Abstract
The European water frog (Pelophylax esculentus) complex represents a unique and adequate model system for the study of interspecific hybridization and the mechanisms enabling interspecific hybrids to overcome the reproductive barriers. The difficulties in the study of individuals from the P. esculentus complex are associated with high polymorphism of morphological characters in parental species and interspecific hybrids, as well as with the presence of polyploid hybrid forms. From the discovery of the phenomenon of interspecific hybridization and the demonstration of successful reproduction of interspecific hybrids, researchers constantly searched for the methods necessary for the most accurate identification of parental species and various hybrid forms. This review describes biochemical, cytogenetic, and molecular methods and approaches used to identify individuals from the European water frog complex, as well as to analyze the genomes transferred with the gametes of hybrids. The advantages and disadvantages of these approaches are discussed. The presented methods can be used for studying other hybrid complexes of fish, amphibians, and reptiles.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Berger, L., Morphology of the F1 generation of various crosses within Rana esculenta complex, Acta Biol. Cracov., Ser. Zool., 1968, vol. 13, no. 13, pp. 301–324.
Tunner, H.G., Demonstration of the hybrid origin of the common green frog Rana esculenta L., Naturwissenschaften, 1973, vol. 60, no. 10, pp. 481–482. doi 10.1007/BF00592872
Heppich, S., Hybridogenesis in Rana esculenta: C-band karyotypes of Rana ridibunda, Rana lessonae and Rana esculenta, Z. Zool. Syst. Evol., 1978, vol. 16, pp. 27–39. doi 10.1111/j.1439-0469.1978.tb00918.x
Koref-Santibacez, S., The karyotypes of Rana lessonae Camerano, Rana ridibunda Pallas and of the hybrid form Rana “esculenta” Linne (Anura), Mitt. Zool. Mus. Berlin, 1979, vol. 55, no. 1, pp. 115–124.
Uzzell, T., Berger, L., and Günther, R., Diploid and triploid progeny from a diploid female of Rana esculenta (Amphibia Salientia), P. Acad. Nat. Sci. Phila., 1975, vol. 127, no. 11, pp. 81–91.
Heppich, S., Tunner, H.G., and Greilhuber, J., Premeiotic chromosome doubling after genome elimination during spermatogenesis of the species hybrid Rana esculenta, Theor. Appl. Genet., 1982, vol. 61, pp. 101–104. doi 10.1007/BF00273874
Schultz, R.J., Evolution and ecology of unisexual fishes, Evol. Biol., 1977, vol. 10, pp. 277–331.
Graf, J.-D. and Pelaz, M.P., Evolutionary genetics of the Rana esculenta complex, in Evolution and Ecology of Unisexual Vertebrates, New York State Museum Bull. 166, New York, 1989, pp. 289–302.
Plötner, J., Die westpaläarktichen Wasserfrösche, Bielefeld: Laurenti, 2005.
Graf, J.-D. and Pelaz, M.P., Rana ridibunda and Rana esculenta: a leaky hybridogenetic system (Amphibia Salientia), P. Acad. Nat. Sci. Phila., 1977, vol. 128, no. 9, pp. 147–171.
Pruvost, N.B.M., Hoffmann, A., and Reyer, H.-U., Gamete production patterns, ploidy, and population genetics reveal evolutionary significant units in hybrid water frogs (Pelophylax esculentus), Ecol. Evol., 2013, pp. 2933–2946. doi 10.1002/ece3.687
Christiansen, D., Fog, K., Pedersen, B.V., and Boomsma, J.J., Reproduction and hybrid load in allhybrid populations of Rana esculenta water frogs in Denmark, Evolution, 2005, vol. 59, no. 6, pp. 1348–1361.
