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An ultrastructural analysis of the gametes and early fertilization in two bivalve molluscs, Chama macerophylla and Spisula solidissima with special reference to gamete binding

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Summary

An ultrastructural investigation of the gametes and their interaction during the early events of fertilization in molluscs has been performed. A gamete binding event involving large numbers of sperm has been identified and examined in detail. The surface of the oocyte is projected into numerous microvilli which extend through the vitelline envelope. Tufts of fibrillar material radiate from the tips of these microvilli, forming a layer external to the vitelline envelope. The acrosomal vesicle of the mature spermatozoon contains two major components, which function differently during fertilization. The vesicle is indented at its adnuclear surface, constituting a preformed acrosomal tubule. This tubule does not elongate during the acrosome reaction. Completion of the reaction results in the formation of an extracellular coat, derived from one component of the acrosomal vesicle, on the anterior surface of the sperm. Sperm-egg binding is accomplished by an association of the extracellular coat on the reacted sperm and the fibrous tufts on the tips of the microvilli of the oocyte. Evidence that gamete membrane fusion occurs by fusion of the acrosomal tubule and a microvillus is presented. These observations provide a generalized pattern of molluscan fertilization.

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References

  • Aketa, K.: On the sperm-egg binding as the initial step of fertilization in the sea urchin. Embryologia (Nagoya) 9, 238–245 (1967)

    Google Scholar 

  • Aketa, K., Onitake, K., Tsuzuki, H.: Tryptic disruption of sperm-binding site of sea urchin egg surface. Exp. Cell Res. 71, 27–32 (1972)

    Google Scholar 

  • Berg, W.E.: Lytic effects of sperm extracts on the eggs of Mytilus edulis. Biol. Bull. 98, 128–138 (1950)

    Google Scholar 

  • Bourcart, C., Lavallard, R., Lubet, P.: Ultrastructure du spermatozoïde de la Moule (Mytilus perna). C.R. Acad. Sci. (Paris) 260, 5096–5099 (1965)

    Google Scholar 

  • Brown, G.G.: Ultrastructural studies of sperm morphology and sperm-egg interaction in the decapod Callinectes sapidus. J. Ultrastruct. Res. 14, 425–440 (1966)

    Google Scholar 

  • Brown, G.G.: Scanning electron-microscopical and other observations of sperm fertilization reactions in Limulus polyphemus L. (Merostomata: Xiphosura). J. Cell Sci. 22, 547–562 (1976)

    Google Scholar 

  • Brown, G.G., Humphreys, W.J.: Sperm-egg interactions of Limulus polyphemus with scanning electron microscopy. J. Cell Biol. 51, 904–907 (1971)

    Google Scholar 

  • Colwin, A.L., Colwin, L.H.: Egg membrane lytic activity of sperm extract and its significance in relation to sperm entry in Hydroides hexagonus (Annelida). J. biophys. biochem. Cytol. 7, 321–328 (1960)

    Google Scholar 

  • Colwin, A.L., Colwin, L.H.: Role of the gamete membranes in fertilization. In: Cellular membranes in development (M. Locke, ed.), pp. 233–279. New York: Academic Press 1964

    Google Scholar 

  • Colwin, L.H., Colwin, A.L.: Changes in the spermatozoon during fertilization in Hydroides hexagonus (Annelida). I. Passage of the acrosomal region through the vitelline membrane. J. biophys. biochem. Cytol. 10, 231–254 (1961)

    Google Scholar 

  • Colwin, L.H., Colwin, A.L.: Membrane fusion in relation to sperm-egg association. In: Fertilization, comparative morphology, biochemistry and immunology (C.B. Metz, A. Monroy, eds.), pp. 295–367. New York: Academic Press 1967

    Google Scholar 

  • Colwin, A.L., Colwin, L.H., Philpott, D.E.: Electron microscope studies of early stages of sperm penetration in Hydroides hexagonus (Annelida) and Saccoglossus kowalevskii (Enteropneusta). J. biophys. biochem. Cytol. 3, 489–502 (1957)

    Google Scholar 

  • Dan, J.C.: The vitelline coat of the Mytilus egg. I. Normal structure and effect of acrosomal lysin. Biol. Bull. 123, 531–541 (1962)

    Google Scholar 

  • Dan, J.C., Wada, S.K.: Studies on the acrosome. IV. The acrosome reaction in some bivalve spermatozoa. Biol. Bull. 109, 40–55 (1955)

    Google Scholar 

  • Daniels, E.W., Longwell, A.C., McNiff, J.M., Wolfgang, R.W.: Ultrastructure of oocytes from the American oyster Crassostrea virginica. Trans. Amer. micros. Soc. 92, 337–349 (1973)

    Google Scholar 

  • Fallon, J.F., Austin, C.R.: Fine structure of gametes of Nereis limbata (Annelida) before and after interaction. J. exp. Zool. 166, 225–242 (1967)

    Google Scholar 

  • Franklin, L.E.: An egg cell-membrane derivative on the vitelline membrane of annelid eggs. Exp. Cell Res. 43, 673–675 (1966)

    Google Scholar 

  • Galtsoff, P.S., Philpott, D.E.: Ultrastructure of the spermatozoon of the oyster, Crassostrea virginica. J. Ultrastruct. Res. 3, 241–253 (1960)

    Google Scholar 

  • Gould-Somero, M., Holland, L.: Oocyte differentiation in Urechis caupo (Echiura): A fine structural study. J. Morph. 147, 475–506 (1975a)

    Google Scholar 

  • Gould-Somero, M., Holland, L.: Fine structural investigation of the insemination response in Urechis caupo. Develop. Biol. 46, 358–369 (1975b)

    Google Scholar 

  • Gwynn, I., Jones, P.: On the egg investments and fertilization reaction in Pomatoceros triqueter (L.). An ultrastructural study. Z. Zellforsch. 113, 388–395 (1971)

    Google Scholar 

  • Hauschka, S.D.: Purification and characterization of Mytilus egg membrane lysin from sperm. Biol. Bull. 125, 363a (1963)

  • Hauschka, S.D.: Hyaline membrane lysis in Mytilus eggs. Biol. Bull. 127, 373a (1964)

  • Hinsch, G.W.: Microtubules in the sperm of the spider crab, Libinia emarginata. J. Ultrastruct. Res. 29, 525–534 (1969)

    Google Scholar 

  • Hinsch, G.W.: Penetration of the oocyte envelope by spermatozoa in the spider crab. J. Ultrastruct. Res. 35, 86–97 (1971)

    Google Scholar 

  • Humphreys, W.J.: Electron microscope studies on eggs of Mytilus edulis. J. Ultrastruct. Res. 7, 467–487 (1962)

    Google Scholar 

  • Humphreys, W.J.: The fine structure of cortical granules in eggs and gastrulae of Mytilus edulis. J. Ultrastruct. Res. 17, 314–326 (1967)

    Google Scholar 

  • Hylander, B.L., Summers, R.G.: An ultrastructural investigation of the spermatozoa of two ophiuroids, Ophiocoma echinata and Ophiocoma wendti: Acrosomal morphology and reaction. Cell Tiss. Res. 158, 151–168 (1975)

    Google Scholar 

  • Langreth, S.: Spermiogenesis in Cancer crabs. J. Cell Biol. 43, 575–603 (1969)

    Google Scholar 

  • Longo, F.J.: An ultrastructural analysis of polyspermy in the surf clam, Spisula solidissima. J. exp. Zool. 183, 153–180 (1973)

    Google Scholar 

  • Longo, F.J., Anderson, E.: Spermatogenesis in the surf clam Spisula solidissima with special reference to the formation of the acrosomal vesicle. J. Ultrastruct. Res. 27, 435–443 (1969a)

