SPECIES AND HYBRID COMPOSITION AND GENETIC DIVERSITY OF WATER FROGS (PELOPHYLAX ESCULENTUS COMPLEX) IN WESTERN UKRAINIAN HEMICLONAL POPULATION SYSTEMS
DOI: http://dx.doi.org/10.30970/sbi.1703.726
Abstract
Background. Two species of water frogs, Pelophylax ridibundus and Pelophylax lessonae, and their hybrid, Pelophylax kl. esculentus, are widespread in Ukraine. The purpose of this study was to investigate the population structure of various types of hemiclonal population systems (HPS) of water frogs formed due to the coexistence of frogs in the same territory. In Ukraine, a hybridization centre with the spread of triploid individuals of hybrid nature has been identified. Triploid hybrids are an intriguing research subject due to the diverse hypotheses about their origin and role in HPS. Outside the hybridization centre in Kharkiv Region, triploids are not commonly found. In our study, we describe the initial findings of triploid specimens in Lviv Region and analyze the genetic structure of the HPS where such individuals were detected.
Methods. In total, 193 specimens of green frogs were collected between 2011 and 2015. Here we present population structure analysis which was conducted using two microsatellite loci, Rrid059A and RlCA1b5. A wide range of software programs were utilized for processing the genetic analysis data, including GenePop 4.7.5, Micro-Checker and NewHybrids 1.1.
Results. Three types of hemiclonal population systems were identified: R-E type in Perekalky and Lake Pisochne, L-E type in Lake Luky, and R-E-L type in Nyzhankovychi, Velykyi Lyubin, Zhovtantsi and Cholgyni. Additionally, population systems with hybrids of mixed ploidy (diploids and triploids) were found in Perekalky, Velykyi Lyubin and Zhovtantsi.
Conclusions. Genetic diversity analysis revealed variations in the number of alleles per population. P. ridibundus individuals exhibited higher genetic diversity compared to P. lessonae individuals, whereas hybrids showed intermediate genetic diversity. Further investigations of the localities where potential triploids were detected are necessary to assess the survival and reproductive potential of hybrid individuals and determine all types of hybrids and individuals of both marsh and pool frogs.
Keywords
water frogs, Rrid059A, RlCA1b5, NewHybrids, hemiclonal population systems (HPS)
Full Text:
PDFReferences
| Ambu, J., & Dufresnes, C. (2023). Buccal swabs for amphibian genomics. Amphibia-Reptilia, 44(2), 249-255. doi:10.1163/15685381-bja10130 Crossref ● Google Scholar | ||||
| ||||
| Anderson, E., & Thompson, E. (2002). A model-based method for identifying species hybrids using multilocus genetic data. Genetic, 160(3), 1217-1229. doi:10.1093/genetics/160.3.1217 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Berger, L. (1964). Is Rana esculenta lessonae Camerano a distinct species? Annales Zoologici, 22(13), 245-261. Google Scholar | ||||
| ||||
| Berger, L., & Berger, A. (1994). Persistence of all-hybrid water frog populations (Rana kl. esculenta) in northern German. Genetica Polonica, 35(1-2), 73-80. Google Scholar | ||||
| ||||
| Biriuk, O., Shabanov, D., Korshunov, O., Borkin, L., Lada, G., Pasynkova, R., Rosanov, J., & Litvinchuk, S. (2015). Gamete production patterns and mating systems in water frogs of the hybridogenetic Pelophylax esculentus complex in north-eastern Ukraine. Journal of Zoological Systematics and Evolutionary Research, 54(3), 215-225. doi:10.1111/jzs.12132 Crossref ● Google Scholar | ||||
| ||||
| Bohling, J., Adams, J., & Waits, L. (2013). Evaluating the ability of Bayesian clustering methods to detect hybridization and introgression using an empirical red wolf data set. Molecular Ecology, 22(1), 74-86. doi:10.1111/mec.12109 Crossref ● Google Scholar | ||||
| ||||
| Bondarieva, A., Bibik, Y., Samilo, S., & Shabanov, D. (2012). Erythrocytes cytogenetic characteristics of green frogs from Siversky Donets centre of Pelophylax esculentus complex diversity. The Journal of V. N. Karazin Kharkiv National University. Series "Biology", 15(1008), 116-123. (In Russian) Google Scholar | ||||
| ||||
| Christiansen, D. G. (2005). A microsatellite-based method for genotyping diploid and triploid water frogs of the Rana esculenta hybrid complex. Molecular Ecology Notes, 5(1), 190-193. doi:10.1111/j.1471-8286.2004.00869.x Crossref ● Google Scholar | ||||
| ||||