Christiansen, D. and Reyer, H.U., From clonal to sexual hybrids: genetic recombination via triploids in allhybrid populations of water frogs, Evolution, 2009, vol. 63, pp. 1754–1768. doi 10.1111/j.1558-5646. 2009.00673.x
Arioli, M., Jakob, C., and Reyer, H.-U., Genetic diversity in water frog hybrids (Pelophylax esculentus) varies with population structure and geographic location, Mol. Ecol., 2010, vol. 19, pp. 1814–1828. doi 10.1111/j.1365-294X.2010.04603.x
Mallet, J., Hybrid speciation, Nature, 2007, vol. 446, pp. 279–283. doi 10.1038/nature05706
Mable, B.K., Alexandrou, M.A., and Taylor, M.I., Genome duplications in amphibians and fish: an extended synthesis, J. Zool., 2011, vol. 284, pp. 151–182. doi 10.1111/j.1469-7998.2011.00829.x
Plötner, J., Becker, C., and Plötner, K., Morphometric and DNA investigations into European water frogs (Rana kl. esculenta synklepton (Anura, Ranidae)) from different population systems, J. Zool. Syst. Evol. Res., 1994, vol. 32, no. 3, pp. 193–210. doi 10.1111/j.1439-0469.1994.tb00482.x
Vorburger, C., Genomic imprinting or mutation and interclonal selection in triploid hybrid frogs? A comment on Tunner, Amphibia—Reptilia, 2001, vol. 22, pp. 263–265.
Kierzkowski, P., Pasko, L., Rybacki, M., et al., Genome dosage effect and hybrid morphology—the case of the hybridogenetic water frogs of the Pelophylax esculentus complex, Ann. Zool. Fenn., 2011, vol. 48, no. 1, pp. 56–66. doi 10.5735/086.048.0106
Tunner, H.G., Evidence for genomic imprinting in unisexual triploid hybrid frogs, Amphibia—Reptilia, 2000, vol. 21, pp. 135–141. doi 10.1163/156853800507327
Plötner, J., Günther, R., and Schade, R., Immunologische Untersuchungen zur Verwandtschaft zwischen den mitteleuropäischen Wasserfrpöschen des Rana kl. esculenta Synkleptons (Amphibia, Anura) und anderen Anuren-Taxa, Mitt. Zool. Mus. Berlin, 1988, vol. 64, no. 2, pp. 323–330.
Berger, L., Hotz, H., and Roguski, H., Diploid eggs of Rana esculenta with two Rana ridibunda genomes, P. Acad. Nat. Sci. Phila., 1986, vol. 138, no. 1, pp. 1–13.
Graf, J.-D., Karch, E., and Moreillon, M.-C., Biochemical variation in the Rana esculenta complex: a new hybrid form related to Rana perezi and Rana ridibunda, Experientia, 1977, vol. 33, pp. 1582–1584.
Tunner, H.G., The morphology and biology of triploid hybridogenetic Rana esculenta: does genome dosage exist?, in II International Symposium on Ecology and Genetics of European Water Frogs, Wroclaw, 1994, p. 505.
Graf, J.-D. and Muller, W.P., Experimental gynogenesis provides evidence of hybridogenetic reproduction in the Rana esculenta complex, Experientia, 1979, vol. 35, no. 12, pp. 1574–1576.
Uzzell, T., Hotz, H., and Berger, L., Genome exclusion in gametogenesis by an interspecific Rana hybrid: evidence from electrophoresis of individual oocytes, J. Exp. Zool., 1980, vol. 214, no. 3, pp. 251–259. doi 10.1002/jez.1402140303
Tunner, H.G. and Heppich, S., Premeiotic genome exclusion during oogenesis in the common edible frog, Rana esculenta, Naturwissenschaften, 1981, vol. 68, no. 4, pp. 207–208. doi 10.1007/BF01047207
Tunner, H.G. and Heppich-Tunner, S., Genome exclusion and two strategies of chromosome duplication in oogenesis of a hybrid frog, Naturwissenschaften, 1991, vol. 78, no. 1, pp. 32–34. doi 10.1007/BF01134041
Berger, L., Roguski, H., and Uzzell, T., Triploid F2 progeny of water frogs (Rana esculenta complex), Folia Biol. (Kraków), 1978, vol. 26, no. 3, pp. 135–152.
Ogielska-Nowak, M., DNA content in erythrocyte nuclei of diploid and triploid green frog hybrids of Rana esculenta L. complex, Zool. Pol., 1978, vol. 28, no. 1, pp. 109–115.
Ogielska, M., Kazana, K., and Kierzkowski, P., DNA content in erythrocyte nuclei of water frogs from a pure Rana esculenta population in Debki (Gdansk district, Poland), Mitt. Mus. Nat. Kd. Berl. Zool. Reihe, 2001, vol. 77, no. 1, pp. 65–70. doi 10.1002/mmnz.20010770111
Polls Pelaz, M.P. and Graf, J.-D., Erythrocyte size as an indicator of ploidy level in Rana kl. esculenta before and after the metamorphosis, Alytes, 1988, vol. 7, no. 2, pp. 53–61.
