Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

A bisexually reproducing all-triploid vertebrate

Abstract

Green toads are common in the Palaearctic region, where they have differentiated into several taxa1,2. The toads exist with variable amounts of ploidy, similar to other anuran species3 or reptiles4. In vertebrate biology, the very rare occurrence of triploidy is coupled with infertility or unisexuality, or requires the coexistence of individuals of different ploidy in a reproductive community. The reproduction of naturally occurring triploids has been reported to occur only through parthenogenesis, gynogenesis or hybridogenesis. The bisexual reproduction of pure triploids has been considered to be impossible because of the problem of equally distributing three chromosome sets in meiosis. Here we report geographically isolated populations of green toads (Bufo viridis complex) that are all-triploid and reproduce bisexually.

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

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: All-triploid, bisexually reproducing green toads (B. pseudoraddei baturae) from the Hunza Valley, Karakoram, Pakistan.
Figure 2: DNA content of testis cells in green toads of different ploidy.
Figure 3: NOR signals in triploid toads.
Figure 4: Diagram of the reproductive system in triploid Batura toads with two possible mechanisms for oogenesis.
Figure 5: Inheritance of polymorphic markers in the offspring of a triploid female.

Similar content being viewed by others

References

  1. Borkin, L.J. in Patterns of Distribution of Amphibians (ed. Duellman, W.E.) 329–420 (J. Hopkins Univ. Press, Baltimore, 1999).

    Google Scholar 

  2. Stöck, M., Günther, R. & Böhme, W. Progress towards a taxonomic revision of the Asian Bufo viridis group: current status of nominal taxa and unsolved problems. Zool. Abh. Mus. Tierkd. Dresden 51, 253–319 (2001).

    Google Scholar 

  3. Green, D.S. & Sessions, K. (eds) Amphibian Cytogenetics and Evolution (Harcourt Brace Jovanovich, San Diego, 1991).

    Google Scholar 

  4. Bickham, J.W., Hanks, B.G., Hale, D.W. & Martin, J.E. Ploidy diversity and the production of balanced gametes in male twist-necked turtles (Platemys platycephala). Copeia 1993, 723–727 (1993).

    Article  Google Scholar 

  5. Roth, P. & Ráb, P. in Proc. 4th Ord. Gen. Meeting Soc. Europ. Herpetol. (eds van Gelder, J.J., Strijbosch, H. & Bergers, P.J.M.) 335–338 (Nijmegen, 1987).

    Google Scholar 

  6. Stöck, M. Polyploidy and Speciation in the Bufo viridis Complex. Thesis, Martin-Luther-Univ. Halle-Wittenberg (2001).

    Google Scholar 

  7. Castellano, S., Giacoma, C., Dujsebayeva, T., Odierna, G. & Balletto, E. Morphometrical and acoustical comparison between diploid and tetraploid green toads. Biol. J. Linn. Soc. 63, 257–281 (1998).

    Article  Google Scholar 

  8. Mezhzherin, S.V. & Pisanets, E.M. Genetic structure and origin of the tetraploid toad Bufo danatensis Pisanets 1978 (Amphibia, Bufonidae) from Central Asia: description of biochemical polymorphism and comparison of heterozygosity levels in diploid and tetraploid species. Genetica 31, 43–53 (1995).

    CAS  Google Scholar 

  9. Pisanets, E.M. On the new species Bufo danatensis sp. n. from Turkmenistan. Doklady Akademii Nauk Ukrainskoi SSR B 3, 280–278 (1978).

    Google Scholar 

  10. Borkin, L.Y. et al. On the distribution of diploid, triploid and tetraploid green toads in south-eastern Kazakhstan. Russ. J. Herpetol. 8, 45–53 (2001).

    Google Scholar 

  11. Stöck, M., Schmid, M., Steinlein, C. & Grosse, W.-R. Mosaicism in somatic triploid specimens of the Bufo viridis complex in the Karakoram with examination of calls, morphology and taxonomic conclusions. Ital. J. Zool. 66, 215–232 (1999).

    Article  Google Scholar 

  12. Schartl, M. et al. On the stability of dispensable constituents of the eukaryotic genome: stability of coding sequences versus truly hypervariable sequences in a clonal vertebrate, the amazon molly Poecilia formosa. Proc. Natl Acad. Sci. USA 88, 8759–8763 (1991).

    Article  CAS  Google Scholar 

  13. Chen, H. & Leibenguth, F. Studies on multilocus fingerprints, RAPD markers and mitochondrial DNA of a gynogenetic fish (Carassius auratus gibelio). Biochem. Gen. 33, 297–306 (1995).

    Article  CAS  Google Scholar 

  14. Stöck, M. & Grosse, W.-R. Erythrocyte size and ploidy determination in green toads (Bufo viridis complex) from Middle Asia. Alytes (Paris) 15, 72–90 (1997).