| Christiansen, D. G. (2009). Gamete types, sex determination and stable equilibria of all-hybrid populations of diploid and triploid edible frogs (Pelophylax esculentus). BMC Evolutionary Biology, 9(1), 135. doi:10.1186/1471-2148-9-135 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Cuevas, А., Patrelle, С., Ciavatti, F., Gendre, T., Sourrouille, P., Geniez, P., Doniol-Valcroze, P., & Crochet, P.-A. (2022). A new PCR-RFLP method for the identification of parental and hybridogenetic western European water frogs, including the Pelophylax perezi-grafi system. Salamandra, 58(3), 218-230. Google Scholar | ||||
| ||||
| Dedukh, D., Mazepa, G., Shabanov, D., Rosanov, J., Litvinchuk, S., Borkin, L., Saifitdinova, A., & Krasikova, A. (2013). Cytological maps of lampbrush chromosomes of European water frogs (Pelophylax esculentus complex) from the eastern Ukraine. BMC Genetics, 14(1), 26. doi:10.1186/1471-2156-14-26 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Dedukh, D., Litvinchuk, S., Rosanov, J., Mazepa, G., Saifitdinova, A., Shabanov, D., & Krasikova, A. (2015). Optional endoreplication and selective elimination of parental genomes during oogenesis in diploid and triploid hybrid European water frogs. PLoS One, 10(4), e0123304. doi:10.1371/journal.pone.0123304 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Dedukh, D., Litvinchuk, S., Rosanov, J., Shabanov, D., & Krasikova, A. (2017). Mutual maintenance of di-and triploid Pelophylax esculentus hybrids in R-E systems: results from artificial crossings experiments. BMC Evolutionary Biology, 17(1), 220. doi:10.1186/s12862-017-1063-3 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Delmotte, F., Leterme, N., & Simon, J. C. (2001). Microsatellite allele sizing: difference between automated capillary electrophoresis and manual technique. Biotechniques, 31(4), 810-814. Google Scholar | ||||
| ||||
| Doležálková, M., Sember, A., Marec, F., Ráb, P., Plötner, J., & Choleva, L. (2016). Is premeiotic genome elimination an exclusive mechanism for hemiclonal reproduction in hybrid males of the genus Pelophylax? BMC Genetics, 17(1), 100. doi:10.1186/s12863-016-0408-z Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Doležálková-Kaštánková, M., Pruvost, N., Plötner, J., Reyer, H. U., Janko, K., & Choleva, L. (2018). All-male hybrids of a tetrapod Pelophylax esculentus share its origin and genetics of maintenance. Biology of Sex Differences, 9(1), 13. doi:10.1186/s13293-018-0172-z Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Dufresnes, C., Denoël, M., Di Santo, L., & Dubey, S. (2017). Multiple uprising invasions of Pelophylax water frogs, potentially inducing a new hybridogenetic complex. Scientific Reports, 7(1), 6506. doi:10.1038/s41598-017-06655-5 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Dufresnes, C., Leuenberger, J., Amrhein, V., Bühler, C., Thiébaud, J., Bohnenstengel, T., & Dubey, S. (2018). Invasion genetics of marsh frogs (Pelophylax ridibundus sensu lato) in Switzerland. Biological Journal of the Linnean Society, 123(2), 402-410. doi:10.1093/biolinnean/blx140 Crossref ● Google Scholar | ||||
| ||||
| Falush, D., Stephens, M., & Pritchard, J. K. (2007). Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes, 7(4), 574-578. doi:10.1111/j.1471-8286.2007.01758.x Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Garner, T. W. J., Gautschi, B., Röthlisberger, S., & Reyer, H. U. (2000). A set of CA repeat microsatellite markers derived from the pool frog, Rana lessonae. Molecular Ecology, 9(12), 2173-2175. doi:10.1046/j.1365-294X.2000.105311.x Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Herczeg, D., Vörös, J., Christiansen, D. G., Benovics, M., & Mikulíček, P. (2017). Taxonomic composition and ploidy level among European water frogs (Anura: Ranidae: Pelophylax) in eastern Hungary. Journal of Zoological Systematics and Evolutionary Research, 55(2), 129-137. doi:10.1111/jzs.12158 Crossref ● Google Scholar | ||||
| ||||
| Hill, G. E. (2019). Mitonuclear ecology. New York, NY: Oxford University Press. doi:10.1093/oso/978098818250.001.0001 Crossref ● Google Scholar | ||||
| ||||
| Hofman, S., Pabijan, M., Dziewulska-Szwajkowska, D., & Szymura, J. M. (2012). Mitochondrial genome organization and divergence in hybridizing central European waterfrogs of the Pelophylax esculentus complex (Anura, Ranidae). Gene, 491(1), 71-80. doi:10.1016/j.gene.2011.08.004 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Hoffmann, A., Plötner, J., Pruvost, N. B. M., Christiansen, D. G., Röthlisberger, S., Choleva, L., Mikulíček, P., Cogălniceanu, D., Sas-Kovács, I., Shabanov, D., Morozov-Leonov, S., & Reyer, H.-U. (2015). Genetic diversity and distribution patterns of diploid and polyploid hybrid water frog populations (Pelophylax esculentus complex) across Europe. Molecular Ecology, 24(17), 4371-4391. doi:10.1111/mec.13325 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 65-70. Google Scholar | ||||
| ||||
| Holsbeek, G., & Jooris, R. (2010). Potential impact of genome exclusion by alien species in the hybridogenetic water frogs (Pelophylax esculentus complex). Biological Invasions, 12(1), 1-13. doi:10.1007/s10530-009-9427-2 Crossref ● Google Scholar | ||||
| ||||
| Hotz, H., & Uzzell, T. (1982). Biochemically detected sympatry of two water frog species: two different cases in the Adriatic Balkans (Amphibia, Ranidae). Proceedings of the Academy of Natural Sciences of Philadelphia, 134, 50-79. Google Scholar | ||||
| ||||
| Hotz, H., Uzzell, T., Guex, G. D., Alpers, D., Semlitsch, R. D., & Beerli, P. (2001). Microsatellites: a tool for evolutionary genetic studies of western Palearctic water frogs. Zoosystematics and Evolution, 77(1), 43-50. doi:10.1002/mmnz.20010770108 Crossref ● Google Scholar | ||||
| ||||
| Hyne, R., Wilson, S., & Byrne, M. (2009). Frogs as bioindicators of chemical usage and farm practices in an irrigated agricultural area. Final Report to Land & Water Australia. Google Scholar | ||||
| ||||
| Kaeuffer, R., Réale, D., Coltman, D. W., & Pontier, D. (2007). Detecting population structure using STRUCTURE software: effect of background linkage disequilibrium. Heredity, 99(4), 374-380. doi:10.1038/sj.hdy.6801010 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Kravchenko, M., Shabanov, D. (2008). Possible ways of transformation of population systems of Pelophylax esculentus complex (Ranidae, Anura, Amphibia). Proceeding of the Ukranian Herpetological Society, 1, 15-20. (In Russian) Google Scholar | ||||
| ||||
| Kryvoltsevych, A., Fedorova, A., Shabanov, D., & Pustovalova, E. (2022). Anomalies in marsh frogs (Pelophylax ridibundus) and hybrid waterfrogs (P. esculentus) (Anura: Ranidae) from two ponds in the Kharkiv region of Ukraine. Reptiles & Amphibians, 29(1), 204-209. doi:10.17161/randa.v29i1.16446 Crossref ● Google Scholar | ||||
| ||||
| Meleshko, O. V., Korshunov, O. V., & Shabanov, D. A. (2014). The study of three hemiclonal population systems Pelophylax esculentus complex from the Seversko-Donetskiy center of green frogs diversity. The Journal of V. N. Karazin Kharkiv National University. Series "Biology", 20(1100), 153-158. Google Scholar | ||||
| ||||
| Ogielska-Nowak, M. (1978). DNA content in erythrocyte nuclei of diploid and triploid green frog hybrid of Rana esculenta L. complex. Zoologica Poloniae, 27, 109-115. Google Scholar | ||||
| ||||
| Perez-Enriquez, R., Medina-Espinoza, J. A., Max-Aguilar, A., & Saucedo-Barrón, C. J. (2018). Genetic tracing of farmed shrimp (Decapoda: Penaeidae) in wild populations from a main aquaculture region in Mexico. Revista de Biología Tropical, 66(1), 381-393. doi:10.15517/rbt.v66i1.27112 Crossref ● Google Scholar | ||||
| ||||
| Pidancier, N., Miquel, C., & Miaud, C. (2003). Buccal swabs as a non-destructive tissue sampling method for DNA analysis in amphibians. Herpetological Journal, 13(4), 175-178. Google Scholar | ||||
| ||||
| Plötner, J. (2005). Die westpaläarktichen Wasserfrösche [West palearctic water frogs]. Bielefeld: Laurenti-Verlag. Google Scholar | ||||
| ||||
| Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945-959. doi:10.1093/genetics/155.2.945 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Pruvost, N. B., Hoffmann, A., & Reyer, H. U. (2013). Gamete production patterns, ploidy, and population genetics reveal evolutionary significant units in hybrid water frogs (Pelophylax esculentus). Ecology and Evolution, 3(9), 2933-2946. doi:10.1002/ece3.687 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Pruvost, N. B. M., Mikulíček, P., Choleva, L., & Reyer, H. U. (2015). Contrasting reproductive strategies of triploid hybrid males in vertebrate mating systems. Journal of Evolutionary Biology, 28(1), 189-204. doi:10.1111/jeb.12556 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Pysanets, Y. (2007). Zemnovodni Ukrainy [The amphibians of Ukraine]. Kyiv: Zoological Museum of the National Museum of Natural History of NAS of Ukraine. (In Ukrainian) Google Scholar | ||||
