Skip to main content

Evolutionary Potential of the Hybrid Form Pelophylax esculentus-ridibundus (Amphibia, Ranidae) within Dnieper and Desna Drainages: Its Loss Caused by the Hemiclonal Inheritance and the Compensatory Role of Parental Genomes’ Recombination

Abstract

The hemiclonal structure of the hybrid form Pelophylax esculentus-ridibundus (Amphibia: Ranidae) within the Dnieper and Desna rivers’ basins was analyzed. The presence of polyclonality in almost all populations was demonstrated. The monoclonality of the studied hybrid form was revealed in only 2 of 17 populations studied. Wide fluctuations in the level of genetic variability within P. esculentus-ridibundus in the study area were shown. The decrease in the genetic variation level was caused by the loss of rare hemiclones. A specific feature of P. esculentus-ridibundus, detected in the studied populations in the Dnieper and Desna basins, is the recombination of parental genomes. This leads to the emergence of new hemiclones and increases the genetic variation level of the inherited genome within this hybrid form.

This is a preview of subscription content, access via your institution.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

REFERENCES

  1. Arnold, M.L., Natural hybridization as an evolutionary process, Annu. Rev. Ecol. Syst., 2003. https://doi.org/10.1146/annurev.es.23.110192.001321

  2. Bashir, T., Chandra Mishra, R., Hasan, M.M., Mohanta, T.K., and Bae, H., Effect of hybridization on somatic mutations and genomic rearrangements in plants, Int. J. Mol. Sci., 2018. https://doi.org/10.3390/ijms19123758

  3. Berger, L., Uzzell, T., and Hotz, H., Sex determination and sex ratios in western Palearctic water frogs: XX and XY female hybrids in the Pannonian Basin?, Proc. Acad. Nat. Sci. Philadelphia, 1988. https://www. jstor.org/ stable/4064926

  4. Bi, K. and Bogart, J., Identification of intergenomic recombination in unisexual salamanders of the genus Ambystoma by genomic in situ hybridization (GISH), Cytogenet. Genome Res., 2006. https://doi.org/10.1159/000089885

  5. Čavlović, K., Buj, I., Karaica, D., Jelić, D., and Choleva, L., Composition and age structure of the Pelophylax esculentus complex (Anura; Ranidae) population in inland Croatia, Salamandra, 2018, vol. 54, pp. 11–20.

    Google Scholar 

  6. Christiansen, D.G. and Reyer, H.U., From clonal to sexual hybrids: genetic recombination via triploids in all-hybrid populations of water frogs, Evolution, 2009. https://doi.org/10.1111/j.1558-5646.2009.00673.x

  7. Cunha, C., Doadrio, I., Abrantes, J., and Coelho, M.M., The evolutionary history of the allopolyploid Squalius alburnoides (Cyprinidae) complex in the northern Iberian Peninsula, Heredity, 2011. https://doi.org/10.1038/hdy.2010.70

  8. Doležálková, M., Sember, A., Marec, F., Ráb, P., Plötner, J., and Choleva, L., Is premeiotic genome elimination an exclusive mechanism for hemiclonal reproduction in hybrid males of the genus Pelophylax?, BMC Genet., 2016. https://doi.org/10.1186/s12863-016-0408-z

  9. Doležalkova-Kaštánková, M., Pruvost, N.B.M., Plötner J., Reyer, H.U., Janko, K., and Choleva, L., All-male hybrids of a tetrapod Pelophylax esculentus share its origin and genetics of maintenance, Biol. Sex Differ., 2018. https://doi.org/10.1186/s13293-018-0172-z

  10. Dorken, M.E. and Eckert, C.G., Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae), J. Ecol., 2001. https://doi.org/10.1046/j.1365-2745.2001.00558.x

  11. Dufresnes, C., Leuenberger, J., Amrhein, V., Bühler, C., Thiébaud, J., Bohnenstengel, T., and Dubey, S., Invasion genetics of marsh frogs (Pelophylax ridibundus sensu lato) in Switzerland, Biol. J. Linn. Soc., 2018. https://doi.org/10.1093/biolinnean/blx140

  12. Dukić, M., Berner, D., Haag, C.R., and Ebert, D., How clonal are clones? A quest for loss of heterozygosity during asexual reproduction in Daphnia magna, J. Evol. Biol., 2019. https://doi.org/10.1111/jeb.13443

  13. Dybdahl, M.F. and Lively, C.M., Diverse, endemic, and polyphyletic clones in mixed populations of a freshwater snail (Potamopyrgus antipodarum), J. Evol. Biol., 2002. https://doi.org/10.1046/j.1420-9101.1995.8030385.x

  14. Forsdyke, D.R., When acting as a reproductive barrier for sympatric speciation, hybrid sterility can only be primary, Biol. J. Linn. Soc., 2019. https://doi.org/10.1093/biolinnean/blz135