Schmeller, D.S., Crivelli, A., and Veith, M., Is triploid indisputably determinable in hybridogenetic hybrids by planimetric analyses of erythrocytes?, Mitt. Mus. Nat. Kd. Berl. Zool. Reihe, 2001, vol. 77, pp. 71–77. doi 10.1002/mmnz.20010770112
Ogielska, M., Kierzkowski, P., and Rybacki, M., DNA content and genome composition of diploid and triploid water frogs belonging to the Rana esculenta complex (Amphibia, Anura), Can. J. Zool., 2004, vol. 82, pp. 1894–1901. doi 10.1139/z04-188
Vinogradov, A.E., Borkin, L.J., Gunther, R., and Rosanov, J.M., Genome elimination in diploid and triploid Rana esculenta males: cytological evidence from DNA flow cytometry, Genome, 1990, vol. 33, pp. 619–627. doi 10.1139/g90-092
Borkin, L.J., Korshunov, A.V., Lada, G.A., et al., Mass occurrence of polyploid green frogs (Rana esculenta complex) in Eastern Ukraine, Russ. J. Herpetol., 2004, vol. 3, no. 11, pp. 194–213.
Bucci, S., Ragghianti, M., Mancino, G., et al., Lampbrush and mitotic chromosomes of the hemiclonally reproducing hybrid Rana esculenta and its parental species, J. Exp. Zool., 1990, vol. 255, no. 1, pp. 37–56. doi 10.1002/jez.1402550107
Dedukh, D., Mazepa, G., Shabanov, D., et al., Cytological maps of lampbrush chromosomes of European water frogs (Pelophylax esculentus complex) from the Eastern Ukraine, BMC Genet., 2013, vol. 04, pp. 14–26. doi 10.1186/1471-2156-14-26
Dedukh, D., Litvinchuk, S., Rosanov, J., et al., Optional endoreplication and selective elimination of parental genomes during oogenesis in diploid and triploid hybrid European water frogs, PLoS One, 2015, vol. 10, no. 4. doi 10.1371/journal.pone.0123304
Ragghianti, M., Guerrini, F., Bucci, S., et al., Molecular characterization of a centromeric satellite DNA in the hemiclonal hybrid frog Rana esculenta and its parental species, Chromosome Res., 1995, vol. 3, no. 8, pp. 497–506. doi 10.1007/BF00713965
Ragghianti, M., Bucci, S., Casola, C., et al., Molecular investigations in western Palearctic water frogs, Ital. J. Zool., Suppl., 2004, vol. 2, pp. 17–23. doi 10.1080/11250000409356601
Ragghianti, M., Bucci, S., Marracci, S., et al., Gametogenesis of intergroup hybrids of hemiclonal frogs, Genet. Res., 2007, vol. 89, no. 1, pp. 39–45. doi 10.1017/S0016672307008610
Lin, K.W. and Yan, J., Endings in the middle: current knowledge of interstitial telomeric sequences, Mutat. Res., 2008, vol. 658, pp. 95–110. doi 10.1016/j.mrrev.2007.08.006
Kato, A., Vega, J.M., Han, F., et al., Advances in plant chromosome identification and cytogenetic techniques, Curr. Opin. Plant Biol., 2005, vol. 8, pp. 148–154. doi 10.1016/j.pbi.2005.01.014
Markova, M. and Vyskot, B., New horizons of genomic in situ hybridization, Cytogenet. Genome Res., 2009, vol. 126, no. 4, pp. 368–375. doi 10.1159/000275796
Zalesna, A., Choleva, L., Ogielska, M., et al., Evidence for integrity of parental genomes in the diploid hybridogenetic water frog Pelophylax esculentus by genomic in situ hybridization, Cytogenet. Genome Res., 2011, vol. 134, pp. 206–212. doi 10.1159/000327716
Doležálková, M., Sember, A., Marec, F., et al., Is premeiotic genome elimination an exclusive mechanism for hemiclonal reproduction in hybrid males of the genus Pelophylax?, BMC Genet., 2016, vol. 17, p. 100. doi 10.1186/s12863-016-0408-z
Plötner, J., Köhler, F., Uzzell, T., et al., Evolution of serum albumin intron-1 is shaped by a 5' truncated non-long terminal repeat retrotransposon in western Palearctic water frogs (Neobatrachia), Mol. Phyl. Evol., 2009, vol. 53, pp. 784–791. doi 10.1016/j.ympev.2009.07.037
Hauswaldt, J.S., Höer, M., Ogielska, M., et al., A simplified molecular method for distinguishing among species and ploidy levels in European water frogs (Pelophylax), Mol. Ecol. Resour., 2012, vol. 12, pp. 797–805. doi 10.1111/j.1755-0998.2012.03160.x
Mayer, M., Hawlitschek, O., Zahn, A., and Glaw, F., Composition of twenty green frog populations (Pelophylax) across Bavaria, Germany, Salamandra, 2013, vol. 49, no. 1, pp. 31–44.
