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The gynogenetic reproduction of diploid and triploid hybrid spined loaches (Cobitis: Teleostei), and their ability to establish successful clonal lineages—on the evolution of polyploidy in asexual vertebrates

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Abstract

Polyploidisation is assumed to have played a significant role in the evolution of hybrid asexual lineages. The virtual absence of natural asexual systems in which more than a single ploidy level successfully establishes successful independent clonal lineages is generally explained by the strong effects of polyploidisation on fitness. Experimental crosses were made between diploid and triploid asexual Cobitis elongatoides × C. taenia hybrids (female) and both parental spined loach species (male). Genotyping of the progeny using allozymes and multilocus DNA fingerprinting, along with flow cytometric measurement of ploidy level, demonstrated the occurrence of gynogenetic reproduction in both female biotypes. The incorporation of the sperm genome occurred in some progeny, giving rise to a higher ploidy level, but the rate of polyploidisation differed significantly between the diploid and triploid females. These outcomes are consistent with the existence of developmental constraints on tetraploidy, which determine the rarity of tetraploids in natural populations. No cases of ploidy level reduction were observed. Since diploid and triploid hybrid populations occur where the lack of potential progenitor excludes the possibility of de novo origin, it is probable that both diploid and triploid females can establish successful clonal lineages. Spined loaches represent a unique example, among asexual vertebrates, where more than one ploidy level can establish persistent clonal lineages, which are reproductively independent of one another.

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References

  • Alves MJ, Coelho MM, Collares-Pereira MJ (2001) Evolution in action through hybridisation and polyploidy in an Iberian freshwater fish: a genetic review. Genetica 111:375–385

    Article  PubMed  CAS  Google Scholar 

  • Arai A, Mukaino M (1997) Clonal nature of gynogenetically reproduced progeny of triploid loach, Misgurnus anguilicaudatus. J Exp Zool 278:412–421

    Article  CAS  Google Scholar 

  • Avise JC, Quattro JM, Vrijenhoek RC (1992) Molecular clones within organismal clones. Evol Biol 26:225–246

    CAS  Google Scholar 

  • Beukeboom LW, Vrijenhoek RC (1998) Evolutionary genetics and ecology of sperm-dependent parthenogenesis. J Evol Biol 11:755–782

    Article  Google Scholar 

  • Bogart JP (1989) A mechanism for interspecific gene exchange via all-female salamander hybrids. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. Bulletin 466, New York State Museum, Albany, New York, pp 170–179

    Google Scholar 

  • Bohlen J (1999) Reproduction of spined loach, Cobitis taenia, (Cypriniformes; Cobitidae) under laboratory conditions. J Appl Ichthyol 15:49–53

    Article  Google Scholar 

  • Bohlen J, Ráb P (2001) Species and hybrid richness in spined loaches of the genus Cobitis L. (Teleostei: Cobitidae.), with a checklist of European forms and suggestions for their conservation. J Fish Biol 59(Suppl A):79–85

    Google Scholar 

  • Bohlen J, Ráb P, Šlechtová V, Rábová M, Ritterbusch D, Freyhof J (2002) Hybridogeneous biotypes in spined loaches (genus Cobitis) in Germany with implications for conservation. In: Collares-Pereira MJ, Coelho MM, Cowx IG (eds) Conservation of freshwater fishes: options for the future (chapter 28). Fishing News Books, Blackwell Science, Oxford, pp 311–321

    Google Scholar 

  • Boroń A (2003) Karotypes and cytogenetic diversity of the genus Cobitis (Pisces, Cobitidae) in Poland: a review. Cytogenetic evidence for a hybrid origin of some Cobitis triploids. Folia Biologica (Krakow) 51(Suppl):49–54

    Google Scholar 

  • Chevassus B, Guyomard R, Chourrout D, Quillet L (1983) Production of viable hybrids in salmonids by triploidisation. Genet Sel Evol 15:519–532

    Google Scholar 

  • Culling MA, Janko K, Côté IM, Hewitt G (2006) European colonisation of the spined loach Cobitis taenia from Ponto-Caspian Refugia based on mitochondrial DNA variation. Mol Ecol 15:173–190

    Article  PubMed  CAS  Google Scholar 

  • Goddard KA, Dawley RM, Dowling TE (1989) Origin and genetic relationships of diploid, triploid and diploid–triploid mosaic biotypes in the Phoxinus eos–neogaeus unisexual complex. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. Bulletin 466, New York State Museum, Albany, New York, pp 268–280

    Google Scholar 

  • Graf JD, Polls-Pelaz M (1989) Evolutionary genetics of the Rana esculenta hybrid complex. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. Bulletin 466, New York State Museum, Albany, New York, pp 289–302

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  PubMed  CAS  Google Scholar 

