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Distribution, Population Systems, and Peculiarities of Hybrid Gametogenesis in Water Frogs (Pelophylax esculentus complex) in the Dniester River Valley (Moldova)

Spartak N. Litvinchuk, Mariya I. Matiushova, Olga S. Bezman-Moseyko, Georgy A. Lada, Dmitry V. Skorinov, Jury M. Rosanov, Leo J. Borkin

Abstract


Hybridogenesis is well-known attributes of water frogs of the genus Pelophylax. The P. esculentus complex consists of two parental species, P. lessonae and P. ridibundus, as well as their hemiclonal (sometimes meroclonal) hybrid, P. esculentus. DNA flow cytometry, genetic and morphometric analyses were used to examine water frog compositions in 27 localities (n = 212) throughout the Dniester River valley in Moldova. Two species were revealed in the studied region (42% individuals were P. esculentus and 58% P. ridibundus). All frogs proved to be diploid. We registered the first species in 74% localities and the second in 78%. Populations, where we found only P. ridibundus occurred in 26% localities and only P. esculentus in 22%, while mixed population systems in 52%. Both species were usually observed in open water bodies and rivers that flow down through agricultural land and urban areas. In populations of P. esculentus the number of males strongly exceeded (90%) the number of females. The half of studied hybrid males was sterile, and most of fertile hybrid males produced sperm with the genome of P. lessonae. Several hybrid males gave the mixture of sperm with genomes of P. lessonae and P. ridibundus (amphispermy) and only one male with the P. ridibundus genome. Both species had the mitochondrial DNA of P. ridibundus. Based on nuclear markers, in P. esculentus and P. ridibundus we revealed the presence of alleles of the closely related Anatolian species P. cf. bedriagae. This might affect the successful reproduction of hybridogenetic P. esculentus. However, comparison of percentage of sterile males and alleles of P. cf. bedriagae among hybrids showed no correlation.

Keywords


Amphibia; hybridogenesis; flow DNA cytometry; genome size; Pelophylax lessonae; Pelophylax ridibundus; Ranidae

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References


Arioli M. (2007), Reproductive Patterns and Population Genetics in Pure Hybridogenetic Water Frog Populations of Rana esculenta. Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich.

Bezman-Moseyko O. S. (2008), «To the species composition of herpetofauna of Dniester Region (preliminary data)», Tr. Ukr. Gerpetol. Obshch., 1, 43 – 46 [in Russian].

Bezman-Moseyko O. S. (2009), «Specific composition of herpetofauna of «Yagorlyk» Nature Reserve: short review», in: Regional Issues of Environments, Rational Nature Management, and Ways of Their Solving, Tiraspol’, p. 191 [in Russian].

Bezman-Moseyko O. S. (2011), «Ecological and faunal survey of amphibians and reptiles in the Dniester River region», in: N. B. Ananjeva (ed.), The Problems of Herpetology, St. Petersburg, pp. 28 – 30 [in Russian].

Bezman-Moseyko O. S. (2015), «Review of the fauna of Pridnestrov’e», in: S. I. Filipenko (ed.), Readings in Memory of Associate Professor and Candidate of Biological Sciences L. L. Popa, Tiraspol’, pp. 5 – 7 [in Russian].

Bezman-Moseyko O. S., Borkin L. J., Rosanov J. M., and Litvinchuk S. N. (2014), «Mass hindlimb anomalies in green frogs (Pelophylax esculentus complex) in Transnistria: causes and bioindication», in: V. L. Vershinin, A. Dubois, K. Henle, and M. Puki (eds.), Anomalies and Pathologies of Amphibians and Reptiles: Methodology, Evolutionary Impact, Possibility of Assessing Health of Environment, Yekaterinburg, pp. 13 – 19 [in Russian].

Biriuk O. V., Shabanov D. A., Korshunov A. V., Borkin L. J., Lada G. A., Pasynkova R. A., Rosanov J. M., and Litvinchuk S. N. (2016), «Gamete production patterns and mating systems in water frogs of the hybridogenetic Pelophylax esculentus complex in north-eastern Ukraine», J. Zool. Syst. Evol. Res., 54(3), 215 – 225.

Borkin L. J., Caune I., Pikulik M., and Sokolova T. (1986), «Distribution and structure of the green frog complex in the USSR», in: Z. Roček (ed.), Studies in Herpetology, Charles University, Prague, pp. 675 – 678.

