Skip to main content
SpringerLink
Log in

Non-motile tetraploid spermatozoa of Misgurnus loach hybrids

  • Original Article
  • Aquaculture
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

We have compared various properties of spermatozoa from the wild diploid male pond loach Misgurnus anguillicaudatus to those from the interspecific male hybrid of the cross between a female M. anguillicaudatus and a male mud loach M. mizolepis. Our results show that spermatozoa from this interspecific hybrid had poor motility, low viability, abnormal morphology, a larger volume of mitochondrial mass per cell and higher ATP content of spermatozoa with tetraploid DNA content, and they were present at a low concentration. The interspecific hybrid males produced spermatozoa with a larger head, with either no flagellum (36.4 %), one flagellum (46.7 %) or two flagella (16.9 %). These flagella were shorter than those of the normal wild-type male M. anguillicaudatus and often presented with abnormalities in microtubule structure. An abnormally shorter flagellum has difficulty in propelling tetraploid spermatozoa with an increased head size in normal progressive motility, although they had higher energy, as shown by their larger volume of mitochondrial mass and higher ATP content. These tetraploid spermatozoa are likely produced by the arrest of the regular meiotic division after chromosomal replication, followed by abnormal spermiogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Suzuki R, Fukuda Y (1973) Sexual maturity of F1 hybrids among salmonid fishes. Bull Freshw Fish Res Lab 23:57–74

    Google Scholar 

  2. Suzuki R (1974) Inter-crossing and back-crossing of F1 hybrids among salmonid fishes. Bull Freshw Fish Res Lab 24:11–31

    Google Scholar 

  3. Chevassus B (1983) Hybridization in fish. Aquaculture 17:113–128

    Article  Google Scholar 

  4. Senanan W, Kapuscinski AR, Na-Nakorn U, Miller LM (2004) Genetic impacts of hybrid catfish farming (Clarias macrocephalus x C. gariepinus) on native catfish populations in central Thailand. Aquaculture 235:157–184

    Article  CAS  Google Scholar 

  5. Pandian TJ (2011) Sex determination in fish. Science Publishers, Enfield/CRC Press, Boca Raton

    Book  Google Scholar 

  6. Johnson KR, Wright JE (1986) Female brown trout x Atlantic salmon hybrids produce gynogens and triploids when backcrossed to male Atlantic salmon. Aquaculture 57:345–358

    Article  Google Scholar 

  7. Dawley RM (1989) An introduction to unisexual vertebrates. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. New York State Museum, Albany, pp 1–18

    Google Scholar 

  8. Arai K, Fujimoto T (2013) Genomic constitution and atypical reproduction in polyploid and unisexual lineages of the Misgurnus loach, a teleost fish. Cytogenet Genome Res 140:226–240

    Article  PubMed  CAS  Google Scholar 

  9. Kimura-Kawaguchi M, Horita M, Abe S, Arai K, Kawata M, Munehara H (2014) Identification of hemiclonal reproduction in three species of Hexagrammos marine reef fishes. J Fish Biol 85:189–209

    Article  PubMed  CAS  Google Scholar 

  10. Alves MJ, Coelho MM, Prospero MI, Collares-Pereira MJ (1999) Production of fertile unreduced sperm by hybrid males of the Rutilus alburnoides complex (Teleostei, Cyprinidae): an alternative route to genome tetraploidization in unisexuals. Genetics 151:277–283

    PubMed  PubMed Central  CAS  Google Scholar 

  11. Cherfas NB, Gomelsky BI, Emelyanova OV, Recoubratsky AV (1994) Induced diploid gynogenesis and polyploidy in crucian carp, Carassius auratus gibelio (Bloch), x common carp, Cyprinus carpio L., hybrids. Aquac Res 25:943–954

    Article  Google Scholar 

  12. Liu S, Liu Y, Zhou G, Zhang X, Luo C, Feng H, He X, Zhu G, Yang H (2001) The formation of tetraploid stocks of red crucian carp × common carp hybrids as an effect of interspecific hybridization. Aquaculture 192:171–186

    Article  Google Scholar 

  13. Sun Y, Zhang C, Liu S, Duan W, Liu Y (2007) Induced interspecific androgenesis using diploid sperm from allotetraploid hybrids of common carp × red crucian carp. Aquaculture 264:47–53

    Article  CAS  Google Scholar 

  14. Yoshikawa H, Morishima K, Kusuda S, Yamaha E, Arai K (2007) Diploid sperm produced by artificially sex-reversed clone loaches. J Exp Zool 307A:75–83

    Article  Google Scholar 

  15. Yoshikawa H, Morishima K, Fujimoto T, Saito T, Kobayashi T, Yamaha E, Arai K (2009) Chromosome doubling in early spermatogonia produces diploid spermatozoa in a natural clonal fish. Biol Reprod 80:973–979

    Article  PubMed  CAS  Google Scholar 

  16. Fujita T (2007) Scientific name for the loach “Kara-Dojo” distributed in Japan. Jpn J Ichthyol 54:243–244 (in Japanese)

    Google Scholar 

  17. Chen IS, Chang YC (2005) A photographic guide to the inland-water fishes of Taiwan. Vol. 1: Cyprinifromes. The Suei Chan Press, Keelung, Taiwan (in Chinese)

  18. Perdices A, Vasil’ev V, Vasil’eva E (2011) Molecular phylogeny and intraspecific structure of loaches (genera Cobitis and Misgurnus) from the Far East region of Russia and some conclusions on their systematics. Ichthyol Res 59:1–11

    Google Scholar 

  19. Ojima Y, Hitotsumachi S (1969) Cytogenetical studies in loaches (Pisces, Cobitidae). Japan Zool Mag 78:139–141 (in Japanese with English summary)

