2003). Paleoclimatic changes explain Anatolian mountain frogs: evolution: a test for alternating vicariance and dispersal events. Molecular Ecology, 12, 185–199.

    Article  PubMed  CAS  Google Scholar 

  • Veith, M., Baumgart, A., Dubois, A., Ohler, A., Galán, P., Vieites, D. R., et al. (2012). Discordant patterns of nuclear and mitochondrial introgression in Iberian populations of the Common frog. Journal of Heredity, 103, 240–249.

    Article  PubMed  CAS  Google Scholar 

  • Vörös, J., & Arntzen, J. W. (2010). Weak population structuring in the Danube crested newt, Triturus dobrogicus, inferred from allozymes. Amphibia-Reptilia, 31, 339–346.

    Article  Google Scholar 

  • Waltari, E., Hijmans, R. J., Peterson, A. T., Nyári, Á. S., Perkins, S. L., & Guralnick, R. P. (2007). Locating pleistocene refugia: Comparing phylogeographic and ecological niche model predictions. PLoS One, 2, e563.

    Article  PubMed  Google Scholar 

  • Warren, D. L., Glor, R. E., & Turelli, M. (2010). ENMTools: a toolbox for comparative studies of environmental niche models. Ecography, 33, 607–611.

    Article  Google Scholar 

  • Wiens, J. J. (2000). Reconstructing phylogenies from allozyme data: comparing method performance with congruence. Biological Journal of the Linnean Society, 70, 613–632.

    Article  Google Scholar 

  • Yakovleva, T. I., & Yakovlev, A. G. (2009). Characteristics of Holocene amphibians and reptiles locations of the west slope of Southern Urals. Samarskaya Luka, Togliatti, 20, 28–48.

    Google Scholar 

  • Zeisset, I., & Beebee, T. J. C. (2007). Two clades of north European pool frogs Rana lessonae identified by cytochrome b sequence analysis. Herpetological Journal, 17, 255–260.

    Google Scholar 

Download references

Acknowledgments

The following persons contributed greatly to some part of the process of this study, during the fieldtrips, laboratory analyses, or reading the manuscript and providing helpful improvements: O. S. Bezman-Moseiko, M. N. Brynskikh, A. Yu. Guseva, O. I. Evstigneev, A. I. Fayzulin, V. P. Foroshchuk, V. P. Ivanchev, N. A. Karpov, V. I. Kazakov, M. D. Khalturin, I. M. Kotserzhinskaya, O. V. Kukushkin, N. F. Marchenko, L. F. Mazanaeva, G. A. Mazepa, K. D. Milto, R. V. Novitsky, M. V. Pestov, J. Plötner, A. V. Ruchin, D. A. Shabanov, A. S. Shapovalov, D. V. Skorinov, S. Yu. Trofimov, M. Veith, A. A. Vlasov, B. Wielstra, and A. I. Zobov. The work was partially funded by grants from the Russian Foundation of Basic Research (project nos. 12-04-01277 and 13-04-90410) and the Serbian Ministry of Education and Science and Technological Development (project no. 173043). PdP was funded by the FI program (Generalitat de Catalunya, Spain) and a grant from the Societas Europaea Herpetologica (2010). Fieldwork in Italy in 2008 was conducted under permit decision DPN-2008-0011754 of 12/05/2008 issued to AC and FA and in Morocco in 2008 and 2009 under permit decision 84°HCEFLCD/DLCDPN/DPRN/CFF issued by Haut Commissariat aux Eaux et Forêts et à la Lutte Contre la Désertification to PdP and DD. The work of AC was supported by a postdoctoral grant from Fundação para a Ciência e a Tecnologia (SFRH/BPD/72908/2010).

Author information

Authors and Affiliations

  1. Institute of Cytology of Russian Academy of Sciences, Tikhoretsky pr. 4, 194064, St. Petersburg, Russia

    Spartak N. Litvinchuk & Jury M. Rosanov

  2. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, R. Padre Armando Quintas, 4485-661, Vairão, Portugal

    Angelica Crottini

  3. ZooPlantLab, Dipartimento di Biotecnologie e Bioscienze, Universitá degli Studi di Milano-Bicocca, Piazza della Scienza, 2, Milano, Italy

    Silvia Federici

  4. Escola Tècnica Superior Enginyeria Agrària, Departament Producció Animal (Fauna Silvestre), University of Lleida, 125198, Lleida, Spain

    Philip De Pous

  5. Institute of Evolutionary Biology (CSIC-UPF), Passeig Maritim de la Barceloneta 37-49, 08003, Barcelona, Spain

    Philip De Pous

  6. Society for the Preservation of Herpetological Diversity, Oude Molstraat 2E, 2513 BB, Den Haag, The Netherlands

    Philip De Pous

  7. Calle Mar Egeo 7, 11407, Jerez de la Frontera, Cadiz, Spain

    David Donaire

  8. Museo Regionale di Scienze Naturali, Via G. Giolitti 36, 10123, Torino, Italy

    Franco Andreone

  9. Faculty of Biology, Institute of Zoology, Studentski trg. 3, Belgrade, 11000, Serbia

    Miloš L. Kalezić

  10. Institute for Biological Research, 29 Novembra 142, Belgrade, 11000, Serbia

    Georg Džukić

  11. Tambov State University, Internatsionalnaya 33, Tambov, 392000, Russia

    Georgy A. Lada

  12. Zoological Institute of Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, 199034, Russia

    Leo J. Borkin

Authors
  1. Spartak N. Litvinchuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angelica Crottini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Silvia Federici
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philip De Pous
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David Donaire
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Franco Andreone
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Miloš L. Kalezić
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Georg Džukić
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Georgy A. Lada
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Leo J. Borkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jury M. Rosanov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Spartak N. Litvinchuk.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 565 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Litvinchuk, S.N., Crottini, A., Federici, S. et al. Phylogeographic patterns of genetic diversity in the common spadefoot toad, Pelobates fuscus (Anura: Pelobatidae), reveals evolutionary history, postglacial range expansion and secondary contact. Org Divers Evol 13, 433–451 (2013). https://doi.org/10.1007/s13127-013-0127-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-013-0127-5

Keywords

Search

Navigation