    Google Scholar 

  15. Günther, R., Uzzell, T. & Berger, L. Inheritance patterns in triploid Rana “esculenta” (Amphibia, Salientia). Mitt. Zool. Mus. Berl. 55, 35–57 (1979).

    Google Scholar 

  16. Vinogradov, A.E., Borkin, L.J., Günther, R. & Rosanov, J.M. Genome elimination in diploid and triploid Rana esculenta males: cytological evidence from DNA flow cytometry. Genome 33, 619–627 (1990).

    Article  CAS  Google Scholar 

  17. Alves, M.J., Coelho, M.M. & Collares-Pereira, M.J. Diversity in the reproductive modes of females of the Rutilus alburnoides complex (Teleostei, Cyprinidae): a way to avoid the genetic constraints of uniparentalism. Mol. Biol. Evol. 15, 1233–1242 (1998).

    Article  CAS  Google Scholar 

  18. Carmona, J.A., Sanjur, O.I., Doadrio, I., Machordom, A. & Vrijenhoek, R.C. Hybridogenetic reproduction and maternal ancestry of polyploid Iberian fish: the Tropidophoxinellus alburnoides complex. Genetics 146, 983–993 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Ohtani, H. Mechanism of chromosome elimination in the hybridogenetic spermatogenesis of allotriploid males between Japanese and European water frogs. Chromosoma 102, 158–162 (1993).

    Article  CAS  Google Scholar 

  20. Sumida, M. & Nishioka, M. Reproductive capacity of allotriploids between Rana tsushimensis from Tsushima and Rana japonica from Ichinoseki and Hiroshima. Sci. Rep. Lab. Amph. Biol. Hiroshima Univ. 12, 133–175 (1993).

    Google Scholar 

  21. Uzzell, T. Meiotic mechanisms of naturally occurring unisexual vertebrates. Am. Nat. 104, 433–445 (1970).

    Article  Google Scholar 

  22. Beukeboom, L.W. & Vrijenhoek, R.C. Evolutionary genetics and ecology of sperm dependent parthenogenesis. J. Evol. Biol. 11, 755–782 (1998).

    Article  Google Scholar 

  23. Schmid, M. Chromosome banding in Amphibia. I. Constitutive heterochromatin and nucleolus organizer regions in Bufo and Hyla. Chromosoma 66, 361–388 (1978).

    Article  Google Scholar 

  24. Klapperstück, T. & Wohlrab, W. DNA image cytometry on sections as compared with image cytometry on smears and flow cytometry in melanoma. Cytometry 25, 82–89 (1996).

    Article  Google Scholar 

  25. Morgan, G.T., Macgregor, H.C. & Colman, A. Multiple ribosomal gene sites revealed by in situ hybridization of Xenopus rDNA to Triturus lampbrush chromosomes. Chromosoma 80, 309–330 (1980).

    Article  CAS  Google Scholar 

  26. Gall, J.G. & Wu, Z. Lampbrush chromosomes. Methods Cell Biol. 36, 149–166 (1991).

    Article  CAS  Google Scholar 

  27. Callan, H.G., Gall, J.G. & Berg, C.A. The lamp brush chromosomes of Xenopus laevis: preparation, identification, and distribution of 5S DNA sequences. Chromosoma 95, 236–250 (1987).

    Article  CAS  Google Scholar 

  28. Tikel, D. et al. Polymerase chain reaction primers for polymorphic microsatellite loci in the invasive toad species Bufo marinus. Mol. Ecol. 9, 1927–1929 (2000).

    Article  CAS  Google Scholar 

  29. Rowe, G., Beebee, T.J.C. & Burke, T. PCR primers for polymorphic microsatellite loci in the anuran amphibian Bufo calamita. Mol. Ecol. 6, 401–402 (1997).

    Article  CAS  Google Scholar 

  30. Scribner, K.T., Arntzen, J.W. & Burke, T. Comparative analysis of intra- and interpopulation genetic diversity in Bufo bufo, using allozyme, single locus microsatellite, minisatellites and multilocus minisatellites data. Mol. Biol. Evol. 11, 737–748 (1994).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank W. Böhme, L.J. Borkin, A. Dubois and R. Günther for references; R. Dressel and H. Veith for assistance during field work in Pakistan; A. Hamel for combinatory views; I. Haufe for statistical advice; E. Trautmann and M. Kuhne for help with histological preparations; D. Frynta for animals; G. Moritz for technical support and C. and H. Stöck for technical and financial help. The costs of publication have been defrayed by the 15th International Chromosome Conference. This work was supported in part by the Deutsche Forschungsgemeinschaft and a graduate fellowship of the country Saxony-Anhalt (Germany; to M.St.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manfred Schartl.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stöck, M., Lamatsch, D., Steinlein, C. et al. A bisexually reproducing all-triploid vertebrate. Nat Genet 30, 325–328 (2002). https://doi.org/10.1038/ng839

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng839

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing