Skip to main content
Log in

Methodological approaches for studying the european water frog Pelophylax esculentus complex

  • Reviews and Theoretical Articles
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. 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.

    Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  Google Scholar 

  4. 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.

    Google Scholar 

  5. 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.

    Google Scholar 

  6. 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

    Article  CAS  PubMed  Google Scholar 

  7. Schultz, R.J., Evolution and ecology of unisexual fishes, Evol. Biol., 1977, vol. 10, pp. 277–331.

    Google Scholar 

  8. 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.

    Google Scholar 

  9. Plötner, J., Die westpaläarktichen Wasserfrösche, Bielefeld: Laurenti, 2005.

    Google Scholar 

  10. 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.

    Google Scholar 

  11. 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

    Google Scholar 

  12. 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.

    Article  PubMed  Google Scholar 

  13. 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

    Article  CAS  PubMed  Google Scholar 

  14. 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

  15. Mallet, J., Hybrid speciation, Nature, 2007, vol. 446, pp. 279–283. doi 10.1038/nature05706

    Article  CAS  PubMed  Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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

    Article  Google Scholar 

  18. 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.

    Google Scholar 

  19. 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

    Article  Google Scholar 

  20. Tunner, H.G., Evidence for genomic imprinting in unisexual triploid hybrid frogs, Amphibia—Reptilia, 2000, vol. 21, pp. 135–141. doi 10.1163/156853800507327

    Google Scholar 

  21. 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.

    Article  Google Scholar 

  22. 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.

    Google Scholar 

  23. 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.

    Article  CAS  PubMed  Google Scholar 

  24. 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.

    Google Scholar 

  25. 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.

    Article  CAS  PubMed  Google Scholar 

  26. 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

    Article  Google Scholar 

  27. 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

    Article  CAS  PubMed  Google Scholar 

  28. 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

    Article  Google Scholar 

  29. 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.

    CAS  Google Scholar 

  30. 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.

    Google Scholar 

  31. 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

    Google Scholar 

  32. 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.

    Google Scholar 

  33. 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

    Google Scholar 

  34. 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

    Article  CAS  Google Scholar 

  35. 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

    Article  CAS  PubMed  Google Scholar 

  36. 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.

    Google Scholar 

  37. 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

    Article  CAS  PubMed  Google Scholar 

  38. 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

    Google Scholar 

  39. 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

  40. 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

    Article  CAS  PubMed  Google Scholar 

  41. 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

    Article  Google Scholar 

  42. 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

    Article  CAS  PubMed  Google Scholar 

  43. 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

    Article  CAS  PubMed  Google Scholar 

  44. 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

    Article  CAS  PubMed  Google Scholar 

  45. 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

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  PubMed  PubMed Central  Google Scholar 

  48. 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

    Article  Google Scholar 

  49. 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

    Article  CAS  PubMed  Google Scholar 

  50. 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.

    Google Scholar 

  51. 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

    Google Scholar 

  52. 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

    Article  CAS  Google Scholar 

  53. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. 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

    Article  PubMed  PubMed Central  Google Scholar 

  55. 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

    Article  CAS  Google Scholar 

  56. 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

    Article  Google Scholar 

  57. 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

    Article  CAS  PubMed  Google Scholar 

  58. Callan, H.G., Lampbrush Chromosomes, London: Springer-Verlag, 1986.

    Book  Google Scholar 

  59. Macgregor, H.C., Lampbrush chromosomes and gene utilization in meiotic prophase, Symp. Soc. Exp. Biol., 1984, vol. 38, pp. 333–347.

    CAS  PubMed  Google Scholar 

  60. Gaginskaya, E.R., The lampbrush chromosomes in the amphibian oocytes, Tsitologiya, 1989, vol. 31, pp. 1267–1291.

    Google Scholar 

  61. 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

    Article  CAS  PubMed  Google Scholar 

  62. 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

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. V. Krasikova.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S102279541708004X

Keywords

Navigation