Цитологія і генетика 2021, том 55, № 3, 10-24
Cytology and Genetics 2021, том 55, № 3, 213–226, doi: https://www.doi.org/10.3103/S0095452721030063

Еволюційний потенціал гібридної форми
Pelophylax esculentus-ridibundus (Amphibia, Ranidae) у басейнах Дніпра та Десни: його втрати, спричинені напівклональним успадкуванням, та компенсаторна роль рекомбінації батьківських геномів

Морозов-Леонов С.Ю.

  • Інститут зоології ім. І.І. Шмальгаузена, Київ, 01601 Україна

Проаналізовано напівклональну структуру гібридної форми Pelophylax esculentus-ridibundus (Amphibia: Ranidae) у басейнах річок Дніпро та Десна. Продемонстровано наявність поліклональності майже у всіх популяціях. Моноклональність досліджуваної гібридної форми виявлена лише у 2 із 17 досліджених популяцій. Показано широкі коливання рівня генетичної мінливос-ті P. esculentus-ridibundus у досліджуваній зоні. Показано зниження рівня генетичних варіацій через втрату рідкісних напівклонів. Специфічною рисою P. esculentus-ridibundus, виявленою у досліджуваних популяціях в басейнах Дніпра та Десни, є рекомбінація батьківських геномів. Це призводить до появи нових напівклонів та підвищує рівень генетичної варіації успадкованого геному в межах цієї гібридної форми.

Ключові слова: Pelophylax, гібридна форма, напівкло-нальна різноманітність, напівклональне успадкування, рекомбінація батьківських геномів

Цитологія і генетика
2021, том 55, № 3, 10-24

Current Issue
Cytology and Genetics
2021, том 55, № 3, 213–226,
doi: 10.3103/S0095452721030063

Повний текст та додаткові матеріали

Цитована література

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.

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

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.

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.

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.

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.

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.

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.

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

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