Borkin L. J., Vinogradov A. E., Rosanov J. M., and Caune I. A. (1987), «Hemiclonal inheritance in the hybridogenic Rana esculenta complex: evidence from flow DNA cytometry», Dokl. AN USSR, 295, 1261 – 1264 [in Russian].

Borkin L. J., Litvinchuk S. N. and Rosanov Yu. M. (1997), «Amphibians and reptiles of Moldavia: additions and corrections, with a list of species», Russ. J. Herpetol., 4(1), 50 – 62.

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

Borkin L. J., Litvinchuk S. N., Mannapova E. I., Pestov M. V., and Rosanov J. M. (2002), «The distribution of green frogs (Rana esculenta complex) in Nizhny Novgorod Province, central European Russia», Russ. J. Herpetol., 9(3), 195 – 207.

Borkin L. J., Korshunov A. V., Lada G. A., Litvinchuk S. N., Rosanov J. M., Shabanov D. A., and Zinenko A. I. (2004), «Mass occurrence of polyploid green frogs (Rana esculenta complex) in eastern Ukraine», Russ. J. Herpetol., 11(3), 194 – 213.

Borkin L. J., Lada G. A., Litvinchuk S. N., Melnikov D. A., and Rosanov J. M. (2006), «The first record of mass triploidy in hybridogenic green frog Rana esculenta in Russia (Rostov Province)», Russ. J. Herpetol., 13(1), 77 – 82.

Borkin L. J., Bezman-Moseyko O. S., Mazepa G. A., Zinenko A. I., Korshunov A. V., Lada G. A., Shabanov D. A., Litvinchuk S. N., and Rozanov J. M. (2008), «On the southern limit of range of hybrid Rana esculenta (Ranidae, Anura, Amphibia) in Ukraine and Moldova: DNA flow cytometry evidence», Tr. Ukr. Gerpetol. Obshch., 1, 5 – 11 [in Russian].

Borkin L. J., Bezman-Maseyko O. S., and Litvinchuk S. N. (2012), «Evaluation of animal deformity occurrence in natural populations (an example of amphibians)», Tr. Zool. Inst. RAN, 316(4), 324 – 343 [in Russian].

Brauner A. (1903), «Vorläufige Mitteilungen über Reptilien und Amphibien in Bessarabien, Chersoner Gouvernement, der Krim und dem nordwestlichen Kaukasus zwischen Noworossisk und Adler», Zap. Novoross. Obshch. Estestvoisp., 25(1), 43 – 59 [in Russian].

Brauner A. (1907), «Amphibien und Reptilien Bessarabiens», Tr. Bessarab. Obshch. Estestvoisp. Lyubit. Estestvozn., 1(2), 149 – 173 [in Russian].

Caune I. A. (1987), Systematics and Distribution of the Hybridogenetic Rana esculenta Complex in Latvia. Candidate’s Thesis, Zoological Institute, USSR Academy of Sciences, Leningrad [in Russian].

Caune I. A. and Borkin L. J. (1993), «A new variant of an unisexual-bisexual population system in European green frogs (Rana esculenta complex)», Arkh. Zool. Muz. MGU, 30, 34 – 52 [in Russian].

Chepurnov V. S., Burkashev M. S., Saenko Ya. M., and Dolgiy V. N. (1953), «Data on vertebrate fauna of lower Dniester and Prut rivers, and southern regions of Moldavia», Uch. Zap. Kishinev. Univ., 8, 359 – 369 [in Russian].

Chmielewska M., Kaźmierczak M., Rozenblut-Kościsty B., Kolenda K., Dudzik A., Dedukh D., and Ogielska M. (2022), «Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus», Front. Cell Dev. Biol., 10, 1008506.

Dedukh D. V. and Krasikova A. V. (2017), «Methodological approaches for studying the European water frog Pelophylax esculentus complex», Russ. J. Genet., 53(8), 843 – 850.

Dedukh D., Mazepa G., Shabanov D., Rosanov J., Litvinchuk S., Borkin L., Saifitdinova A., and Krasikova A. (2013), «Cytological maps of lampbrush chromosomes of European water frogs (Pelophylax esculentus complex) from the Eastern Ukraine», BMC Genetics, 14, 26.

Dedukh D., Litvinchuk S., Rosanov J., Shabanov D., and Krasikova A. (2017), «Mutual maintenance of di- and triploid Pelophylax esculentus hybrids in R-E systems: results from artificial crossings experiments», BMC Evol. Biol., 17, 220.

Dedukh D., Litvinchuk J., Svinin A., Litvinchuk S., Rosanov J., and Krasikova A. (2019), «Variation in hybridogenetic hybrid emergence between populations of water frogs from the Pelophylax esculentus complex», PLoS ONE, 14(11), e0224759.