  • Janko K, Kotlik P, Ráb P (2003) Evolutionary history of asexual hybrid loaches (Cobitis: Teleostie) inferred from phylogenetic analysis of mitochondrial DNA variation. J Evol Biol 16:1280–1287

    Article  PubMed  CAS  Google Scholar 

  • Janko K, Ráb P, Culling MA, Kotlík P (2005) Ice age cloning—comparison of quaternary evolutionary histories of sexual and clonal forms of European loaches (Cobitis; Teleostei) using the analysis of mitochondrial DNA variation. Mol Ecol 14:2991–3004

    Article  PubMed  CAS  Google Scholar 

  • Kim IS, Lee EH (2000) Hybridisation experiment of diploid–triploid cobitid fishes, Cobitis sinensis–longicorpus complex (Pisces, Cobitidae). Folia Zool 49(Suppl 1):17–22

    CAS  Google Scholar 

  • Kondrashov AS (1997) Evolutionary genetics of life cycles. Annu Rev Ecol Syst 28:391–435

    Article  Google Scholar 

  • Kondrashow AS, Crow JF (1991) Haploidy or diploidy, which is better? Nature 351:314–315

    Article  Google Scholar 

  • Lampert KP, Lamatsch DK, Epplen JT, Schartl M (2005) Evidence for a monophyletic origin of triploid clones of the Amazon molly, Poecilia formosa. Evolution 59:881–889

    PubMed  CAS  Google Scholar 

  • Lynch M (1984) Destabilising hybridization, general purpose genotypes and geographic parthenogenesis. Quart Rev Biol 59:257–290

    Article  Google Scholar 

  • Moritz C, Brown WM, Densmore LD, Wright JW, Vyas D, Donnellan S, Adams M, Baverstock P (1989) Genetic diversity and the dynamics of hybrid parthenogenesis in Cnemidophorus (Teiidae) and Heteronotia (Gekkonidae). In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. Bulletin 466, New York State Museum, Albany, New York, pp 268–280

    Google Scholar 

  • Nanda I, Neitzel H, Sperling K, Studer R, Epplen JT (1988) Simple GACTA repeats characterize the X-chromosomal heterochromatin of Microtus agrestis, European field vole (Rodentia, cricetidae). Chromosoma 96:213–219

    Article  PubMed  CAS  Google Scholar 

  • Nanda I, Schartl M, Feichtinger W, Schlupp I, Parzefall J, Schmid M (1995) Chromosomal evidence for laboratory synthesis of a triploid hybrid between the gynogenetic teleost Poecilia formosa and its host species. J Fish Biol 47:619–623

    Google Scholar 

  • Otto FJ (1994) High resolution analysis of nuclear DNA employing the fluorochrome DAPI. In: Darzynkiewicz Z, Robinson JP, Crissman HA (eds) Flow cytometry, 2nd edn., Part A. Vol 41 of methods in cell biology. Academic Press, London, pp 211–217

    Google Scholar 

  • Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437

    Article  PubMed  CAS  Google Scholar 

  • Otto SP (2003) In polyploids, one plus one does not equals two. Trend Ecol Evol 18:431–433

    Article  Google Scholar 

  • Paquin CE, Adams J (1993) Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature 302:495–500

    Article  Google Scholar 

  • Prehn LM, Rasch EM (1969) Cytogenetic studies of Poecilia (Pisces). I. Chromosome numbers of naturally occurring poeciliid species and their hybrids from Eastern Mexico. Canad J Genet Cytol 11:880–895

    PubMed  CAS  Google Scholar 

  • Ráb P, Rábová M, Bohlen J, Lusk S (2000) Genetic differentiation of the two hybrid diploid–polyploid complexes of loaches, genus Cobitis (Cobitidae) involving C. taenia, C. elongatoides and C. spp. in the Czech Republic: karyotypes and cytogenetic diversity. Folia Zool 49(Suppl):55–66

    Google Scholar 

  • Rasch EM, Darnell RM, Kallman KD, Abramoff P (1965) Cytophotometric evidence for triploidy in hybrids of the gynogenetic fish, Poecilia formosa. J Exp Zool. 160:155–169

    Article  PubMed  CAS  Google Scholar 

  • Rasch EM, Balsano JS (1974) Biochemical and cytogenetic studies of Poecilia from eastern Mexico. II. Frequency, perpetuation, and probable origin of triploid genomes in females associated with Poecilia formosa. Reviste de biologia tropical 21:351–381

    Google Scholar 

  • Saat TV (1991) Reproduction of the diploid and polyploid Spinous Loach (Cobitis, Teleostei). Oocyte maturation and fertilization in the triploid form. Soviet J Develop Biol 22:332–338

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schultz RJ, Kallman KD (1968) Triploid hybrids between the all-female teleost Poecilia formosa and Poecilia sphenops. Nature 219:280–282

    Article  Google Scholar 

  • Schultz RJ (1969) Hybridisation, unisexuality and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates. Am Nat 103:605–619

