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Molecular differentiation and taxonomy of the sunwatcher toad-headed agama species complex Phrynocephalus superspecies helioscopus (Pallas 1771) (Reptilia: Agamidae)

  • Animal Genetics
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Abstract

Lizards of the sunwatcher toad-headed agama species complex Phrynocephalus superspecies helioscopus, mostly distributed in Central Asia and Middle East, were examined using analysis of variation at the mitochondrial cytochrome oxidase c subunit I gene fragment and fingerprint analysis of nuclear DNA (inter-SINE PCR technique). A total of 86 individual tissue samples from 53 populations, to the full extent representing different parts of the species complex range, were subjected to molecular genetic examination, and surprisingly deep differentiation was revealed. The populations analyzed split into 12 isolated phylogroups, many of which were characterized by a narrow range and genetic isolation. Monophyly of sunwatcher (Ph. helioscopus) and Persian (Ph. persicus) toad-headed agamas was confirmed. However, both of these species probably represent the species complexes. Zoogeography of Central Asiais discussed.

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References

  1. Bannikov, A.G., Darevsky, I.S., Ishchenko, V.G., et al., Opredelitel’ zemnovodnykh i presmykayushchikhsya fauny SSSR (Key to the Fauna of the Soviet Union: Amphibians and Reptiles), Moscow: Prosveshchenie, 1977.

    Google Scholar 

  2. Sokolovskii, V.V., Comparative Karyological Study of Lizards of the Family Agamidae: I. Chromosome Complements of 8 Species of the Genus Phrynocephalus, Tsitologiya, 1974, vol. 16, no. 7, pp. 920–925.

    CAS  Google Scholar 

  3. Manilo, V.V., Golubev, M.L., and Sattorov, T., Karyotype of Phrynocephalus helioscopus saidalievi (Sauria, Agamidae) from Fergana Valley, Vestn. Zool., 1991, no. 2, pp. 79–81.

  4. Manilo, V.V. and Golubev, M.L., Karyotype Information on Some Toad Agamas of the Phrynocephalus guttatus Species Group (Sauria, Agamidae) of the Former USSR, Asiatic Herpetol. Res., 1993, vol. 5, pp. 105–108.

    Google Scholar 

  5. Eremchenko, V.K. and Panfilov, A.M., Some Methodological Questions on Taxonomy and Phylogeny of Toad-Headed Agamas by Example of Phrynocephalus helioscopus (Pallas, 1771) (Sauria: Agamidae), Nauka Novye Technol., 1999, no. 3, pp. 116–122.

  6. Ushakov, B.P., Cytophysiological Analysis of Intraspecies Differentiation of Takyr Toad-Headed Lizards, Dokl. Akad. Nauk SSSR, 1962, vol. 144, no. 5, pp. 1178–1180.

    Google Scholar 

  7. Melville, J., Hale, J., Mantziou, G., et al., Historical Biogeography, Phylogenetic Relationships and Intraspecific Diversity of Agamid Lizards in the Central Asian Deserts of Kazakhstan and Uzbekistan, Mol. Phylogenet. Evol., 2009, vol. 53, pp. 99–112.

    Article  PubMed  CAS  Google Scholar 

  8. Melnikov, D.A., On Systematics and Phylogeography of Sun Watcher Toad Agamas Phrynocephalus helioscopus (Pallas, 1771), in Otchetnaya nauchnaya sessiya po itogam rabot 2007 g (Scientific Session Reporting Research Results of 2007), (Proc. Conf.), St. Petersburg, 2008, pp. 32–34.

  9. Melnikov, D.A., Ananjeva, N.B., Rajabizadeh, M., and Milto, K.D., On Systematics and Phylogeography of Sun Watcher Toad Headed Agamas Phrynocephalus helioscopus (Pallas, 1771), De Agamis, (Proc. Int. Symp. Agamis Lizards), Bonn, 2008, pp. 21–22.

  10. Solovyeva, E.N. and Poyarkov, N.A., Specificity of Systematics and Phylogeography of Sun Watcher Toad Headed Agamas (Phrynocephalus helioscopus) (Reptilia: Agamidae) Species Complex, in Tezisy XVI konferentsii studentov, aspirantov i molodykh uchenykh “Lomonosov-2009”, sektsiya Biologiya (Abstracts 16th Conference of Students, Postgraduates, and Young Scientists “Lomonosov-2009”, Section Biology), Moscow, 2009, pp. 10–11.

