Allozyme and Genome Size Variation in Tree Frogs from the Caucasus, with Description of a New Subspecies Hyla arborea gumilevskii, from the Talysh Mountains

Spartak N. Litvinchuk, Leo J. Borkin, Jury M. Rosanov, Dmitry V. Skorinov

Abstract


The genome size and allozyme (20 loci) variation in the European (Hyla arborea) and Middle Eastern (H. savignyi) tree frogs in the Caucasus was studied. Additional samples of these species from eastern Europe and Turkey, as well as a sample of the Far Eastern H. japonica, were used for comparison. According to genome size and allozyme data, three geographically distinct groups were revealed among the Caucasian tree frogs. The main territory of the Caucasian region, including the Great Caucasian Range, is inhabited by H. arborea, the Caucasus Minor — by H. savignyi, whereas the Talysh Mountains (Azerbaijan) situated in the extreme south-east of the region harbor another tree frog with reduced inguinal loop. The highest genetic difference was found between the Talysh tree frog and H. savignyi (D = 0.42), the middle one — between H. savignyi and H. arborea (D = 0.27 – – 0.38), and the lowest value between the Talysh tree frog and H. arborea (D = 0.13). The genetic distances between these West Palearctic species and H. japonica were relatively high (D = 0.43 – 0.59). Additionally, we found high genome size differences between the Talysh tree frog and H. arborea, as well as between the former one and H. savignyi. Based on these data, we recognized the Talysh tree frogs as a new subspecies, Hyla arborea gumilevskii, subsp. nov. Hyla arborea schelkownikowi was treated as a junior synonym of H. a. arborea.

Keywords


Amphibia; Hylidae; genome size; nuclear DNA content; flow cytometry; allozymes; Hyla arborea; Hyla savignyi; Hyla japonica; Hyla arborea gumilevskii; subsp. nov

Full Text:

PDF

References


Alekperov A. M. (1957), Amphibia and Reptilia of Azerbaijan. Doctoral Thesis. Vol. 1, Izd. Zool. Inst., USSR Academy of Sciences, Leningrad [in Russian].

Alekperov A. M. (1978), Zemnovodnye i Presmykayushchiyesya Azerbaydzhana [Amphibians and Reptiles of Azerbaijan], Elm, Baku, [in Russian].

Baloutch M. and Kami H. G. (1995), Amphibians of Iran, University Publications of Tehran, Tehran [in Farsi].

Bannikov A. G., Darevsky I. S., Rustamov A. K., and Szczerbak N. N. (1977), Opredelitel’ Zemnovodnykh i Presmykayushchikhsya Fauny SSSR [Guidebook of Amphibians and Reptiles of the USSR Fauna], Prosveshchenie, Moscow [in Russian].

Bedriaga J. (1890), «Die Lurchfauna Europa’s», Bull. Soc. Imp. Naturalistes Moscou, année 1899, 3, 466 – 622.

Blanford W. T. (1876), Eastern Persia. An Account of the Journeys of the Persian Boundary Commission 1870 – 71 – 72. Vol. II. The Zoology and Geology, Macmillan and Co., London.

Boettger O. (1886), «Die Reptilien und Amphibien des Talysch-Gebietes. Nach den neuesten Materialien bearbeitet», in: Radde G., Die Fauna und Flora des südwestlichen Caspi-Gebietes. Wissenschaftliche Beiträge zu den Reisen an der Persisch-Russischen Grenze, F. A. Brockhaus, Leipzig, pp. 30 – 81.

Boettger O. (1899), «Reptilia et Batrachia», in: Die Sammlungen des Kaukasischen Museums, im Vereine mit Special-Gelehrten Bearbeitet, und Herausgegeben von Dr. Gustav Radde. Bd. 1. Zoologie, Tiflis, pp. 271 — 290 [in Russian and German].

Borkin L. J. (1987), «On the systematics and zoogeography of amphibians of the Caucasus», in: Borkin L. J. (ed.), Herpetological Investigations in the Caucasus, pp. 47 – 58 (Trudy Zool. Inst. AN SSSR, Vol. 158 for 1986, in Russian, with English summary).

Borkin L. J. (1998), «Amphibia», in: Ananjeva N. B., Borkin L. J., Darevsky I. S., and Orlov N. L., The Encyclopedia of Nature of Russia. Zemnovodnye i Presmykayushchiyesya [Amphibians and Reptiles], ABF, Moscow, pp. 19 – 174 [in Russian].

