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Spermatogenesis and the fine structure of the mature spermatozoon of the liver fluke, Fasciola hepatica (Trematoda: Digenea)

Published online by Cambridge University Press:  06 April 2009

A. W. Stitt
Affiliation:
School of Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland
I. Fairweather
Affiliation:
School of Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland

Summary

Spermatogenesis and the fine structure of the mature spermatozoon of Fasciola hepatica have been studied by transmission electron microscopy. The primary spermatogonia display a typical gonial morphology and occupy the periphery of the testis. They undergo 3 mitotic divisions to give rise to 8 primary spermatocytes forming a rosette of cells connected to a central cytophore. The primary spermatocytes undergo 2 meiotic divisions, resulting in 32 spermatids that develop into spermatozoa. Intranuclear synaptonemal complexes in primary spermatocytes confirm the first meiotic division. The onset of spermiogenesis is marked by the formation of the zone of differentiation which contains 2 basal bodies and a further centriole derivative, the central body. The zone extends away from the spermatid cell to form the median process; into this migrates the differentiated and elongate nucleus. Simultaneously, 2 axonemes develop from the basal bodies. During development, they rotate through 90° to extend parallel to the median process. The migration of the nucleus to the distal end of the median process coincides with the fusion of the axonemes to the latter to form a monopartite spermatozoon. The mature spermatozoon possesses 2 axonemes of the 9 + ‘1’ pattern typical of parasitic platyhelminths, 2 elongate mitochondria and a variable array of peripheral microtubules. The nuclear region of the spermatozoon is immotile. The value of sperm ultrastructure as a taxonomic tool in platyhelminth phylogeny is discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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References

