Natural polyploidy in amphibians

Authors

  • Spartak Litvinchuk Institute of Cytology, Russian Academy of Sciences, 4, Tikhoretskiy pr., Saint Petersburg, 194064, Russian Federation https://orcid.org/0000-0001-7447-6691
  • Lev Borkin Zoological Institute, Russian Academy of Sciences, 1, Universitetskaya nab., Saint Petersburg, 199164, Russian Federation
  • Dmitriy Skorinov Institute of Cytology, Russian Academy of Sciences, 4, Tikhoretskiy pr., Saint Petersburg, 194064, Russian Federation
  • Rosa Pasynkova Institute of Cytology, Russian Academy of Sciences, 4, Tikhoretskiy pr., Saint Petersburg, 194064, Russian Federation
  • Yuriy Rosanov Institute of Cytology, Russian Academy of Sciences, 4, Tikhoretskiy pr., Saint Petersburg, 194064, Russian Federation

DOI:

https://doi.org/10.21638/11701/spbu03.2016.314

Abstract

This article examines polyploidy in amphibians. 53 polyploid species from 15 genera and 10 families (only anurans) are currently recognized. They can be arranged in 4 groups with different ploidy levels: I (triploids), 4 species of the toad genus Bufotes, II (tetraploids), 33 species from 14 genera and 10 families, III (octoploids), 12 species from 3 genera and 3 families, and IV (dodeсaploids), 4 species of the genus Xenopus. Only one taxon above the species level totally consisting of polyploid (4n to 12n) species is known (the subgenus Xenopus). At least 10 diploid-polyploid species complexes were revealed among amphibians. In nature, triploid individuals can originate in the hybridization zone between di- and tetraploid species. Occasionally, some triploids occur within populations of diploid species. Also polyploids (3n to 5n) are common among diploid-polyploid hybridogenetic forms, which breed clonally (Ambystoma and Pelophylax). The concept of reticulate (hybridogenous) speciation involved the hybridization between species, clonal inheritance and polyploidy is supported by current data. Polyploid amphibian species are mainly distributed in southern regions (Africa, South America, and Australia). In fact, the Oriental realm lacks polyploid amphibians. Refs 39. Figs 1. Tables 2.

Keywords:

amphibians, hybridization, polyploidy, reticulate speciation

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References

McGrath C. L., Lynch M. Evolutionary significance of whole-genome duplication. Polyploidy and Genome Evolution. Berlin, Heidelberg: Springer-Verlag, 2012, pp. 1–20. https://doi.org/10.1007/978-3-642-31442-1_1

Evans B. J., Pyron R. A., Wiens J. J. Polyploidization and sex chromosome evolution in amphibians. Polyploidy and Genome Evolution. Berlin, Heidelberg, Springer-Verlag, 2012, pp. 385–410. https://doi.org/10.1007/978-3-642-31442-1_18

Morescalchi A., Odierna G., Rosati C. On the polyploidy in the family Sirenidae (Amphibia: Caudata). Studies in Herpetology. Prague, Charles Univ., 1986, pp. 165–170.

Sessions S. K. Evolutionary cytogenetics in salamanders. Chromosome Res., 2008, vol. 16, pp. 183–201. https://doi.org/10.1007/s10577-007-1205-3

Stöck M., Ustinova J., Lamatsch D. K., Schartl M., Perrin N., Moritz C. A vertebrate reproductive system involving three ploidy levels: hybrid origin of triploids in a contact zone of diploid and tetraploid Palearctic green toads (Bufo viridis subgroup). Evolution, 2009, vol. 64, pp. 944–959. https://doi.org/10.1111/j.1558-5646.2009.00876.x

Bogart J. P., Bi K. Genetic and genomic interactions of animals with different ploidy levels. Cytogen. Genome Res., 2013, vol. 140, pp. 117–136. https://doi.org/10.1159/000351593

Gruber S. L., Silva A. P. Z., Haddad C. F. B., Kasahara S. Cytogenetic analysis of Phyllomedusa distincta Lutz, 1950 (2n = 2x = 26), P. tetraploidea Pombal and Haddad, 1992 (2n = 4x = 52), and their natural triploid hybrids (2n = 3x = 39) (Anura, Hylidae, Phyllomedusinae). BMC Genetics, 2013, vol. 14, pp. 75. https://doi.org/10.1186/1471-2156-14-75

Bogart J. P., Bi K., Fu J., Noble D. W. A., Niedzwiecki J. Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes. Genome, 2007, vol. 50, pp. 119–136. https://doi.org/10.1139/G06-152