Borkin L. J. (1999), «Distribution of amphibians in North Africa, Europe, Western Asia, and the former Soviet Union», in: Duellman W. E. (ed.), Patterns of Distribution of Amphibians: a Global Perspective, The Johns Hopkins Univ. Press, Baltimore – London, pp. 329 – 420.

Borkin L. J., Caune I. A., Pisanetz E. M., and Rozanov Y. M. (1986), «Karyotype and genome size in the Bufo viridis group», in: Roček Z. (ed.), Studies in Herpetology, Charles University, Prague, pp. 137 – 142.

Borkin L. J., Litvinchuk S. N., Milto K. D., Rosanov J. M., and Khalturin M. D. (2001a), «Cryptic speciation in Pelobates fuscus (Anura, Pelobatidae): cytometrical and biochemical evidences», Dokl. RAN, 376(5), 707 – 709 [in Russian; full English version in Doklady Biol. Sci., 376, 86 – 88].

Borkin L. J., Litvinchuk S. N., Rosanov J. M., and Milto K. D. (2001b), «Cryptic speciation in Pelobates fuscus (Anura, Pelobatidae): evidence from DNA flow cytometry», Amphibia–Reptilia, 22(4), 387 – 396.

Borkin L. J., Litvinchuk S. N., Rosanov J. M., and Skorinov D. V. (2004b), «On cryptic species (from the example of amphibians)», Zool. Zh., 83, 936 – 960 [in Russian; full English version in Entomol. Rev., 84(Suppl. 1), S75 – S98].

Boulenger G. A. (1882), Catalogue of the Batrachia gradientia s. caudata and Batrachia apoda in the collection of the British Museum, London.

Cavalier-Smith T. (1985), «Introduction: the evolutionary significance of genome size», in: Cavalier-Smith T. (ed.), The Evolution of Genome Size, John Wiley and Sons, Chichester, pp. 1 – 36.

Chernov S. A. (1926), «On study of herpetofauna of Armenia and Nakhichevan», Bull. Sci. de l’Inst. l’Explotation Regional du Caucase du Nord, 1, 63 – 71 [in Russian].

Chipman A. D., Khaner O., Haas A., and Tchernov E. (2001), «The evolution of genome size: what can be learned from anuran development?» J. Exp. Zool., 291, 365 – 374.

Danielyan F. D. and Egiasarian E. M. (1973), «Bioacoustic analysis of mating calls of the European tree frog in Armenia», in: Darevsky I. S. (ed.), The Problems of Herpetology. Abstrs. of the 3rd USSR Herpetol. Conf., Nauka, Leningrad, p. 74 [in Russian].

Darevsky I. S. (1987), «Protection of amphibians and reptiles in reserves of the Caucasus», in: Darevsky I. S. and Krever V. G. (eds.), Amphibii i Reptilii Zapovednykh Territoriy [Amphibians and Reptiles of Protected Territories], Moscow, pp. 85 – 101 [in Russian].

De Smet W. H. O. (1981), «The nuclear Feulgen-DNA content of the vertebrates (especially reptiles), as measured by fluorescence cytophotometry, with notes on the cell and chromosome size», Acta Zool. Pathol. Antverp., 76, 119 – 167.

Dorowatowsky N. (1913), «Katalog der Kollektionen des Museums Zoologischen Institut d. K. Universität zu St. Petersburg. I. Lurche (Amphibia)», Trav. Soc. Imp. Naturalistes de St.-Pétersbourg, 42(4), 1 – 56 [in Russian, with German resume].

Egiasarian E. M. and Schneider H. (1990), «The mating calls of tree frogs in Armenia (Anura, Hylidae)», Zool. Anz., 225(3/4), 113 – 122.

Egiasarian E. M. and Schneider H. (1991), «New research of structure and variability of mating calls of tree frog Hyla savignyi (Anura, Hylidae) in Armenia», Biol. Zh. Armenia, 44(3), 181 – 186 [in Russian, with English summary].

Eichwald E. (1831), Zoologia specialis quam expositis animalibus tum vivis, tum fossibilibus potissimum Rossiae in universum, et Poloniae in specie, in usum lectionum publicorum in Universitate Caesare Vilnensi habendarum edidit D. Eduardus Eichwald, P.P.O. Tome 3. Pars posterior specialem expositionem Spondylozoorum continens, Typis Josephi Zawadski, Vilnae.