  15. Genovart, M., Natural hybridization and conservation, Biodiversity Conserv., 2009. https://doi.org/10.1007/s10531-008-9550-x

  16. Grant, P.R. and Grant, B.R., Hybridization increases population variation during adaptive radiation, Proc. Natl. Acad. Sci. U. S. A., 2019. https://doi.org/10.1073/pnas.1913534116

  17. Hofman, S., Pabijan, M., Dziewulska-Szwajkowska, D., and Szymura, J.M., Mitochondrial genome organization and divergence in hybridizing central European waterfrogs of the Pelophylax esculentus complex (Anura, Ranidae), Gene, 2012. https://doi.org/10.1016/j.gene.2011.08.004

  18. Hotz, H., Guex, G.D., Beerli, P., Semlitsch, R.D., and Pruvost, N.B.M., Hemiclone diversity in the hybridogenetic frog Rana esculenta outside the area of clone formation: the view from protein electrophoresis, J. Zool. Syst., 2008. https://doi.org/10.1111/j.1439-0469.2007.00430.x

  19. Hotz, H., Uzzell, T., and Berger, L., Linkage groups of protein-coding genes in Western Palearctic water frogs reveal extensive evolutionary conservation, Genetics, 1997. 147:255–270

    CAS  Article  Google Scholar 

  20. Jelesko, J.G., Harper, R., Furuya, M., and Gruissem, W., Rare germinal unequal crossing-over leading to recombinant gene formation and gene duplication in Arabidopsis thaliana, Proc. Natl. Acad. Sci. U. S. A., 1999. https://doi.org/10.1073/pnas.96.18.10302

  21. Kajtoch, L. and Lachowska-Cierlik, D., Genetic constitution of parthenogenetic form of Polydrusus inustus (Coleoptera: Curculionidae)—hints of hybrid origin and recombinations, Folia Biol. (Krakow), 2009. https://doi.org/10.3409/fb57_3-4.149-156

  22. Maheshwari, S. and Barbash, D.A., The genetics of hybrid incompatibilities, Annu. Rev. Genet., 2011. https://doi.org/10.1146/annurev-genet-110410-132514

  23. Mezhzherin, S.V. and Morozov-Leonov, S.Yu., Genetic instability upon hereditary transmission of variants of the Ldh-B locus in hybrid matings between Rana esculenta complex forms (Amphibia, Ranidae), Dokl. Akad. Nauk, 1994a, vol. 339, pp. 140–141.

    CAS  PubMed  Google Scholar 

  24. Mezhzherin, S.V. and Morozov-Leonov, S.Yu., Genetic defects arising upon hereditary transmission and genetic variation of the Ldh-B locus in hybrid populations of green frogs of the Rana esculenta complex (Amphibia, Ranidae), Izv. Akad. Nauk, 1994b, vol. 5, pp. 779–787.

    Google Scholar 

  25. Mezhzherin, S.V. and Morozov-Leonov, S.Yu., Gene diffusion in hybrid populations of green frogs Rana esculenta L., 1758 complex (Amphibia, Ranidae) from the Dnepr basin, Russ. J. Genet., 1997, vol. 33, pp. 358–364.

    CAS  Google Scholar 

  26. Mezhzherin, S.V. and Peskov, V.N., Biochemical variability and genetic differentiation of the marsh frog Rana ridibunda Pall. populations, Cytol. Genet., 1992, vol. 26, pp. 43–48.

    CAS  Google Scholar 

  27. Mikulíček, P., Kautman, M., Demović, B., and Janko, K., When a clonal genome finds its way back to a sexual species: evidence from ongoing but rare introgression in the hybridogenetic water frog complex, J. Evol. Biol., 2014. https://doi.org/10.1111/jeb.12332

  28. Mikulíček, P., Kautman, M., Kautman, J., and Pruvost, N.B.M., Mode of hybridogenesis and habitat preferences influence population composition of water frogs (Pelophylax esculentus complex, Anura: Ranidae) in a region of sympatric occurrence (western Slovakia), J. Zool. Syst., 2015. https://doi.org/10.1111/jzs.12083

  29. Morozov-Leonov, S.Yu., Hemiclone diversity in the hybrid form Pelophylax esculentus-ridibundus (Amphibia, Ranidae) from the Tisa River drainage, Cytol. Genet., 2017. https://doi.org/10.3103/S0095452717060093

  30. Morozov-Leonov, S.Yu., Hemiclone diversity in the hybrid form Pelophylax esculentus-ridibundus (Amphibia, Ranidae) from the Prypyat, Dnestr, and Southern Boug river basins, Cytol. Genet., 2019. https://doi.org/10.3103/S0095452719010092

  31. Morozov-Leonov, S.Ju., Mezhzherin, S.V., and Kurtyak, Th.Th., The genetic structure of the unisex hybrid Rana esculenta complex populations in the Transcarpathians lowland, Cytol. Genet., 2003, vol. 37, pp. 43–47.