    Google Scholar 

  • Longo, F.J., Anderson, E.: Cytological aspects of fertilization in the lamellibranch, Mytilus edulis. I. Polar body formation and development of the female pronucleus. J. exp. Zool. 172, 69–96 (1969b)

    Google Scholar 

  • Longo, F.J., Anderson, E.: An ultrastructural analysis of fertilization in the surf clam, Spisula solidissima. I. Polar body formation and development of the female pronucleus. J. Ultrastruct. Res. 33, 495–514 (1970a)

    Google Scholar 

  • Longo, F.J., Anderson, E.: An ultrastructural analysis of fertilization in the surf clam, Spisula solidissima. II. Development of the male pronucleus and the association of the maternally and paternally derived chromosomes. J. Ultrastruct. Res. 33, 515–527 (1970b)

    Google Scholar 

  • Longo, F.J., Dornfeld, E.J.: The fine structure of spermatid differentiation in the mussel, Mytilus edulis. J. Ultrastruct. Res. 20, 462–480 (1976)

    Google Scholar 

  • Mabuchi, Y., Mabuchi, L: Acrosomal ATPase in starfish and bivalve mollusc spermatozoa. Exp. Cell Res. 82, 271–279 (1973)

    Google Scholar 

  • Metz, C.B.: Gamete surface components and their role in fertilization. In: Fertilization, comparative morphology, biochemistry and immunology (C.B. Metz, A. Monroy, eds.), pp. 163–236. New York: Academic Press 1967

    Google Scholar 

  • Moses, J.J.: Spermiogenesis in the crayfish (Procambarus clarkii). I. Structural characterization of the mature sperm. J. biophys. biochem. Cytol. 9, 222–228 (1961a)

    Google Scholar 

  • Moses, J.J.: Spermiogenesis in the crayfish (Procambarus clarkii). II. Description of stages. J. biophys. biochem. Cytol. 10, 301–333 (1961b)

    Google Scholar 

  • Mowbray, R.C., Brown, G.G.: Fertilization studies with egg sections of the horseshoe crab Limulus polyphemus. Biol. Reprod. 10, 62–68 (1974)

    Google Scholar 

  • Mowbray, R.C., Brown, G.G., Metz, C.B.: Cytological and immunological investigations of sperm-egg interactions in selected decapods (Crustacea) and Limulus polyphemus L. (Merostomata). Biol. Bull. 139, 313–320 (1970)

    Google Scholar 

  • Niijima, L., Dan, J.C.: The acrosome reaction in Mytilus edulis. I. Fine structure of the intact acrosome. J. Cell Biol. 25, 243–248 (1965a)

    Google Scholar 

  • Niijima, L., Dan, J.C.: The acrosome reaction in Mytilus edulis. II. Stages in the reaction observed in supernumerary and calcium-treated spermatozoa. J. Cell Biol. 25, 249–259 (1965b)

    Google Scholar 

  • Pasteels, J.J.: Aspects structuraux de la fécondation vus au microscope électronique. Arch. Biol. (Liège) 76, 463–509 (1965a)

    Google Scholar 

  • Pasteels, J.J.: Étude au microscope électronique de la réaction corticale. J. Embryol. exp. Morph. 13, 327–339 (1965b)

    Google Scholar 

  • Pasteels, J.J., Harven, E. de: Étude au microscope électronique du cortex de l'oeuf de Barnea Candida (Mollusque bivalve), son évolution au moment de la fécondation, de la maturation et de la segmentation. Arch. Biol. (Liège) 73, 465–490 (1962a)

    Google Scholar 

  • Pasteels, J.J., Harven, E. de: Étude au microscope électronique de spermatozoïde d'un mollusque bivalve, Barnea Candida. Arch. Biol. (Liège) 73, 445–463 (1962b)

    Google Scholar 

  • Paul, M.: The polyspermy block in eggs of Urechis caupo. Exp. Cell Res. 90, 137–142 (1975)

    Google Scholar 

  • Paul, M., Gould-Somero, M.: Evidence for a polyspermy block at the level of sperm-egg plasma membrane fusion in Urechis caupo. J. exp. Zool. 196, 105–112 (1976)