REFERENCES

Awad, A. H. H. & Probert, A. J. (1989). Transmission and scanning electron microscopy of the male reproductive system of Schistosoma margrebowiei Le Roux, 1933. Journal of Helminthology 63, 197205.CrossRefGoogle Scholar
Barker, K. E. & Diegenbach, P. C. (1973). The ultrastructure of spermatozoa of Aspidogaster conchicola Baer, 1826 (Aspidogastridae, Trematoda). Netherlands Journal of Zoology 23, 345–6.Google Scholar
Burton, P. R. (1960). Gametogenesis and fertilisation in the frog lung fluke, Haematoloechus medioplexus Stafford (Trematoda: Plagiorchiidae). Journal of Morphology 107, 93121.CrossRefGoogle ScholarPubMed
Burton, P. R. (1972). Fine structure of the reproductive system of a frog lung fluke. III. The spermatozoon and its differentiation. Journal of Parasitology 58, 6883.CrossRefGoogle Scholar
Daddow, L. Y. M. & Jamieson, B. G. M. (1983). An ultrastructural study of spermiogenesis in Neochasmus sp. (Cryptogonimidae: Digenea: Trematoda). Australian Journal of Zoology 31, 114.CrossRefGoogle Scholar
Davis, R. E. & Roberts, L. S. (1983). Platyhelminthes–Eucestoda. In Reproductive Biology of Invertebrates, Vol. 2, Spermatogenesis and Sperm Function (ed. Adiyodi, K. G. & Adiyodi, R. G.), pp. 131149. Chichester, New York, Toronto: John Wiley and Sons Ltd.Google Scholar
Erwin, B. E. & Halton, D. W. (1983). Fine structural observations on spermatogenesis in a progenetic trematode, Bucephaloides gracilescens. International Journal for Parasitology 13, 413–26.CrossRefGoogle Scholar
Euzet, L., Swiderski, Z. & Mokhtar-Maamouri, F. (1981). Ultrastructure comparée du spermatozoïde des cestodes. Relations avec la phylogénèse. Annales de Parasitologie Humaine et Comparée 56, 247–59.CrossRefGoogle Scholar
Fujino, T., Ishii, Y. & Mori, T. (1977). Ultrastructural studies on the spermatozoa and spermatogenesis in Paragonimus and Eurytrema (Trematoda: Digenea). Japanese Journal of Parasitology 26, 240–55.Google Scholar
Grant, W. C., Harkema, R. & Muse, K. E. (1976). Ultrastructure of Pharyngostomoides procyonis Harkema 1942 (Diplostomatidae). 1. Observations on the male reproductive system. Journal of Parasitology 62, 3949.CrossRefGoogle ScholarPubMed
Gresson, R. A. R. (1957). Spermateleosis in Fasciola hepatica. Quarterly Journal of Microscopical Science 98, 493–8.Google Scholar
Gresson, R. A. R. (1965). Spermatogenesis in the hermaphroditic Digenea (Trematoda). Parasitology 55, 117–25.CrossRefGoogle Scholar
Gresson, R. A. R. & Perry, M. M. (1961). Electron microscope studies of spermateleosis in Fasciola hepatica L. Experimental Cell Research 22, 18.CrossRefGoogle ScholarPubMed
Halton, D. W. & Hardcastle, A. (1976). Spermatogenesis in a monogenean, Diclidophora merlangi. International Journal for Parasitology 6, 4353.CrossRefGoogle Scholar
Hendelberg, J. (1962). Paired fiagella and nucleus migration in the spermiogenesis of Dicrocoelium and Fasciola (Digenea, Trematoda). Zoologiska bidrag från Uppsala 35, 569–87.Google Scholar
Hendelberg, J. (1986). The phylogenetic significance of sperm morphology in the Platyhelminthes. Hydrobiologia 132, 53–8.CrossRefGoogle Scholar
Hershenov, B. R., Tulloch, G. S. & Johnson, A. D. (1966). The fine structure of trematode sperm-tails. Transactions of the American Microscopical Society 85, 480–3.CrossRefGoogle ScholarPubMed
Jamieson, B. G. M. & Daddow, L. M. (1982). The ultrastructure of the spermatozoon of Neochasmus sp. (Cryptogonimidae, Digenea, Trematoda) and its phylogenetic significance. International Journal for Parasitology 12, 547–59.CrossRefGoogle Scholar
John, B. (1953). The behaviour of the nucleus during spermatogenesis in Fasciola hepatica. Quarterly Journal of Microscopical Science 94, 4155.Google Scholar
Justine, J.-C., Lambert, A. & Mattei, X. (1985 a). Spermatozoon ultrastructure and phylogenetic relationships in the monogeneans (Platyhelminthes). International Journal for Parasitology 15, 601–8.CrossRefGoogle ScholarPubMed
Justine, J.-C., Le Brun, N. & Mattei, X. (1985 b). The aflagellate spermatozoon of Diplozoon (Platyhelminthes: Monogenea: Polyopisthocotylea): a demonstrative case of relationship between sperm ultrastructure and biology of reproduction. Journal of Ultrastructure Research 92, 4754.CrossRefGoogle ScholarPubMed
Justine, J.-C. & Mattei, X. (1981). Etude ultrastructurale du flagelle spermatique des schistosomes (Trematoda: Digenea). Journal of Ultrastructure Research 76, 8995.CrossRefGoogle ScholarPubMed
Justine, J.-C. & Mattei, X. (1982 a). Etude ultrastructurale de la spermiogénèse et du spermatozoïde d'un platyhelminthe: Gonapodasmius (Trematoda: Didymozoidae). Journal of Ultrastructure Research 79, 350–65.CrossRefGoogle Scholar
