Skip to main content
Log in

Fertilization in Oikopleura dioica (Tunicata, Appendicularia): Acrosome reaction, cortical reaction and sperm-egg fusion

  • Published:
Zoomorphology Aims and scope Submit manuscript

Summary

Fine structural changes in the egg and sperm are described during gamete interaction in Oikopleura dioica, an appendicularian tunicate. The unfertilized egg has a vitelline layer 80 nm thick and a perivitelline space about 5 μm wide. In the peripheral cytoplasm are a few cortical granules 0.6×0.7 μm in diameter and areas rich in parallel cisternae of rough endoplasmic reticulum alternating with areas rich in long mitochondria. In the deeper cytoplasm the predominant organelles are multivesicular bodies. From 25 s to 60 s after insemination, the egg transiently elongates, although with no obvious cytoplasmic rearrangement, and the egg surface becomes bumpy. During this interval sperm enter the egg, and the cortical granules undergo exocytosis. After expulsion into the perivitelline space, the cortical granule contents do not appear to change their shape or blend with the vitelline layer, which neither elevates further nor loses its ability to bind sperm. On encountering the egg, the sperm undergoes an acrosome reaction involving exocytosis of the acrosome and production of an acrosomal tubule. The acrosomal contents bind the sperm to the vitelline layer, and the posterior portion of the acrosomal membrane and the anterior portion of the nuclear envelope evaginate together to form an acrosomal tubule, which fuses with the egg plasma membrane to form a fertilization cone. By 45 s after insemination, the sperm nucleus, centriole, mitochondrion and at least the anterior portion of the axoneme are within the fertilization cone. By 60 s sperm entry is complete. In having eggs with a cortical reaction and sperm with an acrosome reaction, O. dioica resembles echinoderms and enteropneusts and differs markedly from ascidian tunicates, which lack both these features. The relatively unmodified pattern of gamete interaction in O. dioica in comparison with the highly modified pattern in ascidians is difficult to reconcile with the neoteny theory that appendicularians have evolved via ascidian ancestors. The present results are more consistent with the idea that an appendicularian-like ancestor gave rise to ascidians.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Afzelius BA (1956) The ultrastructure of the cortical granules and their products in the sea urchin egg as studied with the electron microscope. Exp Cell Res 10:257–285

    Google Scholar 

  • Baccetti B (1985) Evolution of the sperm cell. In: Metz CB and Monroy A (eds) Biology of Fertilization, Vol 2: Biology of the sperm. Academic Press, Orlando, pp 3–58

    Google Scholar 

  • Baccetti B (1986) News on sperm evolution. Dev Growth Differ 28 suppl:27–28

    Google Scholar 

  • Baccetti B, Burrini AG, Dallai R (1972) The spermatozoon of Branchiostoma lanceolatum. J Morphol 136:221–226

    Google Scholar 

  • Brooks WK (1893) The genus Salpa. Mem Biol Lab John Hopkins University 2:1–396 57 plates. Johns Hopkins Press, Baltimore

    Google Scholar 

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

    Google Scholar 

  • Cerfontaine P (1906) Recherches sur le développement de l'Amphioxus. Arch Biol 22:229–418

    Google Scholar 

  • Colombera D, Fenaux R (1973) Chromosome form and number in the Larvacea. Boll Zool 40:347–353

    Google Scholar 

  • Colwin LH, Colwin AL (1963a) Role of the gamete membranes in fertilization in Saccoglossus kowalevskii (Enteropneusta). I. The acrosomal region and its changes in early stages of fertilization. J Cell Biol 19:477–500

    Google Scholar 

  • Colwin LH, Colwin AL (1963b) Role of the gamete membranes in fertilization in Saccoglossus kowalevskii (Enteropneusta). II. Zygote formation by gamete membrane fusion. J Cell Biol 19:501–518

    Google Scholar 

  • Conklin EG (1905) The organization and cell-lineage of the ascidian. J Acad Nat Sci Philadelphia 2nd Ser. 13:1–119

    Google Scholar 

  • Crowther RJ, Whittaker JR (1986) Differentiation without cleavage: multiple cytospecific ultrastructural expressions in individual one-celled ascidian embryos. Dev Biol 117:114–126

    Google Scholar 

  • De Felice LJ, Kell MJ (1987) Sperm-activated currents in ascidian oocytes. Dev Biol 119:123–128

    Google Scholar 

  • Fenaux R (1963) Écologie et biologie des Appendiculaires Méditerranéens (Villefranche-sur-mer). Vie Milieu suppl. 16:1–142

    Google Scholar 

  • Fenaux R (1967) Les appendiculaires de mers d'Europe et du bassin Méditerranéen. Faune de l'Europe et du Bassin Méditerranéen 2. Masson et Cie (eds) Paris, 113 pp

  • Fenaux R (1976) Cycle vital d'un appendiculaire Oikopleura dioica Fol 1872. Ann Inst Océanogr (Paris) 52:89–101

    Google Scholar 

  • Fenaux R (1977) Life history of the appendicularians (Genus Oikopleura). Proc Symp Warm Water Zool Spl. Publ UNESCO/N. 10:89–101

    Google Scholar 

  • Fenaux R (1985) Rhythm of secretion of oikopleurid's houses. Bull Mar Sci 37:498–503

    Google Scholar 

  • Fenaux R, Bedo A, Gorsky G (1986) Premières données sur la dynamique d'une population d'Oikopleura dioica Fol, 1872 (Appendiculaire) en élevage. Can J Zool 64:1745–1749

    Google Scholar 

  • Flood PR, Afzelius BA (1978) The spermatozoon of Oikopleura dioica Fol (Larvacea, Tunicata). Cell Tiss Res 191:27–37

    Google Scholar 

  • Fol H (1872) Etudes sur les appendiculaires du détroit de Messine. Mem Soc Phys Genève 21:445–499

    Google Scholar 

  • Franzén Å (1958) On sperm morphology and acrosome filament formation in some Annelida, Echiuroidea, and Tunicata. Zool Bidrag Uppsala 33:1–28

    Google Scholar 

  • Franzén Å (1983) Urochordata. In: Adiyodi KG and Adiyodi RG (eds). Reproductive Biology of Invertebrates. Vol 2 Spermatogenesis and Sperm Function. John Wiley and Sons, Chichester, pp 621–632

    Google Scholar 

  • Fukumoto M (1983) Fine structure and differentiation of the acrosome-like structure in the solitary ascidians Pyura haustor and Styela plicata. Dev Growth Differ 25:503–515

    Google Scholar 

  • Fukumoto M (1984a) The apical structure in Perophora annectens (Tunicate) spermatozoa: Fine structure, differentiation and possible role in fertilization. J Cell Sci 66:175–187

    Google Scholar 

  • Fukumoto M (1984b) Fertilization in ascidians: Acrosome fragmentation in Ciona intestinalis spermatozoa. J Ult Res 87:252–262

    Google Scholar 

  • Fukumoto M (1986) The acrosome in ascidians. I. Pleurogona. Int J Invertebr Reprod 10:335–346

    Google Scholar 

  • Galt CP (1972) Development of Oikopleura dioica (Urochordata: Larvacea): Ontogeny of behavior and of organ systems related to construction and use of the house. Ph. D. dissertation. Univ. Washington, Seattle, 83 pp

    Google Scholar 

  • Garstang W (1928) The morphology of the Tunicata and its bearings on the phylogeny of the Chordata. Quart J Microsc Sci 72:51–187

    Google Scholar 

  • Ghiselin MT, Field KG, Olsen GJ, Lane DJ, Raff RA, Raff EC, Pace NR (1986) A phylogenetic tree of chordate subphyla based on 18s ribosomal RNA sequences. Am Zool 26:92A (abstract)

    Google Scholar 

  • Gorsky G, Fenaux R, Palazzuoli I (1986) Une methode de maintien en suspension des organismes zooplanctoniques fragiles. Rapp Comm Int Mer Médit 30.2.204. P III:21–22

    Google Scholar 

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

    Google Scholar 

  • Grygier MJ (1982) Sperm morphology in Ascothoracida (Crustacea: Maxillopoda): confirmation of generalized nature and phylogenetic importance. Int J Invert Reprod 4:323–332

    Google Scholar 

  • Guraya SS (1982) Recent progress in the structure, origin, composition, and function of cortical granules in animals. Int Rev Cytol 78:257–360

    Google Scholar 

  • Harvey EB (1956) The American Arbacia and other sea urchins. Princeton Univ. Press, Princeton 298 pp

