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Sexual reproduction in the compound ascidian Diplosoma listerianum (Tunicata). II. Sperm penetration through ovary wall and evidence of internal fertilization

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Abstract

Diplosoma listerianum differs from most ascidians in that, at ovulation, eggs are emitted at the bottom of the ovary and segregated into the tunic, so that fertilization occurs far from seawater. A fertilization canal, a hollow extension of the ovary, conducts sperm towards the egg. In the present paper, ultrastructural evidence is reported on the morphological relationship between the ovary, egg envelopes and oocyte and on the mechanism by which sperm-egg interaction is established. In the ovary, the very complex sperm, equipped with a spiral “dense groove”, undergo metamorphosis as the first step in a sperm reaction and then pass through the ovary epithelium insinuating themselves between the intercellular junctions which appear to be mouldable, although able to maintain the egg-ovary barrier. Sperm then reach the vitelline coat, where a further step in the sperm reaction occurs. Before the egg abandons the ovary, the sperm head is incorporated into the oocyte by a process recalling phagocytosis, with the formation of an engulfing pocket. Sperm-egg contact and incorporation in D. listerianum occur in a way, never previously reported for other ascidians, in which fusion of plasma membranes takes place immediately after sperm-egg contact. Unlike other cytoplasmic components, the dense groove persists until the sperm enters the egg. It gives a corkscrew-like configuration to the sperm head and allows close adhesion to cell membranes, facilitating sperm movement. Expulsion of numerous cortical granules and features of a cortical reaction were observed in the egg penetrated by the sperm. The mode of internal fertilization of this species in comparison with that of other tunicates and phylogenetic aspects are discussed. Ripe colonies of D. listerianum collected in the Lagoon of Venice, Italy in 1986 and 1991 and colonies reared on glass in aquaria were used for our investigations.

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References

  • Baccetti, B., Afzelius, B. A. (1976). The biology of sperm cell. In: Wolsky, A. (ed.) Monographs in developmental biology, Vol. 10. S. Karger, New York

    Google Scholar 

  • Berrill, N. J. (1950). The Tunicata with an account of the British species. Ray Society, London

    Google Scholar 

  • Bishop, J. D. D., Ryland, J. S. (1991). Storage of exogeneous sperm by the compound ascidian Diplosoma listerianum. Mar. Biol. 108: 111–118

    Google Scholar 

  • Brunetti, R., Bressan, M., Marin, M., Libralato, M. (1988). On the ecology and biology of Diplosoma listerianum (Milne Edwards, 1841) (Ascidiacea, Didemnidae). Vie Milieu 38: 123–131

    Google Scholar 

  • Burighel, P., Martinucci, G. B. (1991). Sperm morphology and fertilization biology in ascidians. Acta Embryol. Morph. exp. (N.S.) 12: 85–86

    Google Scholar 

  • Burighel, P., Martinucci, G. B. (1994). Sexual reproduction in the compound ascidian Diplosoma listerianum (Tunicata). I. Metamorphosis, storage and phagocytosis of sperm in female duct. Mar. Biol. 118: 489–498

    Google Scholar 

  • Burighel, P., Martinucci, G. B., Magri, F. (1985). Unusual structures in the spermatozoa of the ascidian Diplosoma listerianum (Didemnidae). Cell Tissue Res. 241: 513–521

    Google Scholar 

  • Burighel, P., Martinucci, G. B., Zaniolo, G. (1987). Tissue repair during egg segregation in tunic of the compound ascidian Diplosoma listerianum. Acta Embryol. Morph. exp. (N.S.) 8: 333–340

    Google Scholar 

  • Cloney, R. A., Abbott, L. C. (1980). The spermatozoa of ascidians: acrosome and nuclear envelope. Cell Tissue Res. 206: 261–270

    Google Scholar 

  • De Santis, R., Pinto, M. R. (1988). The pathway of sperm-egg interaction in ascidians: biology and chemistry. Zool. Sci. 5: 919–924

    Google Scholar 

  • Dym, M., Fawcett, D. W. (1970). The blood-testis barrier in the rat and the physiological compartimentation of the seminiferous epithelium. Biol. Reprod. 3: 308–326

    Google Scholar 

  • Fisher, G. W., Rebhun, L. I. (1983). Sea urchin egg cortical granules exocytosis is followed by a burst of membrane retrieval via uptake into coated vesicles. Devl Biol. 99: 456–472

    Google Scholar 

  • Flood, P. R., Afzelius, B. A. (1978). The spermatozoon of Oikopleura dioica Fol (Larvacea, Tunicata). Cell Tissue Res. 191: 27–37

    Google Scholar 

  • Franzen, Å. (1956). On spermiogenesis, morphology of the spermatozoon, and biology of fertilization among invertebrates. Zool. Bidr. Upps. 31: 355–482