    Google Scholar 

  20. Kim DS, Nam YK, Park IS (1995) Survival and karyological analysis of reciprocal diploid and triploid hybrids between mud loach (Misgurnus mizolepis) and cyprinid loach (Misgurnus anguillicaudatus). Aquaculture 135:257–265

    Article  Google Scholar 

  21. Park IS, Nam YK, Kim DS (2006) Growth performance, morphometric traits and gonad development of induced reciprocal diploid and triploid hybrids between the mud loach (Misgurnus mizolepis Günther) and cyprinid loach (Misgrunus anguillicaudatus Cantor). Aquac Res 37:1246–1253

    Article  Google Scholar 

  22. Fujimoto T, Yasui GS, Yoshikawa H, Yamaha E, Arai K (2008) Genetic and reproductive potential of spermatozoa of diploid and triploid males obtained from interspecific hybridization of Misgurnus anguillicaudatus female with M. mizolepis male. J Appl Ichthyol 24:430–437

    Article  Google Scholar 

  23. Zhao Y, Pšenička M, Fujimoto T, Saito T, Yasui GS, Yamaha E, Arai K (2012) Motility, morphology, mitochondria and ATP content of diploid spermatozoa from sex-reversed clonal diploid and neo-tetraploid loach, Misgurnus anguillicaudatus. J Appl Ichthyol 28:1006–1012

    Article  CAS  Google Scholar 

  24. Zhao Y, Saito T, Pšenička M, Fujimoto T, Arai K (2014) Comparison of spermatozoa parameters, fine structures, and energy-related factors among tetraploid, hyper-tetraploid, and hyper-triploid loaches (Misgurnus anguillicaudatus). J Exp Zool Part A Ecol Genet Physiol 321:198–206

    Article  CAS  Google Scholar 

  25. Zhao Y, Toda M, Hou JL, Aso M, Arai K (2012) The occurrence of hypertetraploid and other unusual polyploid loaches Misgurnus anguillicaudatus among market specimens in Japan. Fish Sci 78:1219–1227

    Article  CAS  Google Scholar 

  26. Kurokura H, Hirano R, Tomita M, Iwahashi M (1984) Cryopreservation of carp sperm. Aquaculture 37:267–273

    Article  Google Scholar 

  27. Yasui GS, Arias-Rodriguez L, Fujimoto T, Arai K (2009) A sperm cryopreservation protocol for the loach Misgurnus anguillicaudatus and its applicability for other related species. Anim Reprod Sci 116:335–345

    Article  PubMed  CAS  Google Scholar 

  28. Iwamatsu T, Ishijima S, Nakashima S (1993) Movement of spermatozoa and changes in micropyles durind fertilization in medaka eggs. J Exp Zool 266:57–64

    Article  Google Scholar 

  29. Poot M, Zhang YZ, Kramer JA, Wells KS, Lj Jones, Hanzel DK, Lugade AG, Singer VL, Haugland RP (1996) Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J Histochem Cytochem 44:1363–1372

    Article  PubMed  CAS  Google Scholar 

  30. Métivier D, Dallaporta B, Zamzami N, Larochette N, Susin SA, Marzo I, Kroemer G (1998) Cytofluorometric detection of mitochondrial alterations in early CD95/Fas/APO-1-triggered apoptosis of Jurkat T lymphoma cells. Comparison of seven mitochondrion-specific fluorochromes. Immunol Lett 61:157–163

    Article  PubMed  Google Scholar 

  31. Shimizu Y, Shibata N, Yamashita M (1997) Spermiogenesis without preceding meiosis in the hybrid medaka between Oryzias latipes and O. curvinotus. J Exp Zool 279:102–112

    Article  Google Scholar 

  32. Cosson J (2008) The motility apparatus of fish spermatozoa. In: Alavi SMH, Cosson JJ, Coward K, Rafiee C (eds) Fish spermatology. Alpha Science International Ltd, Oxford, pp 281–316

    Google Scholar 

Download references

Acknowledgments

This work was supported in part by Grants-in-Aid from JSPS-KAKENHI (grant no. 21380114) and JAMBIO (grant nos. 23-11 and 24-11) to KA and TF; grants from Youth Scholars of Shanghai Higher Education Institutions–China (grant no. A1-2035-14-0010-9) and the Doctoral Fund (grant no. A1-0209-13-0105390) to YZ; grants from the Ministry of Education, Youth and Sports of the Czech Republic (projects “CENAKVA”; grant no. CZ.1.05/2.1.00/01.0024 and “CENAKVA II”, LO1205 under the NPU I program) to MP.

Author information

Author notes

  1. Yan Zhao

    Present address: Key Laboratory of Freshwater Aquatic Genetic Resources of the Ministry of Agriculture, Shanghai Ocean University, Shanghai, 201306, China

  2. Martin Pšenička

    Present address: Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, University of South Bohemia in České Budějovice, Vodňany, Zátiší 728/II, České Budějovice, 389 25, Czech Republic

  3. Taiju Saito

    Present address: South Ehime Fisheries Research Center, Ehime University, Uchidomari, Ainan, Ehime, 798-4206, Japan

Authors and Affiliations

  1. Faculty and Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido, 041-8611, Japan

    Yan Zhao, Takafumi Fujimoto, Martin Pšenička, Taiju Saito & Katsutoshi Arai

Authors
  1. Yan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takafumi Fujimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin Pšenička
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Taiju Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katsutoshi Arai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katsutoshi Arai.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, Y., Fujimoto, T., Pšenička, M. et al. Non-motile tetraploid spermatozoa of Misgurnus loach hybrids. Fish Sci 82, 127–135 (2016). https://doi.org/10.1007/s12562-015-0939-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-015-0939-7

Keywords

Search

Navigation