Bogart J. P., Bartoszek J., Noble D. W. A., Bi K. Sex in unisexual salamanders: discovery of a new sperm donor with ancient affinities. Heredity, 2009, vol. 103, pp. 483–493. https://doi.org/10.1038/hdy.2009.83

Bi K., Bogart J. P. Time and time again: unisexual salamanders (genus Ambystoma) are the oldest unisexual vertebrates. BMC Evol. Biol., 2010, vol. 10, pp. 238. https://doi.org/10.1186/1471-2148-10-238

Dedukh D., Litvinchuk S., Rosanov J., Mazepa G., Saifitdinova A., Shabanov D., Krasikova A. 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, p. e0123304. https://doi.org/10.1371/journal.pone.0123304

Borkin L. J., Garanin W. I., Tichenko N. D., Zaune I. A. Some results in the green frogs survey in the USSR. Mitt. Zool. Mus. Berlin, 1979, Bd. 55, H. 1, S. 153–170. https://doi.org/10.1002/mmnz.4830550115

Jakob C. Structure and Dynamics of Pure Hybridogenetic Water Frog Populations of Rana esculenta in Southern Sweden. PhD thesis. Zürich. Universität Zürich, 2007. 197 p.

Hermaniuk A., Pruvost N. B. M., Kierzkowski P., Ogielska M. Genetic and cytogenetic characteristics of pentaploidy in water frogs. Herpetologica, 2013, vol. 69, pp. 36–45. https://doi.org/10.1655/HERPETOLOGICA-D-12-00037

Schmeller D., Crivelli A., Veith M. Is triploidy indisputably determinable in hybridogenetic hybrids by planimetric analyses of erythrocytes? Mitt. Mus. Naturk. Berlin. Zool. Reihe, 2001, Bd. 77, H. 1, S. 71–77. https://doi.org/10.1002/mmnz.4850770112

Feder J. H. Natural hybridization and genetic divergence between the toads Bufo boreas and Bufo punctatus. Evolution, 1979, vol. 33, pp. 1089–1097. https://doi.org/10.1111/j.1558-5646.1979.tb04764.x

Green D. M., Delisle D. M. Allotriploidy in natural hybrid frogs, Rana chiricahuensis × R. pipiens, from Arizona: chromosomes and electrophoretic evidence. J. Herpetol., 1985, vol. 19, pp. 385–390. https://doi.org/10.2307/1564266

Sofianidou T. S. Electrophoretic studies of hybrids of water frogs (Rana epeirotica, R. balcanica) in the Ionian zone of Greece. Isr. J. Zool., 1996, vol. 42, pp. 149–157.

Borkin L. J., Darevskii I. S. Setchatoe (gibridogennoe) vidoobrazovanie u pozvonochnykh [Reticulate (hybridogenous) speciation in vertebrates]. Zhurnal obshchei biologii [J. Gener. Biol.], 1980, vol. 16, no. 4, pp. 485–507. (In Russian)

Lantz L. A., Callan H. G. Phenotypes and spermatogenesis of interspecific hybrids between Triturus cristatus and T. marmoratus. J. Genet., 1954, vol. 52, pp. 165–185. https://doi.org/10.1007/BF02981497

Blair W. F. Appendix G. Combinations of species of Bufo which produce diploid progeny and those species which have been found to produce only polyploid off spring. Evolution in the Genus Bufo. Austin and London, University of Texas Press, 1972, pp. 382–387.

Malone J. H., Fontenot B. E. Patterns of reproductive isolation in toads. PLoS ONE, 2008, vol. 3, no. 12, pp. e3900. https://doi.org/10.1371/journal.pone.0003900

Bogart J. P., Licht L. E. Reproduction and the origin of polyploids in hybrid salamanders of the genus Ambystoma. Can. J. Genet. Cytol., 1986, vol. 28, pp. 605–617. https://doi.org/10.1139/g86-089

Berger L. Some peculiar phenomena in European water frogs. Zool. Polon., 1994, vol. 39, no. 3–4, pp. 267–280.

Stöck M., Lamatsch D. K., Steinlein C., Epplen J. T., Grosse W.-R., Hock R., Klapperstück T., Lampert K. P., Scheer U., Schmid M., Schartl M. A bisexually reproducing all-triploid vertebrate. Nat. Genet., 2002, vol. 30, pp. 325–328. https://doi.org/10.1038/ng839

Guignard M., Büchi L., Gétaz M., Betto-Colliard C., Stöck M. Genome size rather than content might affect call properties in toads of three ploidy levels (Anura: Bufonidae: Bufo viridis subgroup). Biol. J. Linn. Soc., 2012, vol. 105, pp. 584–590. https://doi.org/10.1111/j.1095-8312.2011.01837.x