Eiselt J. and Schmidtler J. F. (1973), «Froschlurche aus dem Iran unter Berücksichtigung außeriranischer Populationsgruppen», Ann. Naturhist. Mus. Wien, 77, 181 – 243.

Faivovich J. N., Haddad C. F. B., Garcia P. C. A., Frost D. R., Campbell J. A., and Wheeler W. C. (2005), «Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision», Bull. Am. Mus. Nat. Hist., 294, 1 – 240.

Felsenstein J. (2004), PHYLIP ver. 3.6b. Distributed by the Author, Univ. of Washington, Seattle.

Forcart L. (1949), «Amphibien und Reptilien von Iran», in: Aellen P. (ed.), Ergebnisse einer botanisch-zoologisch Sammelreise durch den Iran, pp. 133 – 156.

Ganiev F. R. and Nuriev E. R. (2000), «Amphibia», In: Gadzhiev D. V. and Rakhmatulina I. K. (eds.), Animals of Azerbaijan. Vol. 3. Vertebrates, Elm, Baku, pp. 179 – 194 [in Russian].

Güldenstädt J. A. (1787), D. Johann Anton Güldenstädt Russisch-Kayserl. Akademikers und Professors der Naturgeschichte auch der Chutfürstl. Mannzischen und der Berlin. Naturforschenden, wie auch der St. Petersburgischen ökonomischen Gesellschaft Mitgliedes, Reisen durch Russland und im Caucasischen Gebürge, Kayserl, Akademie der Wissenschaften, St. Petersburg.

Gumilevsky B. A. (1939), «Amphibian fauna of Armenia and Nakhichevan», Zool. Sb. Issue 1, Trudy Biol. Inst. Arm. Fil. AN SSSR, 3, 3 — 24 [in Russian].

Gvozdík V., , Moravec J., and Kratochvil L. (2005), «Morphometric analysis of geographic variation in Hyla savignyi and southeastern populations of Hyla arborea», in: Abstrs. and Program of the 5th World Congr. of Herpetol., Stellenbosch, p. 131.

Harrison T. M., Copeland P., Kidd W. S. F., and Yin A. (1992), «Raising Tibet», Science, 255, 1663 – 1670.

Igawa T., Kurabayashi A., Nishioka M., and Sumida M. (2006), «Molecular phylogenetic relationship of toads distributed in the Far East and Europe inferred from the nucleotide sequences of mitochondrial DNA genes», Mol. Phyl. Evol., 38, 250 – 260.

Khalturin M. D., Litvinchuk S. N., Borkin L. J., Rosanov J. M., and Milto K. D. (2003), «Genetic variation in two cryptic forms of the common spadefoot toad Pelobates fuscus (Pelobatidae, Anura, Amphibia) differing in genome size», Tsitologiya, 45, 308 – 323 [in Russian, with English summary].

Kumar S., Tamura K., Jakobsen I. B., and Nei M. (2001), MEGA2: Molecular Evolutionary Genetics Analysis Software, Arizona State Univ., Tempe, AZ, USA.

Kuzmin S. L. (1999), Zemnoodnye Byvshego SSSR [The Amphibians of the Former Soviet Union], KMK, Moscow [in Russian.

Kyriakopoulou-Sklavounou P., Xeros G., Charilaou C., and Tsiora A. (2003), «Preliminary data on the genetic differentiation of populations of three frog species (Anura, Amphibia) from Cyprus and Greece», Belg. J. Zool., 133(2), 191 – 193.

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

Licht L. E. and Lowcock L. A. (1991), «Genome size and metabolic rate in salamanders», Comp. Biochem. Physiol., 100B, 83 – 92.

Linnaeus C. (1758 [1956]), Caroli Linnaei Systema Naturae. A photographic facsimile of the first volume of the tenth edition (1758). Regnum Animale, British Museum (Natural History), London.

Litvinchuk S. N., Borkin L. J., Dћukić G., Kalezić M. L., Khalturin M. D., and Rosanov Y. M. (1999), «Taxonomic status of Triturus karelinii on the Balkans, with some comments about other crested newt taxa», Russ. J. Herpetol., 6(2), 153 – 163.

Litvinchuk S. N., Borkin L. J., and Rosanov J. M. (2004), «Intra- and interspecific genome size variation in hynobiid salamanders of Russia and Kazakhstan: determination by flow cytometry», Asiatic Herpetol. Res., 10, 282 – 294.

Litvinchuk S. N., Borkin L. J., Rosanov J. M., Skorinov D. V., Khalturin M. D., Dћukić G., Kalezić M. L., and Mazanaeva L. F. (2005a), «Geographic differentiation in newts (Triturus) of eastern Europe: genome size, allozymes, and morphology», in: Ananjeva N. and Tsinenko O. (eds.), Herpetologica Petropolitana. Proc. of the 12th Ord. Gen.Meeting Soc. Eur. Herpetol., August 12 – 16, 2003, St. Petersburg, Russ. J. Herpetol., 12(Suppl.), pp. 51 – 54.

Litvinchuk S. N., Rosanov J. M., and Borkin L. J. (1997), «A contact zones between the newts Triturus cristatus and Triturus dobrogicus in the Ukrainian Transcarpathians: distribution and genome size variation», in: Böhme W., Bischoff W., and Ziegler T. (eds.), Herpetologia Bonnensis, Bonn, pp. 229 – 235.

Litvinchuk S. N., Rosanov J. M., and Borkin L. J. (2001a), «Natural autotriploidy in the Danube newt, Triturus dobrogicus (Salamandridae)», Russ. J. Herpetol., 8(1), 74 – 76.

Litvinchuk S. N., Rosanov J. M., Borkin L. J., Khalturin M. D., Timofeev B. I., Dћukić G., and Kalezić M. L. (2001b), «Genome size and some problems of urodelan systematics (Salamandridae and Hynobiidae)», in: Ananjeva N. B. et al. (eds.), The Problems of Herpetology, Pushchino – Moscow, pp. 168 – 170 [in Russian, with English summary].

Litvinchuk S. N., Zuiderwijk A., Borkin L. J., and Rosanov J. M. (2005b), «Taxonomic status of Triturus vittatus (Amphibia: Salamandridae) in western Turkey: trunk vertebrae count, genome size and allozyme data», Amphibia– Reptilia, 26, 305 – 323.

Lizana M., Marquez R., Martin-Sanchez R., Ciudad J., Lopez A., and Orfao A. (2000), «Determination of cellular DNA content of Iberian salamanders by flow cytometry», Amphibia–Reptilia, 21, 411 – 418.

MacCulloch R. D., Upton D. E., and Murphy R. W. (1996), «Trends in nuclear DNA content among amphibians and reptiles», Comp. Biochem. Physiol., 113B, 601 – 605.

Mazin A. L. (1980), «Amounts of nuclear DNA in anurans of the USSR», Experientia, 36, 190 – 191.

Ménétries E. (1832), Catalogue raisonné des Objets de Zoologie recueillis dans un Voyage au Caucase et jusquaux Frontières actuelles de la Perse entrepris par ordre de S. M. LEmpereur. LImprimerie de lAcadémie Impériale des Sciences, St. Pétersbourg.

Mezhzherin S. V. and Morozov-Leonov S. Y. (1999), «Allozyme variation and genetic relationships of European tree frog Hyla arborea (L., 1758) (Amphibia: Hylidae) from the Crimea Mountains», Tsitol. Gen. Kiev, 33(1), 44 – 48 [in Russian, with English summary].

Murphy R. W., Lowcock L. A., Smith C., Darevsky I. S., Orlov N., MacCulloch R. D., and Upton D. E. (1997), «Flow cytometry in biodiversity surveys: methods, utility, and constraints», Amphibia–Reptilia, 18, 1 – 13.

Nei M. (1978), «Estimation of average heterozygosity and genetic distance from a small number of individuals», Proc. Natl. Acad. Sci. USA, 70, 3321 – 3323.

Nikolsky A. M. (1905), «Herpetologia Rossica», Mém. l’Acad. Imp. Sci. de St. Pétersbourg. VIIIe Sér. Classe Phys.-Math., 17(1) [in Russian].

Nikolsky A. M. (1913), Herpetologia Caucasica, The Caucasian Museum, Tiflis [in Russian].

Nikolsky A. M. (1918), Amphibia. Faune de la Russie et des Pays limitrophes, L’Académie des Sciences de Russie, Petrograd [in Russian].

Oeldorf E., Nishioka M., and Bachman K. (1978), «Nuclear DNA amounts and development rate in Holarctic Anura», Zeitschr. Zool. Syst. Evolutionsforsch., 16, 216 – 224.

