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Partial formation of sperm dimorphism from spermatocytes of the cottoid fish, Hemilepidotus gilberti in cell culture

Published online by Cambridge University Press:  01 November 2007

Y. Hayakawa ,
E. Takayama-Watanabe ,
A. Watanabe ,
M. Kobayashi ,
H. Munehara  and
K. Onitake
Y. Hayakawa
Affiliation:
Department of Biology, Division of Natural Sciences, International Christian University, 3-10-2 Osawa, Mitaka, Tokyo, 181-8585Japan.
E. Takayama-Watanabe
Affiliation:
Yamagata Junior College, 515 Katayachi, Yamagata, 990-2316Japan.
A. Watanabe*
Affiliation:
Department of Biology, Faculty of Science, Yamagata University, 1–4-12 Kojirakawa, Yamagata, 990–8560, Japan.
M. Kobayashi
Affiliation:
Department of Biology, Division of Natural Sciences, International Christian University, 3-10-2 Osawa, Mitaka, Tokyo, 181-8585Japan.
H. Munehara
Affiliation:
Usujiri Fisheries Station, Field Science Center for Northern Biosphere, Hokkaido University, Hakodate, Hokkaido, 041–1613, Japan.
K. Onitake
Affiliation:
Department of Biology, Faculty of Science, Yamagata University, 1–4-12 Kojirakawa, Yamagata, 990–8560, Japan.
*
All correspondence to: Akihiko Watanabe, Department of Biology, Faculty of Science, Yamagata University, 1-4-12 Kojirakawa, Yamagata, 990-8560, Japan. Tel:/Fax: +81 23 628 4619. e-mail: watan@sci.kj.yamagata-u.ac.jp
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Summary

Polymorphism of sperm is considered to be significant for the reproductive strategy in some animal species. The phenomenon is thought to occur in the species-specific stage of spermatogenesis, but how the identical germ cells are differentiated towards polymorphic sperm remains unknown. We here performed a germ cell culture in the cottoid fish, Hemilepidotus gilberti, whose sperm exhibit dimorphism with fertilizable eusperm and unfertilizable parasperm. In the culture, germ cells, which were obtained with an identical morphology, a spherical shape of 5–7 µm in diameter, differentiated into smaller spherical cells with a single nucleus, a moving flagellum and localized mitochondria. In addition, large retroflex-shaped cells with two elongated nuclei were also observed in the cell culture. Germ cells that had each morphological feature were histologically also observed in some cysts of the spermatogenetic testis, suggesting that the former type of cell corresponded to developing eusperm and the latter corresponded to developing parasperm. When BrdU was incorporated into germ cells in the culture, it was detected in both cells with eusperm-like and those with parasperm-like morphologies. These findings suggest that DNA-duplicating spermatocytes are potent to autonomously progress a part of spermatogenesis to form dimorphic sperm.

Keywords

Cottoid fishDimorphic spermIn vitro spermatogenesisParaspermSpermiogenesis
Type
Research Article
Information
Zygote , Volume 15 , Issue 4 , November 2007 , pp. 285 - 293
Copyright
Copyright © Cambridge University Press 2007