Justine, J.-C. & Mattei, X. (1982 b). Réinvestigation de l'ultrastructure du spermatozoïde d'Haematoloechus (Trematoda: Haematoloechidae). Journal of Ultrastructure Research 81, 322–32.CrossRefGoogle ScholarPubMed
Justine, J.-C. & Mattei, X. (1983 a). Etude ultrastructurale comparée de la spermiogénèse des Monogènes. 1. Megalocotyle (Monopisthocotylea Capsalidae). Journal of Ultrastructure Research 82, 296308.CrossRefGoogle Scholar
Justine, J.-C. & Mattei, X. (1983 b). Comparative ultrastructural study of spermiogenesis in monogeneans (fiatworms). 2. Heterocotyle (Monopisthocotylea, Monocotylidae). Journal of Ultrastructure Research 84, 213–23.CrossRefGoogle Scholar
Justine, J.-C. & Mattei, X. (1983 c). A spermatozoon with two 9 + 0 axonemes in a parasitic flatworm, Didymozoon (Digenea: Didymozoidae). Journal of Submicroscopic Cytology 15, 1101–5.Google Scholar
Justine, J.-C. & Mattei, X. (1984 a). Atypical spermiogenesis in a parasitic flatworm, Didymozoon (Trematoda: Digenea: Didymozoidae). Journal of Ultrastructure Research 87, 106–11.CrossRefGoogle Scholar
Justine, J.-C. & Mattei, X. (1984 b). Comparative ultrastructural study of spermiogenesis in monogeneans (flatworms). 4. Diplectanum (Monopisthocotylea Diplectanidae). Journal of Ultrastructure Research 88, 7791.CrossRefGoogle Scholar
Kitajima, E. W., Paraense, W. L. & Correa, L. R. (1976). The fine structure of Schistosoma mansoni sperm (Trematoda: Digenea). Journal of Parasitology 62, 215–21.CrossRefGoogle ScholarPubMed
Lumsden, R. D. (1965). Macromolecular structure of glycogen in some cyclophyllidean and trypanorhynch cestodes. Journal of Parasitology 51, 501–15.CrossRefGoogle ScholarPubMed
Mahendrasingam, S., Fairweather, I. & Halton, D. W. (1989). Spermatogenesis and the fine structure of the mature spermatozoon in the free proglottis of Trilocularia acanthiaevulgaris (Cestoda, Tetraphyllidea). Parasitology Research 75, 287–98.CrossRefGoogle ScholarPubMed
Mohandas, A. (1983). 4. Platyhelminthes – Trematoda. In Reproductive Biology of Invertebrates, Vol. II, Spermatogenesis and Sperm Function (ed. Adiyodi, K. G. & Adiyodi, R. G.), pp. 105129. Chichester, New York, Toronto: John Wiley and Sons Ltd.Google Scholar
Morseth, D. J. (1969). Spermtail finestructure of Echinococcus granulosus and Dicrocoelium dendriticum. Experimental Parasitology 24, 4753.CrossRefGoogle ScholarPubMed
Nez, M. M. & Short, R. B. (1957). Gametogenesis in Schistosomatium douthitti (Cort) (Schistosomatidae: Trematoda). Journal of Parasitology 43, 167–82.CrossRefGoogle ScholarPubMed
Orido, Y. (1988). Ultrastructure of spermatozoa of the lung fluke, Paragonimus ohirai (Trematoda: Troglotrematidae), in the seminal receptacle. Journal of Morphology 196, 333–43.CrossRefGoogle ScholarPubMed
Orido, Y. & Hata, H. (1988). Cytological and cytofluorometrical studies on gametogenesis of Paragonimus ohirai (Trematoda: Troglotrematidae). International Journal for Parasitology 18, 95101.CrossRefGoogle Scholar
Rees, F. G. (1979). The ultrastructure of the spermatozoon and spermiogenesis in Cryptocotyle lingua (Digenea: Heterophyidae). International Journal for Parasitology 9, 405–19.CrossRefGoogle Scholar
Robinson, R. D. & Halton, D. W. (1982). Fine structural observations on spermatogenesis in Corrigia vitta (Trematoda: Dicrocoeliidae). Zeitschrift für Parasitenkunde 68, 5372.CrossRefGoogle Scholar
Rohde, K. (1971). Untersuchungen an Multicotyle purvisi Dawes, 1941 (Trematoda: Aspidogastrea). VI. Ultrastruktur des spermatozoons. Zoologische Jahrbucher. Abteilung für Anatomie und Ontogenie der Tiere 88, 399405.Google Scholar
Sato, M., Oh, M. & Sakoda, K. (1967). Electron microscopic study of spermatogenesis in the lung fluke (Paragonimus miyazakii). Zeitschrift für Zellforschung und mikroskopische Anatomie 77, 232–43.CrossRefGoogle ScholarPubMed
Shapiro, J. E., Hershenov, B. R. & Tulloch, G. S. (1961). The fine structure of Haematoloechus spermatozoan tail. Journal of Biophysics and Biochemical Cytology 9, 211–17.CrossRefGoogle ScholarPubMed
Spurr, A. R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research 26, 3143.CrossRefGoogle ScholarPubMed
Swiderski, Z. & Tsinonis, N. (1986). Spermatogenesis in Schistosoma mattheei. Proceedings of the XIth International Congress on Electron Microscopy, Kyoto, Japan, pp. 3325–6.Google Scholar
Tuzet, O. & Ktari, M. H. (1971 a). La spermiogénèse et la structure du spermatozoïde de Microcotyle mormyri Lorenz, 1878 (Monogenea). Comptes Rendus des Séances de l'Académie des Sciences. Série D 272, 2702–5.Google Scholar
Tuzet, O. & Ktari, M. H. (1971 b). Recherches sur l'ultrastructure du spermatozoïde de quelques monogènes. Bulletin de la Société Zoologique de France 96, 535–40.Google Scholar
Yosufzai, H. R. (1952). Cytological studies on the spermatogenesis of Fasciola hepatica L. La Cellule 55, 719.Google ScholarPubMed