Doležálková-Kaštánková M., Pruvost N. B. M., Plötner J., Reyer H.-U., Janko K., and Choleva L. (2018), «All-male hybrids of a tetrapod Pelophylax esculentus share its origin and genetics of maintenance», Biol. Sex Diff., 9, 13.

Drohvalenko M. and Fedorova A. (2022), «The first evidence of triploidy among Pelophylax esculentus (Linnaeus, 1758) (Anura: Ranidae) in the Chornobyl Exclusion Zone», Bonn Zool. Bull., 71(2), 105 – 108.

Dufresnes C., Denoël M., Di Santo L., and Dubey S. (2017), «Multiple uprising invasions of Pelophylax water frogs, potentially inducing a new hybridogenetic complex», Sci. Rep., 7, 6506.

Dufresnes C., Leuenberger J., Amrhein V., Bühler C., Thiébaud J., Bohnenstengel T., and Dubey S. (2018), «Invasion genetics of marsh frogs (Pelophylax ridibundus sensu lato) in Switzerland», Biol. J. Linn. Soc., 123, 402 – 410.

Ermakov O. A., Zaks M. M., and Titov S. V. (2013), «Diagnostics and distribution of «western» and «eastern» forms of the marsh frog Pelophylax ridibundus s. l. in the Penza Province (based on data of the mitochondrial cytochrome oxidase gene)», Vestn. Tambov. Gos. Univ., 18, 2999 – 3002 [in Russian].

Ermakov O. A., Fayzulin A. I., Zaks M. M., Kaybeleva E. I., and Zaripova F. F. (2014), «Distribution of «western» and «eastern» forms of marsh frog Pelophylax ridibundus s. l. in the Samara and Saratov regions (on data of analysis of mtDNA and nDNA)», Izv. Samar. NTs RAN, 16, 409 – 412 [in Russian].

Ermakov O., Ivanov A., Titov S., Svinin A., and Litvinchuk S. N. (2019), «New multiplex PCR method for identification of East European green frog species and their hybrids», Russ. J. Herpetol., 26(6), 367 – 370.

Fayzulin A. I., Zamaletdinov R. I., Litvinchuk S. N., Rosanov J. M., Borkin L. J., Ermakov O. A., Ruchin A. B., Lada G. A., Svinin A. O., Bashinsky I. V., and Chikhlyaev I. V. (2018), «Species composition and distributional peculiarities of green frogs (Pelophylax esculentus complex) in protected areas of the Middle Volga region (Russia)», Nat. Conserv. Res.., 3(Suppl. 1), 1 – 16.

Filipenko S. I., Bogatyi D. P., Ignat’ev I. I., and Serbinova L. P. (2015), «Hydrofauna of ‘Kolpak’ and ‘Dikul’’ points», in: S. I. Filipenko (ed.), Readings in Memory of Associate Professor and Candidate of Biological Sciences L. L. Popa, Tiraspol’, pp. 166 – 173 [in Russian].

Garner T. W. J., Gautschi B., Röthlisberger S., and Reyer H.-U. (2000), «A set of CA repeat microsatellite markers derived from the pool frog, Rana lessonae», Mol. Ecol., 9, 2173 – 2175.

Hemmer H. (1979), «Contribution to diagnostic problems and selection within the Rana esculenta complex», Mitt. Zool. Mus. Berlin, 55, 125 – 129.

Holsbeek G., Mergeay J., Hotz H., Plötner J., Volckaert F. A. M., and De Meester L. (2008), «A cryptic invasion within an invasion and widespread introgression in the European water frog complex: consequences of uncontrolled commercial trade and weak international legislation», Mol. Ecol., 17, 5023 – 5035.

Ivanov A. Yu. (2019), Molecular-genetic and Ecological Peculiarities of Distribution of Cryptic Forms of the Marsh Frog in Eastern Part of Range. Candidate’s Thesis, Penza, Penza State University [in Russian].

Ivanov A. Yu., Korzikov V. A., Alekseev S. K., and Ermakov O. A. (2015), «Molecular genetic characterisation of marsh frogs Pelophylax ridibundus s. l. from the Upper Pooche», in: F. I. Vasilevich, V. V. Spitsin, and S. V. Popov (eds.), Modern Problems of Zoology, Ecology and Conservancy, Moscow, pp. 228 – 232 [in Russian].