  11. Solovyeva, E.N. and Poyarkov, N.A., Analysis of Sun Watcher Toad Headed Agamas (Phrynocephalus helioscopus) (Reptilia: Agamidae) Species Complex Distribution Using GIS-Mapping, in Tezisy XVI konferentsii studentov, aspirantov i molodykh uchenykh “Lomonosov-2010”, sektsiya Biologiya (Abstracts 16th Conference of Students, Postgraduates, and Young Scientists “Lomonosov-2010”, Section Biology), Moscow, 2010, p. 142.

  12. Solovyeva, E.N., Poyarkov, N.A., Dunayev, E.A., et al., Taxonomy and Phylogeography of the Sunwatcher Toad-Headed Agama Species Complex (Phrynocephalus helioscopus and Phrynocephalus persicus; Reptilia: Agamidae), in SEH 15th OGM, Programs and Abstracts, Kusadasi: Aydin, 2009, pp. 77–78.

    Google Scholar 

  13. Solovyeva, E.N., Poyarkov, N.A., Dunayev, E.A., and Bannikova, A.A., Phylogeny of the Sunwatcher Agama Species Complex, Phrynocephalus helioscopus (Reptilia, Agamidae) Inferred from Mitochondrial and Nuclear DNA Markers, Molecular Phylogenetics, (Proc. 2nd Moscow Int. Conf. MolPhy-2), Moscow, 2010, p. 71.

  14. Solovyeva, E.N., Molecular Differentiation and Distribution within the Species Complex of Phrynocephalus helioscopus (Reptilia: Agamidae) De Agamis, (Proc. 2nd Int. Symp. Agamis Lizards), St. Petersburg, 2010, pp. 26–27.

  15. Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, New York: Cold Spring Harbor Lab., 1989.

    Google Scholar 

  16. Ivanova, N.V. and Hebert, P.D.N., An Inexpensive, Automation-Friendly Protocol for Recovering High-Quality DNA, Mol. Ecol. Notes, 2006, vol. 6, pp. 998–1002.

    Article  CAS  Google Scholar 

  17. Bannikova, A.A., Bulatova, N.Sh., and Kramerov, D.A., Molecular Variability in the Commom Shrew Sorex araneus L. from European Russia and Siberia Inferred from the Length Polymorphism of DNA Regions Flanked by Short Interspersed Elements (Inter-SINE PCR) and the Relationships between the Moscow and Seliger Chromosome Races, Russ. J. Genet., 2006, vol. 42, no. 6, pp. 595–604.

    Article  CAS  Google Scholar 

  18. Jurka, J., Zietkiewicz, E., and Labuda, D., Ubiquitous Mammalian-Wide Interspersed Repeats (MIRs) Are Molecular Fossils from the Mesozoic Era, Nucl. Acids Res., 1995, vol. 23, no. 1, pp. 170–175.

    Article  PubMed  CAS  Google Scholar 

  19. Hall, T.A., BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT, Nucl. Acids Symp., 1999, ser. 41, pp. 95–98.

  20. Swofford, D.L., Phylogenetic Analysis Using Parsimony (and Other Methods): Version 4, Sunderland: Sinauer, 1998.

    Google Scholar 

  21. Tamura, K., Dudley, J., Nei, M., and Kumar, S., MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0, Mol. Biol. Evol., 2007, vol. 24, pp. 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  22. Nei, M. and Li, W.-H., Mathematical Model for Studying Genetic Variation in Terms of Restriction Endonucleases, Proc. Natl. Acad. Sci. USA, 1979, vol. 76, pp. 5269–5273.

    Article  PubMed  CAS  Google Scholar 

  23. STATISTICA for Windows (Computer Program Manual), Tulsa: StatSoft, 1996.

  24. Excoffier, L., Smouse, P.E., and Quattro, J.M., Analysis of Molecular Variance Inferred from Metric Distances among DNA Haplotypes: Application to Human Mitochondrial DNA Restriction Data, Genetics, 1992, vol. 131, no. 2, pp. 479–491.

    PubMed  CAS  Google Scholar 

  25. Excoffier, L., Laval, G., and Schneider, S., Arlequin ver. 3.5.1.2: An Integrated Software Package for Population Genetics Data Analysis, http://cmpg.unibe.ch/software/arlequin35.