    Google Scholar 

  32. Morozov-Leonov, S.Yu., Mezhzherin, S.V., Nekrasova, O.D., Shabanov, D.A., Korshunov, A.V., and Kurtyak, F.F., Inheritance of parental genomes by a hybrid form Rana “esculenta” (Amphibia, Ranidae), Russ. J. Genet., 2009. https://doi.org/10.1134/S1022795409040061

  33. Nei, M. and Roychoudhury, A.K., Sampling variances of heterozygosity and genetic distance, Genetics, 1974, vol. 76, pp. 379–390.

    CAS  Article  Google Scholar 

  34. Nürnberger, B., Lohse, K., Fijarczyk, A., Szymura, J.M., and Blaxter, M.L., Para-allopatry in hybridizing fire-bellied toads (Bombina bombina and B. variegata): inference from transcriptome-wide coalescence analyses, Evolution, 2016. https://doi.org/10.1111/evo.12978

  35. Parker, E.D., Ecological implications of clonal diversity in parthenogenetic morphospecies, Am. Zool., 1979. https://doi.org/10.1093/icb/19.3.753

  36. Plotner, J., Uzzell, T., Beerli, P., Spolsky, C., Ohst, T., Litvinchuk, S.N., Guex, G.D., Reyer, H.U., and Hotz, H., Widespread unidirectional transfer of mitochondrial DNA: a case in western Palaearctic water frogs, J. Evol. Biol., 2008. https://doi.org/10.1111/j.1420-9101.2008.01527.x

  37. Quattro, J.M., Avise, J.C., and Vrijenhoek, R.C., An ancient clonal lineage in the fish genus Poeciliopsis (Atheriniformes: Poeciliidae), Proc. Natl. Acad. Sci. U. S. A., 1992. https://doi.org/10.1073/pnas.89.1.348

  38. Sánchez-Montes, G., Wang, J., Arico, A.H., Vizmanos, J.L., and Martínez-Solano, I., Reliable effective number of breeders/adult census size ratios in seasonal-breeding species: opportunity for integrative demographic inferences based on capture–mark–recapture data and multilocus genotypes, Ecol. Evol., 2017. https://doi.org/10.1002/ece3.3387

  39. Scali, V., Tinti, F., Mantovani, B., and Marescalchi, O., Mate recognition and gamete cytology features allow hybrid species production and evolution in Bacillus stick insects, Ital. J. Zool., 1995. https://doi.org/10.1080/11250009509356052

  40. Shang, H. and Yan, Y., Natural hybridization and biodiversity conservation, Biodiversity Sci., 2017. https://doi.org/10.17520/biods.2017122

  41. Vorburger, C., Fixation of deleterious mutations in clonal lineages: evidence from hybridogenetic frogs, Evolution, 2001. https://doi.org/10.1111/j.0014-3820.2001.tb00745.x

  42. Vorburger, C. and Reyer, H.U., A genetic mechanism of species replacement in European waterfrogs?, Conserv. Genet., 2003, vol. 4, pp. 141–155. https://doi.org/10.1023/A:1023346824722

    CAS  Article  Google Scholar 

  43. Zalesna, A., Choleva, L., Ogielska, M., Rábová, M., Marec, F., and Ráb, P., Evidence for integrity of parental genomes in the diploid hybridogenetic water frog Pelophylax esculentus by genomic in situ hybridization, Cytogenet. Genome Res., 2011. https://doi.org/10.1159/000327716

Download references

ACKNOWLEDGMENTS

I am sincerely grateful to my colleagues—Doctor of Biological Sciences, Professor S.V. Mezhzherin, Ph.D., O.D. Nekrasova, Ph.D., L.I. Razvodovskaya, Ph.D., and О.В. Rostovskaya—for invaluable assistance in collecting primary material, its laboratory processing, interpretation of the obtained data and preparation of this article.

Funding

This study was performed was part of the implementation of a long-term research work plan of the Schmalhausen Institute of Zoology (National Academy of Sciences of Ukraine) “Evolutionary-Genetic Consequences of Anthropogenic Transformation of the Animal World” (no. ІІІ-38-16).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Yu. Morozov-Leonov.

Ethics declarations

Conflict of interests. The author declares that he has no conflict of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. We used lifelong analysis of animals. The source of protein was a fragment of the thumb of the hind limb.

Additional information

Translated by V. Mittova

About this article

Verify currency and authenticity via CrossMark

Cite this article

Morozov-Leonov, S.Y. Evolutionary Potential of the Hybrid Form Pelophylax esculentus-ridibundus (Amphibia, Ranidae) within Dnieper and Desna Drainages: Its Loss Caused by the Hemiclonal Inheritance and the Compensatory Role of Parental Genomes’ Recombination. Cytol. Genet. 55, 213–226 (2021). https://doi.org/10.3103/S0095452721030063

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452721030063

Keywords:

  • Pelophylax
  • hybrid form
  • hemiclonal diversity
  • hemiclonal inheritance
  • recombination of parental genomes