Ivanov A. Yu., Ruchin A. B., Fayzulin A. I., Chikhlyaev I. V., Litvinchuk S. N., Kirillov A. A., Svinin A. O., and Ermakov O. A. (2019), «The first record of natural transfer of mitochondrial DNA from Pelophylax cf. bedriagae into P. lessonae (Amphibia, Anura)», Nat. Conserv. Res., 4(2), 125 – 128.

Korshunov A. V. (2010), Ecological Pecularities of Distribution of the Pelophylax esculentus Complex in Biotopes of the Upper Part of the Severskiy Donets River Drainage. Candidate’s Thesis, Kharkov State University, Kharkov. [in Russian].

Krage S., Schreiber R., John S., Plötner M., and Plötner J. (2022), «Morphologisch-morphometrische und genetische Untersuchungen an Wasserfröschen (Pelophylax spp.) im Müritz-Nationalpark (Mecklenburg-Vorpommern) unter besonderer Berücksichtigung des Kleinen Wasserfroschs (Pelophylax lessonae)», Zeitschr. Feldherpetol., 29, 184 – 208.

Kulikova E. A., Axenova E. A., Korzun E. V., and Koloskov M. N. (2013), «The distribution of water frogs (Pelophylax esculentus complex) in Belarus», in: N. B. Ananjeva, E. V. Syromyatnikova, and I. V. Doronin (eds.), Modern Herpetology: Problems and Ways of their Solutions, St. Petersburg, pp. 101 – 104 [in Russian].

Kulikova E. A., Korzun E. V., Koloskov M. N., Litvinchuk S. N., Rosanov Y. M., Axenova E. A., and Chmielewska M. (2015), «Water frogs (Pelophylax esculentus complex) distribution in Belarus by using PCR-RFLP-based and DNA flow cytometry methods», in: B. Borczyk, M. Ogielska, K. Kolenda, and T. Skawiñski (eds.), Programme & Abstracts XVIII European Congress of Herpetology, Wroclaw, p. 147.

Lada G. A., Borkin L. J., Litvinchuk S. N., and Rosanov J. M. (2011), «Types of population systems of green frogs (Rana esculenta complex) in the territory of the Russian Plain», in: N. B. Ananjeva (ed.), Problems of Herpetology, St. Petersburg, pp. 142 – 148 [in Russian].

Litvinchuk S. N. (2018), «Testicular anomalies in the hybridogenetic frog Pelophylax esculentus (Amphibia: Anura: Ranidae)», in: The Second Int. Conf. «Amphibians and Reptiles Anomalies and Pathology: Methodology, Evolutionary Significance, Monitoring and Environmental Health», KnE Life Science, pp. 92 – 96.

Litvinchuk S. N., Borkin L. J., Litvinchuk Y. S., and Rosanov J. M. (2015), «Distribution and population systems of green frogs (Pelophylax esculentus complex) in Kaliningrad Oblast’, Russia (Baltic Sea Region)», Russ. J. Herpetol., 22(3), 188 – 196.

Litvinchuk S. N., Ivanov A. Yu., Lukonina S. A., and Ermakov O. A. (2020), «A record of alien Pelophylax species and widespread mitochondrial DNA transfer in Kaliningradskaya Oblast’ (the Baltic coast, Russia)», BioInvasions Rec., 9(3), 599 – 617.

Lukonina S. A., Ivanov A. Yu., Litvinchuk S. N., Svinin A. O., Fayzulin A. I., and Ermakov O. A. (2019), «The eastern boundary of distributional range of Pelophylax kurtmuelleri haplotypes on the Russian Plain», in: I. V. Doronin (ed.), Modern Herpetology: Problems and Ways of their Solutions, St. Petersburg, Zoological Institute, RAS, p. 58 [in Russian].

Mikulíček P. and Kotlík P. (2001), «Two water frog populations from western Slovakia consisting of diploid females and diploid males of the hybridogenetic hybrid Rana esculenta (Anura, Ranidae)», Mitt. Mus. Naturk. Berlin Zool. Reihe, 77, 59 – 64.

Miura I., Vershinin V., Vershinina S., Lebedinskii A., Trofimov A., Sitnikov I., and Ito M. (2021), «Hybridogenesis in the water frogs from Western Russian Territory: intrapopulation variation in genome elimination», Genes, 12, 244.

Milto K. D., Barabanov A. V., Borkin L. J., Rosanov J. M., and Litvinchuk S. N. (2022), «Distribution and population systems of water frogs (the Pelophylax esculentus complex) in northwestern Russia», Russ. J. Herpetol., 29(5), 298 – 316.