Hotz, H., Uzzell, Th., Guex, G.-D., et al., Microsatellites: a tool for evolutionary genetic studies of western Palearctic water frogs, Mitt. Mus. Nat. Kd. Berl. Zool. Reihe, 2001, vol. 77, pp. 43–50. doi 10.1002/mmnz.20010770108
Christiansen, D., A microsatellite-based method for genotyping diploid and triploid water frogs of the Rana esculenta hybrid complex, Mol. Ecol. Notes, 2005, vol. 5, no. 1, pp. 190–193. doi 10.1111/j.1471-8286.2004.00869.x
Spolsky, C. and Uzzell, T., Natural interspecies transfer of mitochondrial DNA in amphibians, Proc. Natl. Acad. Sci. U.S.A., 1984, vol. 81, no. 18, pp. 5802–5805.
Plötner, J., Uzzell, T., Beerli, P., et al., Widespread unidirectional transfer of mitochondrial DNA: a case in western Palearctic water frogs, J. Evol. Biol., 2008, vol. 21, no. 3, pp. 668–681. doi 10.1111/j.1420-9101.2008.01527.x
Patrelle, C., Ohst, T., Picard, D., et al., A new PCRRFLP-based method for an easier systematic affiliation of European water frogs, Mol. Ecol. Res., 2011, vol. 11, pp. 200–205. doi 10.1111/j.1755-0998.2010.02905.x
Schultz, J., Muller, T., Achtziger, M., et al., The internal transcribed spacer 2 database—a web server for (not only) low level phylogenetic analyses, Nucleic Acids Res., 2006, vol. 34, pp. 704–707. doi 10.1093/nar/gkl129
Vinogradov, A.E., Borkin, L.J., Gunther, R., and Rosanov, J.M., Two germ cell lineages with genomes of different species in one and the same animal, Hereditas, 1991, vol. 114, pp. 245–251. doi 10.1111/j.1601-5223.1991.tb00331.x
Callan, H.G., Lampbrush Chromosomes, London: Springer-Verlag, 1986.
Macgregor, H.C., Lampbrush chromosomes and gene utilization in meiotic prophase, Symp. Soc. Exp. Biol., 1984, vol. 38, pp. 333–347.
Gaginskaya, E.R., The lampbrush chromosomes in the amphibian oocytes, Tsitologiya, 1989, vol. 31, pp. 1267–1291.
Morgan, G.T., Lampbrush chromosomes and associated bodies: new insights into principles of nuclear structure and function, Chromosome Res., 2002, vol. 10, pp. 177–200. doi 10.1023/A:1015227020652
Gall, J.G., Wu, Z., Murphy, C., and Gao, H., Structure in the amphibian germinal vesicle, Exp. Cell Res., 2004, vol. 296, pp. 28–34. doi 10.1016/j.yexcr.2004.03.017
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © D.V. Dedukh, A.V. Krasikova, 2017, published in Genetika, 2017, Vol. 53, No. 8, pp. 885–894.
Rights and permissions
About this article
Cite this article
Dedukh, D.V., Krasikova, A.V. Methodological approaches for studying the european water frog Pelophylax esculentus complex. Russ J Genet 53, 843–850 (2017). https://doi.org/10.1134/S102279541708004X
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S102279541708004X