    Google Scholar 

  • Franzen, Å. (1970). Phylogenetic aspects of the morphology of spermatozoa and spermiogenesis. In: Baccetti, B. (ed.) Comparative spermatology. Academic Press, New York, p. 29–45

    Google Scholar 

  • Franzen, Å. (1992). Spermatozoan ultrastructure and spermatogenesis in aplousobranch ascidians, with some phylogenetic considerations. Mar. Biol. 113: 77–87

    Google Scholar 

  • Fuke, M. (1983). Self and non-self recognition between gametes of the ascidian, Halocynthia roretzi. Wilhelm Roux Arch. dev. Biol. 192: 347–352

    Google Scholar 

  • Fukumoto, M. (1981). The spermatozoa and spermiogenesis of Perophora formosana (Ascidia) with special reference to the striated apical structure and the filamentous structures in the mitochondrion. J. Ultrastruct. Res. 77: 37–53

    Google Scholar 

  • Fukumoto, M. (1988). Fertilization in ascidians: apical processes abd gamete fusion in Ciona intestinalis spermatozoa. J. Cell Sci. 89: 189–196

    Google Scholar 

  • Fukumoto, M. (1990a). Morphological aspects of ascidian fertilization: acrosome reaction, apical processes and gamete fusion in Ciona intestinalis. Invert. Reprod. Dev. 17: 147–154

    Google Scholar 

  • Fukumoto, M. (1990b). Morphological aspects of ascidian fertilization. Zool. Sci. 7: 989–998

    Google Scholar 

  • Godknecht, A., Honegger, T. G. (1991). Isolation, characterization, and localization of a sperm-bound N-acetylglucosaminidase that is indispensable for fertilization in the ascidian, Phallusia mammillata. Devl Biol. 143: 398–407

    Google Scholar 

  • Guraya, S. S. (1982). Recent progress in the structure, origin, composition, and function of the cortical granules in animal egg. Int. Rev. Cytol. 257–359

  • Holland, L. Z. (1988). Spermatogenesis in the salps Thalia democratica and Cyclosalpa affinis (Tunicata: Thaliacea): an electron microscopic study. J. Morph. 198: 189–204

    Google Scholar 

  • Holland, L. Z. (1989). Fine structure of spermatids and sperm of Dolioletta gegenbauri and Doliolum nationalis (Tunicata: Thaliacea): implications for tunicate phylogeny. Mar. Biol. 101: 83–95

    Google Scholar 

  • Holland, L. Z. (1990). Spermatogenesis in Pyrosoma atlanticum (Tunicata: Thaliacea: Pyrosomatida): implications for tunicate phylogeny. Mar. Biol. 105: 451–470

    Google Scholar 

  • Holland, L. Z. (1991). The phylogenetic significance of tunicate sperm morphology. In: Baccetti B. (ed.) Comparative spermatology twenty years after. Serono Symp. Publ. Vol. 75, Raven Press, New York, p. 961–965

    Google Scholar 

  • Holland, L. Z., Gorsky, G., Fenaux, R. (1988). Fertilization in Oikopleura dioica (Tunicata, Appendicularia): acrosome reaction, cortical reaction and sperm-egg fusion. Zoomorphology 108: 229–243

    Google Scholar 

  • Honegger, T. G. (1986). Fertilization in ascidians: studies on the egg envelope, sperm and gamete interactions in Phallusia mammillata. Devl Biol. 118: 118–128

    Google Scholar 

  • Hoshi, M., De Santis, R., Pinto, M. R., Cotelli, F., Rosati, F. (1985). Sperm glycosidases as mediators of sperm-egg binding in the ascidians. Zool. Sci. 2: 65–69

    Google Scholar 

  • Hoshi, M., Numakunai, T., Sawada, H. (1981). Evidence for participation of sperm proteinases in fertilization of the solitary ascidian, Halocynthia roretzi: effect of protease inhibitors. Devl Biol. 86: 117–121

    Google Scholar 

  • Jamieson, B. G. M. (1987). A biological classification of sperm types, with special reference to annellids and molluscs, and an example of spermiocladistics. In: Mohri, H. (ed.). New horizons in sperm cell research. New York, p. 311–332

  • Jamieson, B. G. M. (1991). Fish evolution and systematics: evidence from spermatozoa. With a survey of lophophorate, echinoderm and protochordate sperm and an account of gamete cryopreservation. Cambridge University Press, Cambridge

    Google Scholar 

  • Kawamura, K., Fujita, H., Nakauchi, M. (1987). Cytological characterization of self incompatibility in gametes of the ascidian, Ciona intestinalis. Dev. Growth Differentiation 29: 627–642

    Google Scholar 

  • Koch, R. A., Lambert, C. C. (1990). Ultrastructure of sperm, spermiogenesis and sperm-egg interactions in selected invertebrates and lower vertebrates which use external fertilization. J. Electron Microsc. Tech. 16: 115–154