  26. Tajima, F., Evolutionary Relationship of DNA Sequences in Finite Populations, Genetics, 1983, vol. 105, pp. 437–460.

    PubMed  CAS  Google Scholar 

  27. Rogers, A.R. and Harpending, H., Population Growth Makes Waves in the Distribution of Pairwise Genetic Differences, Mol. Biol. Evol., 1992, vol. 9, pp. 552–569.

    PubMed  CAS  Google Scholar 

  28. Aris-Brosou, S. and Excoffier, L., The Impact of Population Expansion and Mutation Rate Heterogeneity on DNA Sequence Polymorphism, Mol. Biol. Evol., 1996, vol. 13, pp. 494–504.

    PubMed  CAS  Google Scholar 

  29. Ray, N., Currat, M., and Excoffier, L., Intra-Deme Molecular Diversity in Spatially Expanding Populations, Mol. Biol. Evol., 2003, vol. 20, pp. 76–86.

    Article  PubMed  CAS  Google Scholar 

  30. Ryabinina, N.L., Bannikova, A.A., Sheremet’eva, V.A., et al., Analysis of DNA of Higher Primates Using Inter-SINE PCR, Russ. J. Genet., 2008, vol. 44, no. 3, pp. 266–272.

    Article  CAS  Google Scholar 

  31. Ryabinina, N.L., Bannikova, A.A., Kosuchkin, S.A., et al., Estimation of the Subspecific Level of Differentiation in Caucasian Lizards of the Genus Darevskia (Syn. “Lacerta saxicola Complex”, Lacertidae, Sauria) Using Genome DNA Markers, Russ. J. Herpetol., 2002, vol. 9, no. 3, pp. 185–194.

    Google Scholar 

  32. Grechko, V.V., Bannikova, A.A., Kosushkin, S.A., et al., Molecular Genetic Diversification of the Lizard Complex Darevskia raddei (Sauria: Lacertidae): Early Stages of Speciation, Mol. Biol. (Moscow), 2007, vol. 41, no. 5, pp. 839–851.

    Article  CAS  Google Scholar 

  33. Buntjer, J.B., DNA Repeats in Vertebrate Genome as Probes in Phylogeny and Species Identification, Utrecht: Univ. Utrecht, 1997, pp. 25–38.

    Google Scholar 

  34. Bannikova, A.A., Matveev, V.A., and Kramerov, D.A., Using Inter-SINE-PCR to Study Mammalian Phylogeny, Russ. J. Genet., 2002, vol. 38, no. 6, pp. 704–715.

    Article  Google Scholar 

  35. Pang, J., Wang, Y., Zhong, Y., et al., A Phylogeny of Chinese Species in the Genus Phrynocephalus (Agamidae) Inferred from Mitochondrial DNA Sequences, Mol. Phylogenet. Evol., 2003, vol. 27, pp. 398–409.

    Article  PubMed  CAS  Google Scholar 

  36. Dunayev, E.A., Ivanova, N.V., Poyarkov, N.A., et al., Molecular Perspective on the Evolution and Barcoding of Toad-Headed Agamas (Genus Phrynocephalus; Agamidae) in Middle Asia, 14th European Congress of Herpetology and SEH Ordinary General Meeting (Porto (Portugal), 2007), Porto, 2007, p. 208.

  37. Avise, J.C., Arnold, J., Ball, R.M., et al., Intraspecific Phylogeography: The Mitochondrial DNA Bridge between Population Genetics and Systematics, Annu. Rev. Ecol. Syst., 1987, vol. 18, pp. 489–522.

    Google Scholar 

  38. Avise, J.C., Phylogeography: The History and Formation of Species, Cambridge, Massachusetts: Harvard Univ. Press, 2000.

    Google Scholar 

  39. Ananjeva, N.B. and Tuniev, B.S., Historical Biogeography of the Phrynocephalus Species of the USSR, Asiatic Herpetol. Res., 1992, vol. 4, pp. 76–98.

    Google Scholar 

  40. Melnikov, D.A., Ananjeva, N.B., Agasyan, A.L., and Radzhabizade, M., Historical Background and Taxonomic Status of the Persian Toad Head Agama, Phrynocephalus persicus de Filippi, 1863 and Horvath’s Sun Watcher Toad Head Agama Phrynocephalus helioscopus horvathi Mehely, 1894, in Tretii s“ezd gerpetologicheskogo obshchestva im. A.N. Nikol’skogo (The Problems of Herpetology), (Proc. 3rd Congr. of A.N. Nikol’skiy, Herpetological Society, St-Peterburg, 2008), St-Peterburg, 2008, pp. 286–297.