Litvinchuk S. N., Mazepa G. O., Pasynkova R. A., Saidov A., Satorov T., Chikin Y. A., Shabanov D. A., Crottini A., Borkin L. J., Rosanov J. M., Stöck M. Influence of environmental conditions on the distribution of Central Asian green toads with three ploidy levels. J. Zool. Syst. Evol. Res., 2011, vol. 49, pp. 233–239. https://doi.org/10.1111/j.1439-0469.2010.00612.x

Stöck M., Ustinova J., Betto-Colliard C., Schartl M., Moritz C., Perrin N. Simultaneous Mendelian and clonal genome transmission in a sexually reproducing, all-triploid vertebrate. Proc. Roy. Soc. London B, 2012, vol. 279, pp. 1293–1299. https://doi.org/10.1098/rspb.2011.1738

Litvinchuk S. N., Borkin L. J., Skorinov D. V., Mazepa G. A., Pasynkova R. A., Dedukh D. V., Krasikova A. V., Rozanov J. M. Neobychnoe triploidnoe vidoobrazovanie u zelenykh zhab kompleksa Bufo viridis Vysokogornoi Azii [Unusual triploid speciation in green toads Bufo viridis group in high-altitude Asia]. Voprosy gerpetologii [Problems of Herpetology]. Minsk, 2012, pp. 160–165. (In Russian)

Tandy M., Bogart J. P., Largen M. J., Feener D. J. Variation and evolution in Bufo kerinyagae Keith, B. regularis Reuss and B. asmarae Tandy et al. (Anura, Bufonidae). Monit. Zoo. Ital., 1985, Suppl., vol. 20, no. 1, pp. 211–267. https://doi.org/10.1080/03749444.1985.10736699

Vieira K. D. S., Silva A. P. Z., Arzabe C. Cranial morphology and karyotypic analysis of Ceratophrys joazeirensis (Anura: Ceratophryidae, Ceratophrynae): taxonomic considerations. Zootaxa, 2006, vol. 1320, pp. 57–68. https://doi.org/10.11646/zootaxa.1320.1.6

Bogart J. P., Tandy M. Polyploid amphibians: three more diploid-tetraploid cryptic species of frogs. Science, 1976, vol. 193, pp. 334–335. https://doi.org/10.1126/science.935871

Bogart J. P., Wasserman F. O. Diploid-polyploid cryptic species pairs: a possible clue to evolution by polyploidization in anuran amphibians. Cytogenetics, 1972, vol. 11, pp. 7–24. https://doi.org/10.1159/000130172

Valetti J. A., Salas N. E., Martino A. L. A new polyploid species of Pleurodema (Anura: Leiuperidae) from Sierra de Comechingones, Córdoba, Argentina and redescription of Pleurodema kriegi (Müller, 1926). Zootaxa, 2009, vol. 2073, pp. 1–21. https://doi.org/10.11646/zootaxa.2073.1.1

Martino A. L., Sinsch U. Speciation by polyploidy in Odontophrynus americanus. J. Zool., 2002, vol. 257, pp. 67–81. https://doi.org/10.1017/S0952836902000663

Evans B. J., Kelley D. B., Tinsley R. C., Melnick D. J., Cannatella D. C. A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Mol. Phyl. Evol., 2004, vol. 33, pp. 197–213. https://doi.org/10.1016/j.ympev.2004.04.018

Channing A., Bogart J. P. Description of a tetraploid Tomopterna (Anura: Ranidae) from South Africa. S. Afr. J. Zool., 1996, vol. 31, pp. 80–85. https://doi.org/10.1080/02541858.1996.11448397

Litvinchuk S. N., Rosanov J. M. The first case of natural spontaneous triploidy in the family Bombinatoridae. Amphibia-Reptilia, 2016, vol. 37, pp. 243–245. https://doi.org/10.1163/15685381-00003042

Litvinchuk S. N., Skorinov D. V., Rosanov J. M. Natural spontaneous autotriploidy in the genus Pelophylax (Anura: Ranidae). Russ. J. Herpetol., 2015, vol. 22, pp. 318–320.

Vestnik of Saint Petersburg University. Series 3. Biology

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Published

2016-09-26

How to Cite

Litvinchuk, S., Borkin, L., Skorinov, D., Pasynkova, R., & Rosanov, Y. (2016). Natural polyploidy in amphibians. Biological Communications, (3), 77–86. https://doi.org/10.21638/11701/spbu03.2016.314

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No. 3 (2016)

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Full communications

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Articles of Biological Communications are open access distributed under the terms of the License Agreement with Saint Petersburg State University, which permits to the authors unrestricted distribution and self-archiving free of charge.