    Article  Google Scholar 

  • Šlechtová V, Lusková V, Šlechta V, Lusk S, Halačka K, Bohlen J (2000) Genetic differentiation of two diploid–polyploid complexes of spined loach, genus Cobitis (Cobitidae), in the Czech Republic, involving C. taenia, C. elongatoides and C. spp.: allozyme interpopulation and interspecific differences. Folia Zool 49(Suppl):67–78

    Google Scholar 

  • Spolsky CM, Phyllips CA, Uzzell T (1992) Gynogenetic reproduction in hybrid mole salamanders (Genus Ambystoma). Evolution 46:1935–1944

    Article  Google Scholar 

  • Strommen CA, Rasch EM, Balsano JS (1975) Cytogenetic studies of Poecilia (Pisces) V. Cytophotometric evidence for the production of fertile offspring by triploids related to Poecilia formosa. J Fish Biol 7:667–676

    Article  Google Scholar 

  • Vasil’ev VP, Vasil’eva ED, Osinov AG (1990) On the problem of reticular speciation in vertebrates: Diploid–triploid–tetraploid complex in the genus Cobitis (Cobitidae). III. Origin of the triploid form. Voprossy Ichthiologii 30:543–550 (In Russian with a summary in English)

    Google Scholar 

  • Vasil’ev VP, Akimova NV, Emel’yanova NG, Pavlov DA, Vasil’eva ED. (2003) Reproductive capacities in the polyploid males of spined loaches from the unisexual–bisexual complex, occurred in the Moscow river. Folia Biologica-Krakow 51(Suppl S):67–73

    Google Scholar 

  • Vasil’eva ED, Vasil’ev VP, Osinov AG (1989) Evolution of diploid–triploid–tetraploid complex of fishes genus Cobitis. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. Bulletin 466, New York State Museum, Albany, New York, pp 153–169

    Google Scholar 

  • Vrijenhoek RC (1998) Clonal organisms and the benefits of sex. In: Carvalho GR (ed) Advances in molecular ecology. IOS Press, pp 151–172

  • Vrijenhoek RC, Dawley RM, Cole CJ, Bogart JP (1989) A list of the known unisexual vertebrates. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. Bulletin 466, New York State Museum, Albany, New York, pp 19–23

    Google Scholar 

Download references

Acknowledgements

We are deeply obliged to Jana Pivoňková and Vlastimil Šlechta for laboratory assistance, and to M. Stöck for his critical reading of the manuscript and for his useful comments. Three anonymous referees provided a useful criticism on the previous version of the manuscript. The research was supported by the Ministry of Education, Youth and Sport of the Czech Republic, MSM 126100001, Grant Agency of the Czech Republic No. GAČR 206/05/P586, and by the German Research Foundation in the SFB 567 ‘Mechanisms of interspecific interactions’ and the EU Marie Curie Research and Training Network ‘SexAsex’ (MCRTN-CT-2004-512492). The study was supported in part by USB RIFCH project No. MSM6007665809 (to M.F.). The Laboratory of Fish Genetics at Liběchov receives continuous support from the Academy of Sciences of the Czech Republic (IRP lIAPG No. AV0Z50450515). We also thank www.smartenglish.co.uk for linguistic advice in the preparation of this manuscript.

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  1. Dunja Lamatsch

    Present address: Freshwater Biology, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, 1000, Brussels, Belgium

Authors and Affiliations

  1. Laboratory of Fish Genetics, Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, Rumburská 89, 27721, Libechov, Czech Republic

    Karel Janko, Jörg Bohlen, Petr Ráb, Petr Kotlík & Věra Šlechtová

  2. Department of Physiological Chemistry I, University of Wuerzburg, Biozentrum, Am Hubland, 97074, Wuerzburg, Germany

    Dunja Lamatsch

  3. Joint Laboratory of Fish Genetics, Physiology and Reproduction of lnstitute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic and Research lnstitute of Fish Culture and Hydrobiology, University of South Bohemia České Budějovice, 389 25, Vodňany, Czech Republic

    Martin Flajšhans, Petr Ráb & Petr Kotlík

  4. Human genetics Ruhr-Universität, Universitätsstr. 150, 44801, Bochum, Germany

    Jörg T. Epplen

  5. Research lnstitute of Fish Culture and Hydrobiology, University of South Bohemia České Budějovice, 389 25, Vodňany, Czech Republic

    Martin Flajšhans

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  1. Karel Janko
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Correspondence to Karel Janko.

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Janko, K., Bohlen, J., Lamatsch, D. et al. The gynogenetic reproduction of diploid and triploid hybrid spined loaches (Cobitis: Teleostei), and their ability to establish successful clonal lineages—on the evolution of polyploidy in asexual vertebrates. Genetica 131, 185–194 (2007). https://doi.org/10.1007/s10709-006-9130-5

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