    Google Scholar 

  • Popham, J.D.: Comparative morphometrics of the acrosomes of the sperms of “externally” and “internally” fertilizing sperms of the shipworms (Teredinidae, bivalvia, mollusca). Cell Tiss. Res. 150, 291–297 (1974a)

    Google Scholar 

  • Popham, J.D.: The acrosome reaction in the sperm of the shipworm Bankia australis Calman (Bivalvia, mollusca). Cell Tiss. Res. 151, 93–101 (1974b)

    Google Scholar 

  • Popham, J.D.: The fine structure of the oocyte of Bankia australis (Teredinidae, bivalvia) before and after fertilization. Cell Tiss. Res. 157, 521–534 (1975)

    Google Scholar 

  • Popham, J.D., Dickson, M.R., Goddard, C.K.: Ultrastructural study of the mature gametes of two species of Bankia (Mollusca: Teredinidae). Aust. J. Zool. 22, 1–12 (1974c)

    Google Scholar 

  • Rebhun, L.I.: Electron microscope studies on the vitelline membrane of the surf clam Spisula solidissima. J. Ultrastruct. Res. 6, 107–122 (1962)

    Google Scholar 

  • Shoger, R.L., Brown, G.G.: Ultrastructural study of sperm-egg interactions of the horseshoe crab Limulus polyphemus (Merostomata: Xiphosura). J. submicr. Cytol. 2, 167–179 (1970)

    Google Scholar 

  • Summers, R., Hylander, B.L.: An ultrastructural analysis of early fertilization in the sand dollar Echinarachnius parma. Cell Tiss. Res. 150, 343–368 (1974)

    Google Scholar 

  • Summers, R.G., Hylander, B.L.: Species-specificity of acrosome reaction and primary gamete binding in echinoids. Exp. Cell Res. 96, 63–68 (1975)

    Google Scholar 

  • Summers, R.G., Hylander, B.L.: Primary gamete binding. Quantitative determination of its specificity in echinoid fertilization. Exp. Cell Res. 100, 190–194 (1976)

    Google Scholar 

  • Takashima, R., Takashima, Y.: Electron microscope studies on the fine structure of Nereis spermatozoa before and after the acrosomal reaction. Tokushima J. exp. Med. 10, 117–123 (1963)

    Google Scholar 

  • Tyler, A.: The biology and chemistry of fertilization. Amer. Nat. 99, 309–334 (1965)

    Google Scholar 

  • Vacquier, V.D., Payne, J.E.: Methods for quantitating sea urchin sperm-egg binding. Exp. Cell Res. 82, 227–235 (1973)

    Google Scholar 

  • Wada, S.K., Collier, J.R., Dan, J.C.: Studies on the acrosome. V. An egg membrane lysin from the acrosome of Mytilus edulis spermatozoa. Exp. Cell Res. 10, 168–180 (1956)

    Google Scholar 

  • Ziomek, C.A., Epel, D.: Polyspermy block of Spisula eggs is prevented by Cytochalasin B. Science 189, 139–141 (1975)

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomical Sciences, State University of New York at Buffalo, Buffalo, New York, USA

    B. L. Hylander & R. G. Summers

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  1. B. L. Hylander
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  2. R. G. Summers
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The assistance of Mr. B. Calloway in identifying and obtaining the organisms is gratefully acknowledged. This investigation was supported by NSF grants PCM 76-13459 and PCM 76-09654 and performed at the Bermuda Biological Station with instruments made available through the courtesy of Philips, Inc., DuPont-Sorvall, and L.K.B. Inc. Bermuda Biological Station Contribution No. 709

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Hylander, B.L., Summers, R.G. An ultrastructural analysis of the gametes and early fertilization in two bivalve molluscs, Chama macerophylla and Spisula solidissima with special reference to gamete binding. Cell Tissue Res. 182, 469–489 (1977). https://doi.org/10.1007/BF00219830

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