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References

Abe, S-I. (1981). Meiosis of primary spermatocytes and early spermiogenesis in the resultant spermatids in newt, Cynops pyrrhogaster in vitro. Differentiation 20, 65–70.CrossRefGoogle ScholarPubMed
Abe, S-I. (1988). Cell culture of spermatogenic cells from amphibians. Develop. Growth Differ. 30, 209–18.CrossRefGoogle ScholarPubMed
Chong, K.L., Koh, M. & Melamed, P. (2005). Molecular regulation of gonadotropin gene expression in teleosts. In: Hormones and Their Receptors in Fish Reproduction (eds P. Melamed & N. Sherwood). pp. 76–104. Tuck Ling, Singapore: World Science Publishing.CrossRefGoogle Scholar
Cook, P.A. & Wedell, N. (1999). Non-fertile sperm delay female re-mating. Nature 397, 486.Google Scholar
Feng, L-X., Chen, Y., Dettin, L., Pera, R.A.R., Herr, J.C., Goldberg, E. & Dym, M. (2002). Generation and in vitro differentiation of a spermatogonial cell line. Science 297, 392–5.Google ScholarPubMed
Hayakawa, Y. (2007). Parasperm: morphological and functional studies on the non-fertile sperm. Ichthyol. Res. 54, 111–30.CrossRefGoogle Scholar
Hayakawa, Y. & Munehara, H. (1998). Fertilization environment of the non-copulating marine sculpin, Hemilepidotus gilberti. Env. Biol. Fish. 52, 181–6.CrossRefGoogle Scholar
Hayakawa, Y. & Munehara, H. (2004). Ultrastructural observations of euspermatozoa and paraspermatozoa in a copulatory cottoid fish Blepsias cirrhosus. J. Fish Biol. 64, 1530–9.CrossRefGoogle Scholar
Hayakawa, Y., Komaru, A. & Munehara, H. (2002a). Ultrastructural observations of eu- and paraspermiogenesis in the cottid fish Hemilepidotus gilberti (Teleostei: Scorpaeniformes: Cottidae). J. Morphol. 253, 243–54.CrossRefGoogle ScholarPubMed
Hayakawa, Y., Munehara, H. & Komaru, A. (2002b). Obstructive role of the dimorphic sperm in a non-copulatory marine sculpin, Hemilepidotus gilberti, to prevent other males’ eusperm from fertilization. Env. Biol. Fish. 64, 419–27.CrossRefGoogle Scholar
Hayakawa, Y., Kobayashi, M., Munehara, H., Watanabe, A. & Onitake, K. (2007). Spermatogenesis involving the parasperm production in the marine cottoid fish, Hemilepidotus gilberti. Raffles Bul. Zool., Suppl 14, 29–35.Google Scholar
Hong, Y., Liu, T., Zhao, H., Xu, H., Wang, W., Liu, R., Chen, T., Deng, J. & Gui, J. (2004). Establishment of a normal medaka fish spermatogonial cell line capable of sperm production in vitro. Proc. Natl. Acad. Sci. USA. 101, 8011–6.CrossRefGoogle ScholarPubMed
Jamieson, B.G. (1987). A biological classification of sperm type, with special reference to annelids and molluscs and examermiocladistics. In: New Horizons in Sperm Cell Research (ed. H. Mohri). pp. 311–32. Tokyo, Japan: Japan Societies Press, Gordon and Breach Science Publishers.Google Scholar
Okura, N., Kohata, Y., Harutsugu, Y. & Yasuzumi, F. (1988). The aberrant meiosis and the hyperpyrenic atypical spermatozoon in the black snail, Semisulcospina libertina. J. Submicr. Cytol. Pathol. 20, 683–9.Google Scholar
Osanai, M., Kasuga, H. & Aigaki, T. (1987). Physiological role of apyrene spermatozoa of Bombyx mori. Experimentia 43, 593–6.CrossRefGoogle Scholar
Pudney, J. (1993). Comparative cytology of the non-mammalian vertebrate Sertoli cell. In: The Sertoli Cell (ed. L.D. Russell & M.D. Griswold). pp. 611–57. Clearwater, FL: Cache River Press.Google Scholar
Risley, M.S. & Eckhardt, R.A. (1979). Evidence for the continuation of meiosis and spermiogenesis in in vitro cultures of spermatogenic cells from Xenopus laevis. J. Exp. Zool. 207, 513–20.CrossRefGoogle Scholar
Sahara, K. & Kawamura, N. (2002). Double copulation of a female with sterile diploid and polyploid males covers fertility in Bombyx mori. Zygote 10, 23–9.CrossRefGoogle Scholar
Saiki, A., Tamura, M., Matsumoto, M., Katowgi, J., Watanabe, A. & Onitake, K. (1997). Establishment of in vitro spermatogenesis from spermatocytes in the medaka, Oryzias latipes. Develop. Growth Differ. 39, 337–44.CrossRefGoogle ScholarPubMed
Sasaki, T., Watanabe, A., Takayama-Watanabe, E., Suzuki, M., Abe, H. & Onitake, K. (2005). Ordered progress of spermiogenesis to the fertilizable sperm of the medaka fish, Oryzias latipes, in cell culture. Develop. Growth Differ. 47, 87–97.CrossRefGoogle Scholar
Sherwood, N.M. & Adams, B.A. (2005). Gonadotropin-releasing hormone in fish: evolution, expression and regulation of the GnRH gene. In: Hormones and Their Receptors in Fish Reproduction (ed. P. Melamed & N. Sherwood). pp. 1–39. Tuck Ling, Singapore: World Science Publishing.Google Scholar
Swallow, J.G. & Wilkinson, G.S. (2002). The long and short sperm polymorphism in insects. Biol. Rev. 77, 153–82.CrossRefGoogle Scholar
Till-Bottraud, I., Joly, D., Lachaise, D. & Snook, R.R. (2005). Pollen and sperm heteromorphism: convergence across kingdom? J. Evol. Biol. 18, 1–18.CrossRefGoogle Scholar
Yamashiki, N. & Kawamura, N. (1997). Behaviors nucleus, basal bodies and microtubules during eupyrene and apyrene spermiogenesis in the silkworm, Bombyx mori (Lepidoptera). Develop. Growth Differ. 39, 715–22.CrossRefGoogle ScholarPubMed
Young, G., Kusakabe, M., Nakamura, I., Lokman, P.M. & Goetz, F.W. (2005). Gonadal steroidogenesis in teleost fish. In: Hormones and Their Receptors in Fish Reproduction (eds P. Melamed & N. Sherwood), pp. 155–223. Tuck Ling, Singapore: World Science Publishing.CrossRefGoogle Scholar
Watanabe, A. & Onitake, K. (2007). The regulation of spermatogenesis in fish: recent cellular and molecular approaches. In: Fish Spermatology (eds S.M.H. Alavi, J.J. Cosson, K. Coward, & Gh. Rafiee), pp. 141–60. Oxford, Alpha Science Ltd.Google Scholar