| ||||
| Quilodran, C. S., Montoya-Burgos, J. I., & Currat, M. (2015). Modelling interspecific hybridization with genome exclusion to identify conservation actions: the case of native and invasive Pelophylax waterfrogs. Evolutionary Applications, 8(2), 199-210. doi:10.1111/eva.12245 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Raymond, M., & Rousset, F. (1995a). Genepop (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86(3), 248-249. doi:10.1093/oxfordjournals.jhered.a111573 Crossref ● Google Scholar | ||||
| ||||
| Raymond, M., & Rousset, F. (1995b). An exact test for population differentiation. Evolution, 49(6) 1280-1283. doi:10.2307/2410454 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Reyer, H. U., Arioli-Jakob, C., & Arioli, M. (2015). Post-zygotic selection against parental genotypes during larval development maintains all-hybrid populations of the frog Pelophylax esculentus. BMC Evolutionary Biology, 15(1), 131. doi:10.1186/s12862-015-0404-3 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Rousset, F., & Leblois, R. (2007). Likelihood and approximate likelihood analyses of genetic structure in a linear habitat: performance and robustness to model misspecification. Molecular Biology and Evolution, 24(12), 2730-2745. doi:10.1093/molbev/msm206 Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Rousset, F. (2008). Genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8(1), 103-106. doi:10.1111/j.1471-8286.2007.01931.x Crossref ● PubMed ● Google Scholar | ||||
| ||||
| Rybacki, M., & Berger, L. (2001). Types of water frog populations (Rana esculenta complex) in Poland. Zoosystematics and Evolution, 77(1), 51-57. doi:10.1002/mmnz.20010770109 Crossref ● Google Scholar | ||||
| ||||
| Smouse, P. E., Banks, S. C., & Peakall, R. (2017). Converting quadratic entropy to diversity: both animals and alleles are diverse, but some are more diverse than others. PLoS One, 12(10), e0185499. doi:10.1371/journal.pone.0185499 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Stakh, V., Belokon, M., Khamar, I., Belokon, Yu., Reshetylo, O. (2014). Morphological and genetic polymorphism of green frogs (Pelophylax) in water bodies of western Ukraine. Visnyk of Lviv University. Biological series, 64, 241-249. (In Ukraine) Google Scholar | ||||
| ||||
| Stakh, V. O., Strus, I. M., & Khamar, I. S. (2018). Genetic diversity in population systems of green frogs (Pelophylax esculentus complex) in waterbodies of western Ukraine. Studia Biologica, 12(3-4), 17-26. doi:10.30970/sbi.1203.575 Crossref ● Google Scholar | ||||
| ||||
| Stöck, M., Dedukh, D., Reifová, R., Lamatsch, D. K., Starostová, Z., & Janko, K. (2021). Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the 'extended speciation continuum'. Philosophical Transactions of the Royal Society B: Biological Sciences, 376(1833), 20200103. doi:10.1098/rstb.2020.0103 Crossref ● PubMed ● PMC ● Google Scholar | ||||
| ||||
| Tunner, H., & Kárpáti, L. (1997). The water frogs (Rana esculenta complex) of the Neusiedlersee region (Austria, Hungary). Herpetozoa, 10, 139-148. Google Scholar | ||||
| ||||
| Uzzell, T., Günther, R., & Berger, L. (1976). Rana ridibunda and Rana esculenta: a leaky hybridogenetic system (Amphibia Salientia). Proceedings of the Academy of Natural Sciences of Philadelphia, 147-171. Google Scholar | ||||
| ||||
| Van Oosterhout, C., Hutchinson, W. F., Wills, D. P., & Shipley, P. (2004). Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4(3), 535-538. doi:10.1111/j.1471-8286.2004.00684.x Crossref ● Google Scholar | ||||
| ||||
| Yin, S., Wang, Y., & Nan, Z. (2018). Genetic diversity studies of alfalfa germplasm (Medicago sativa L. subsp. sativa) of United States origin using microsatellite analysis. Legume Research-An International Journal, 41(2), 202-207. doi:10.18805/LR-358 Crossref ● Google Scholar | ||||
| ||||
| Zeisset, I., Rowe, G., & Beebee, T. (2001). Polymerase chain reaction primers for microsatellite loci in the north European water frogs Rana ridibunda and R. lessonae. Molecular Ecology, 9(8), 1173-1174. doi:10.1046/j.1365-294x.2000.00954-2.x Crossref ● PubMed ● Google Scholar | ||||
Refbacks
- There are currently no refbacks.
Copyright (c) 2023 Vasylyna Strus, Iurii Strus, Ihor Khamar
This work is licensed under a Creative Commons Attribution 4.0 International License.