Olmo E. (1983), «Nucleotype and sell size in vertebrates: a review», Basic Appl. Histochem., 27, 227 – 256.

Pallas P. S. (1814), Zoographia Rosso-Asiatica, sistens omnium animalium in extenso Imperio Rossico et adjacentibus maribus observatorum recensionem, domicilia, mores et descriptiones, anatomen atque icones plurimorum. Tomus III. Animalia monocardia seu frigidi sanguinis Imperii Rosso-Asiatici. Ex officina Caes., Academiae Scientarum, Petropoli.

Pryalkina T. I. (1989), Study of Systematic Relationships between Anurans of the USSR Fauna with Use of Comparative Analysis of Proteins. Author’s Abstract of Candidate’s Thesis, Zoological Institute, USSR Academy of Sciences, Leningrad [in Russian].

Rosanov J. M. and Vinogradov A. E. (1998), «Precise DNA cytometry: investigation of individual variability in animal genome size», Tsitologiya, 40, 792 – 800 [in Russian].

Saitou N. and Nei M. (1987), «The neighbor-joining method: a new method for reconstructing of phylogenetic trees», Mol. Biol. Evol., 4, 406 – 425.

Schneider H. and Nevo E. (1972), «Bio-acoustic study of the yellow-lemon treefrog, Hyla arborea savignui Audouin», Zool. Jb. Physiol., 76, 497 – 506.

Schelkownikow A. B. (1911), «Bericht über eine Reise nach Zuvant im Juli 1906», Mittel. Kaukasischen Mus., 5, 171 – 216 [in Russian, with German summary].

Sobolevsky N. I. (1929), «The herpetofauna of the Talysh and the Lenkoran Lowland», Mem. Soc. Amis Sci. Naturelles. d’Antropol. d’Ethnographie, 5, 1 – 143 [in Russian].

Sokal R. R. and Sneath P. H. A. (1963), Principles of Numerical Taxonomy, Freeman, San Francisco.

Swofford D. L. and Selander R. B. (1981), BIOSYS-1. A Computer Program for the Analysis of Allelic Variation in Population Genetics and Biochemical Systematics. Distributed by the Author, Illinois Natural Hystory Survey, Champaigh.

Tarkhnishvili D. N. and Gokhelashvili R. K. (1999), «The Amphibians of the Caucasus», Adv. Amphibian Res. Former Soviet Union, 4, 1 – 233.

Terentjev P. V. (1960), «An example of biometrical study of Schelkovnikov’s tree frog», Vestnik LGU. Ser. Biol., 21(4), 119 – 136 [in Russian].

Terentjev P. V. and Chernov S. A. (1949), Opredelitel’ Presmykayushchikhsya i Zemnovodnykh [Guidebook of Reptiles and Amphibians]. 3rd Edition, Sovetskaya Nauka, Moscow – Leningrad [in Russian].

Tuniyev B. S. (1985), «New records of amphibians and reptiles in the Caucasus», in: Darevsky I. S. (ed.), The Problems of Herpetology, Leningrad, pp. 213 – 214 [in Russian].

Tuniyev B. S. (1999 [1998]), «A systematic list of amphibians from the Alpides of the Caucasus and Middle Asia, with comments on their taxonomy», Adv. Amphibian Res. Former Soviet Union, 3, 43 – 75.

Velieva Z. D. (1975), Fauna and Ecology of Amphibia of Southeastern Azerbaijan. Author’s Abstract of Candidate’s Thesis, Azerbaijan State Pedagogical Inst., Baku [in Russian].

Vialli M. (1957), «Volume et contenu en ADN par noyau», Exp. Cell Res., 4(Suppl.), 284 – 293.

Vinogradov A. E. (1998), «Genome size and GC-percent in vertebrates as determined by flow cytometry: the triangular relationship», Cytometry, 31, 100 – 109.

Wright S. (1978), Variability Within and Among Natural Populations, Univ. of Chicago Press, Chicago.

Ullerich F.-H. (1970), «DNA-Gehalt und Chromosomenstruktur bei Amphibien», Chromosoma, 30, 1 – 37.

Zhordania R. G. (1960), «List of collections of amphibians of Zoological Department of State Museum of Georgia im. S. N. Dzhanashia AN GSSR», Trudy Gos. Mus. GrSSR, 20-A, 159 – 179 [in Russian].




DOI: http://dx.doi.org/10.30906/1026-2296-2006-13-3-187-206

Refbacks

  • There are currently no refbacks.