Plötner J. (2005), Die westpaläarktischen Wasserfrosche, Laurenti-Verlag, Bielefeld.

Reminnyi V. Y. and Matviychuk O. A. (2018), Nature of the Vinnitsa Region. Amphibians and Reptiles, Vinnits’ka oblastna drukarnya, Vinnitsa [in Ukrainian].

Ruchin A. B., Borkin L. J., Lada G. A., Litvinchuk S. N., Rosanov Yu. M., and Ryzhov M. K. (2005), «Morphological variation, genome size and population systems of the green frogs (Rana esculenta complex) of Mordovia», Bull. MOIP Biol., 110(2), 3 – 10 [in Russian].

Rybacki M. and Berger L. (2001), «Types of water frog populations (Rana esculenta complex) in Poland», Mitt. Mus. Naturk. Berlin Zool. Reihe, 77, 51 – 57.

Svinin A. O., Ivanov A. Yu., Zaks M. M., Litvinchuk S. N., Borkin L. J., Rosanov J. M., and Ermakov O. A. (2016 [2015]), «Distribution of the «eastern» and «western» forms of the marsh frog, Pelophylax ridibundus, and their participation in the origin of hemiclonal hybrids, P. esculentus in Mari El Republic», Curr. Stud. Herpetol., 15(3/4), 120 – 129 [in Russian].

Svinin A. O., Dedukh D. V., Borkin L. J., Ermakov O. A., Ivanov A. Yu., Litvinchuk J. S., Zamaletdinov R. I., Mikhaylova R. I., Trubyanov A. B., Skorinov D. V., Rosanov J. M., and Litvinchuk S. N. (2021), «Genetic structure, morphological variation, and gametogenic peculiarities in water frogs (Pelophylax) from northeastern European Russia», J. Zool. Syst. Evol. Res., 59(3), 646 – 662.

Tofan V. E. (1966), Fauna of Amphibians and Reptiles of Moldavia. Candidate’s Thesis, Leningr. Gos. Univ., Leningrad [in Russian].

Tofan V. E. (1967), «Ecology and intraspecific variation in green frogs of Moldavia», Byull. AN Mold. SSR, 1, 32 – 40 [in Russian].

Tuanmu M.-N. and Jetz W. (2014), «A global 1-km consensus land-cover product for biodiversity and ecosystem modeling», Global Ecol. Biogeogr., 23(9), 1031 – 1045.

Tunner H. G. (1974), «Die klonale Struktur einer Wasserfroschpopulation», Zeitschr. Zool. Syst. Evol., 12, 309 – 314.

Tunner H. G. and Heppich-Tunner S. (1992), «A new population system of water frogs discovered in Hungary», in: Z. Korsós and I. Kiss (eds.), Proc. of the 6th Ord. Gen. Meeting of the Soc. Eur. Herpetol., Budapest, pp. 453 – 460.

Ualiyeva D., Ermakov O. A., Litvinchuk S. N., Guo X., Ivanov A. Yu., Xu R., Li J., Xu F., Arifulova I. I., Kaptyonkina A. G., Khromov V. A., Krainyuk V. N., Sarzhanov F., and Dujsebayeva T. N. (2022), «Diversity, phylogenetic relationships and distribution of marsh frogs (the Pelophylax ridibundus complex) from Kazakhstan and Northwest China», Diversity, 14, 869.

Vinogradov A. E., Rosanov J. M., Caune I. A., and Borkin L. J. (1988), «Elimination of one parental genome prior premeiotic DNA synthesis in the hybridogenic hybrid Rana esculenta», Tsitologiya, 30, 691 – 698 [in Russian].

Vinogradov A. E., Borkin L. J., Günther R., and Rosanov J. M. (1990), «Genome elimination in diploid and triploid Rana esculenta males: cytological evidence from DNA flow cytometry», Genome, 33(5), 619 – 627.

Vinogradov A. E., Borkin L. J., Günther R., and Rosanov J. M. (1991), «Two germ cell lineages with genomes of different species in one and the same animal», Hereditas, 114(3), 245 – 251.

Zubkov N. I., Buchuchanu L. S., and Tsurkanu V. F. (1999), «Ornithological and herpetological complexes of ‘Yagorlyk’ Nature Reserve», in: Biodiversity Conservation of the Dniester River Basin, BIOTICA Ecological Society, Chisinau, pp. 76 – 78 [in Russian].




DOI: https://doi.org/10.30906/1026-2296-2023-30-2-88-100

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