    Google Scholar 

  • Lambert, C. C. (1982). The ascidian sperm reaction. Am. Zool. 22: 841–849

    Google Scholar 

  • Lambert, C. C. (1986). Fertilization-induced modification of chorion n-acetylglucosamine groups blocks polyspermy in ascidian eggs. Devl Biol. 116: 168–173

    Google Scholar 

  • Lambert, C. C., Epel, D. (1979). Calcium-mediated mitochondrial movement in ascidian sperm during fertilization. Devl Biol. 69: 296–304

    Google Scholar 

  • Lambert, C. C., Koch, R. A. (1988). Sperm binding and penetration during ascidian fertilization. Dev. Growth Differentiation 30: 325–356

    Google Scholar 

  • Lambert, C. C., Lambert, G. (1983). Mitochondrial movement during the ascidian sperm reaction. Gamete Res. 8: 295–307

    Google Scholar 

  • Lane, N. J., Dallai, R., Burighel, P., Martinucci, G. B. (1986). Tight and gap junctions in the intestinal tract of tunicates: a freeze-fracture study. J. Cell Sci. 84: 1–17

    Google Scholar 

  • Longo, F. J. (1987). Fertilization. Chapman and Hall, New York

    Google Scholar 

  • Martinucci, G. B., Burighel, P., Zaniolo, G., Brunetti, R. (1988). Ovulation and egg segregation in the tunic of the colonial ascidian, Diplosoma listerianum, (Tunicata, Ascidiacea). Zoomorphology 108: 219–227

    Google Scholar 

  • Miller, R. L. (1982). Sperm chemotaxis in ascidians. Am. Zool. 22: 827–840

    Google Scholar 

  • Monroy, A., Rosati, F. (1983). Review article: a comparative analysis of sperm-egg interaction. Gamete Res. 7: 85–102

    Google Scholar 

  • Mukai, H. (1977). Comparative studies on the structure of reproductive organs of four botryllids ascidians. J. Morph. 193: 263–276

    Google Scholar 

  • Patricolo, E., Villa, L. (1992). Ascidian interspecific fertilization. II. A study of the external egg coating in hybrid crosses. Anim. Biol. (Palermo, Italy) 1: 9–15

    Google Scholar 

  • Reverberi, G. (1971). The embryology of ascidians. In: Reverberi, G. (ed.) Experimental embryology of marine and freshwater invertebrates. North-Holland, Amsterdam, p. 507–550

    Google Scholar 

  • Rosati, F. (1985). Sperm-egg interaction in ascidians. In: Metz, C. B, Monroy, A. (eds.) Biology of fertilization, Vol 2. Biology of the sperm. Academic Press, New York, p. 361–388

    Google Scholar 

  • Rosati, F., De Santis, R. (1978). Studies on fertilization in the ascidians. I. Self-sterility and specific recognition between gametes of Ciona intestinalis. Expl Cell Res. 112: 111–119

    Google Scholar 

  • Rosati, F., Monroy, A., De Prisco, P. (1977). Fine structural study of fertilization in the ascidian, Ciona intestinalis. J. Ultrastruct. Res. 58: 261–270

    Google Scholar 

  • Russel, L., Peterson, R. N. (1985). Sertoli cell junctions: morphological and functional correlates. Int. Rev. Cytol. 94: 177–211

    Google Scholar 

  • Ryland, J. S., Bishop, J. D. D. (1990). Prevalence of cross-fertilization in the hermaphroditic compound ascidian Diplosoma listerianum. Mar. Ecol. Prog. Ser. 61: 125–131

    Google Scholar 

  • Tuzet, O., Bogoraze, D., Lafargue, F. (1972). Recherches ultrastructurales sur la spermiogénèse de Diplosoma listerianum (Milne-Edwards, 1841) et Lissoclinum pseudoleptoclinum (Von Drasche, 1883) (Ascidies composèes, Aplousobranches). Annls Sci. nat. (sér. Zool.) 14: 177–190

    Google Scholar 

  • Villa, L. (1981). An electron microscope study of spermiogenesis and spermatozoa of Molgula impura and Styela plicata (Ascidiacea, Tunicata). Acta Embryol. Morph. exp. (N.S.) 2: 69–85

    Google Scholar 

  • Woollacott, R. M. (1977). Spermatozoa of Ciona intestinalis and analysis of ascidian fertilization. J. Morph. 152: 77–88

    Google Scholar 

  • Zaniolo, G., Burighel, P., Martinucci, G. B. (1987). Ovulation and placentation in Botryllus schlosseri (Ascidiancea): an ultrastructural study. Can. J. Zool. 65: 1181–1190

    Google Scholar 

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Communicated by M. Sarà, Genova

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Burighel, P., Martinucci, G.B. Sexual reproduction in the compound ascidian Diplosoma listerianum (Tunicata). II. Sperm penetration through ovary wall and evidence of internal fertilization. Marine Biology 118, 499–510 (1994). https://doi.org/10.1007/BF00350307

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