  41. Darevsky, I.S., Turanian Elements in Herpetofauna of Transcaucasia and Conceivable Ingress Routes from Middle Asia, Izv. Akad. Nauk Armyanskoi SSR, 1957, vol. 10, no. 12, pp. 69–77.

    Google Scholar 

  42. Golubev, M.L. and Mezhzherin, S.V., On the Specific Attribution and the Origin of the Persian Toad-Headed Agama Phrynocephalus persicus (Reptilia, Agamidae) Apsheron Population, Byull. Mosk. O-va. Ispytateley Prirody, Otdel Biol., 1999, vol. 104, no. 1, pp. 59–61.

    Google Scholar 

  43. Barabanov, A.V. and Ananjeva, N.A., Catalogue of the Available Scientific Species-Group Names for Lizards of the Genus Phrynocephalus Kaup, 1825 (Reptilia, Sauria, Agamidae), Zootaxa, 2007, vol. 1399, pp. 1–56.

    Google Scholar 

  44. Nikol’skii, A.M., Presmykayushchiesya (Reptilia): Chelonia and Sauria. Fauna Rossii i sopredel’nykh stran (Reptiles (Reptilia): Chelonia and Sauria. Fauna of Russia and Neighboring Countries), Petrograd, 1915.

  45. Dunaev, E.A., Systematics and Paleogeography: Contseptual Synthesis by Example of Phrynocephalus (Superspecies guttatus) (Reptilia: Agamidae), Sb. Tr. Zool. Muzeya Mosk. Gos. Univ., 2009, vol. 50, pp. 275–298.

    Google Scholar 

  46. Sindaco, R. and Jeremcenko, V.K., The Reptiles of the Western Palearctic, Latina: Edizioni Belvedere, 2008.

    Google Scholar 

  47. Fu, J.-z. and Zeng, X.-m., How Many Species Are in the Genus Batrachuperus? A Phylogeographical Analysis of the Stream Salamanders (Family Hynobiidae) from Southwestern China, Mol. Ecol., 2008, vol. 17, pp. 1469–1488.

    Article  PubMed  CAS  Google Scholar 

  48. Guo, X. and Wang, Y., Partitioned Bayesian Analyses, Dispersal-Vicariance Analysis, and the Biogeography of Chinese Toad-Headed Lizards (Agamidae: Phrynocephalus): A Re-Evaluation, Mol. Phylogenet. Evol., 2007, vol, 45, no. 2, pp. 643–662.

    Article  PubMed  CAS  Google Scholar 

  49. Macey, J.R., Schulte, J.A.., Larson, A., et al., Evaluating Trans-Tethys Migration: An Example Using Acrodont Lizard Phylogenetics, Syst. Biol., 2000, vol. 49, no. 2, pp. 233–256.

    Article  PubMed  CAS  Google Scholar 

  50. An Zh.-sh., Kutzbach, J.E., Prell, W.L., and Porter, S.C., Evolution of Asian Monsoons and Phased Uplift of the Himalaya-Tibetan Plateau Since Late Miocene Times, Nature, 2001, vol. 411, pp. 62–66.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Vertebrate Zoology, Lomonosov Moscow State University, Moscow, 119991, Russia

    E. N. Solovyeva, N. A. Poyarkov & A. A. Bannikova

  2. Zoological Museum, Lomonosov Moscow State University, Moscow, 125009, Russia

    E. A. Dunaev

  3. Institute of Zoology, Almaty, 480060, Kazakhstan

    T. N. Duysebayeva

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  1. E. N. Solovyeva
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  2. N. A. Poyarkov
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  3. E. A. Dunaev
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  4. T. N. Duysebayeva
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  5. A. A. Bannikova
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Correspondence to A. A. Bannikova.

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Original Russian Text © E.N. Solovyeva, N.A. Poyarkov, E.A. Dunaev, T.N. Duysebayeva, A.A. Bannikova, 2011, published in Genetika, 2011, Vol. 47, No. 7, pp. 952–967.

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Solovyeva, E.N., Poyarkov, N.A., Dunaev, E.A. et al. Molecular differentiation and taxonomy of the sunwatcher toad-headed agama species complex Phrynocephalus superspecies helioscopus (Pallas 1771) (Reptilia: Agamidae). Russ J Genet 47, 842–856 (2011). https://doi.org/10.1134/S1022795411070155

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  • DOI: https://doi.org/10.1134/S1022795411070155

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