    Google Scholar 

  • Hedwig M, Schäfer W (1986) Vergleichende Untersuchungen zur Ultrastrukture und zur phylogenetischen Bedeutung der Spermien der Scyphozoa. Z Zool Syst und Evol Forsch 24:109–122

    Google Scholar 

  • Herdman WA (1888) Report upon the Tunicata collected during the voyage of HMS Challenger during the years 1873–1876. Part III. Report on the scientific results of the voyage of HMS Challenger. XXVII, part LXXVI

  • Honegger TG (1986) Fertilization in ascidians: Studies on the egg envelope, sperm and gamete interactions in Phallusia mammillata. Dev Biol 118:118–128

    Google Scholar 

  • Hopkins CR (1986) Membrane boundaries involved in the uptake and intracellular processing of cell-surface receptors. Trends in Biochem Sci 11:473–477

    Google Scholar 

  • Jaffe LA, Gould M (1985) Polyspermy preventing mechanisms. In: Metz CB and Monroy A (eds) Biology of fertilization, Vol 3, Academic Press, Orlando, pp 223–250

    Google Scholar 

  • Jefferies RPS (1987) The ancestry of the vertebrates. British Museum, London, pp 1–376

    Google Scholar 

  • Julin C (1912) Research sur le développement embryonnaire de Pyrosoma giganteum Les. Zool Jahrb Suppl 15:775–863

    Google Scholar 

  • Korotneff A (1905) Zur Embryologie von Pyrosoma. Mitt Zool Sta Neapel 17:295–311

    Google Scholar 

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

    Google Scholar 

  • Lambert CC (1986) Fertilization-induced modification of chorion N-acetylglucosamine groups blocks polyspermy in ascidian eggs. Dev Biol 116, 168–173

    Google Scholar 

  • Lambert CC, Lambert GL (1981) Formation of the block to polyspermy in ascidian eggs. J Exp Zool 217:291–295

    Google Scholar 

  • La Spina D'Anna R (1974) Light and electron microscopic study of unfertilized egg of Ascidia malaca (Tunicata). Acta Embryol Exp 1:3–17

    Google Scholar 

  • Lohmann H (1933) Erster Unterstamm der Chordata. Tunicata = Manteltiere. Allgemeine Einleitung in die Naturgeschichte der Tunicata. In: Kukenthal W and Krumbach T (eds): Handbuch der Zoologie. 5 pt. 2, pp 3–14

  • Longo FJ, Anderson E (1969) Sperm differentiation in the sea urchins Arbacia punctulata and Strongylocentrotus purpuratus. J Ult Res 27:486–509

    Google Scholar 

  • Miller RL (1975) Chemotaxis of the spermatozoa of Ciona intestinalis. Nature (London) 254:244–245

    Google Scholar 

  • Miller RL, King KR (1983) Sperm chemotaxis in Oikopleura dioica Fol 1872 (Urochordata, Larvacea). Biol Bull 165:419–428

    Google Scholar 

  • Pictet C (1891) Recherches sur la spermatogénèse chez quelques invertébrés de la Méditerranée. Mitt Zool Sta Neapel 10:75–152

    Google Scholar 

  • Remane A, Storch V, Welsch U (1976) Systematische Zoologie, Stämme des Tierreichs. Fischer, Stuttgart, 499 pp

    Google Scholar 

  • Reverberi G, De Leo G (1972) The oocyte of Amphioxus examined by the electron microscope. Acta Embryol Exp 1972:65–84

    Google Scholar 

  • Retzius G (1905) Zur Kenntnis der Spermien der Evertebraten II. Biol Untersuchungen N.F. 12:79–115

    Google Scholar 

  • Sawada T, Osanai K (1981) The cortical contraction related to the ooplasmic segregation in Ciona intestinalis eggs. Wilhelm Roux Arch 190:208–214

    Google Scholar 

  • Sawada T, Osanai K (1985) Distribution of actin filaments in fertilized egg of the ascidian Cona intestinalis. Dev Biol 111:260–265

    Google Scholar 

  • Schmidt H, Zissler D (1979) Die Spermien der Anthozoen und ihre phylogenetische Bedeutung. Zoologica Stuttgart 129:1–97

    Google Scholar 

  • Seeliger O (1885) Die Entwicklungsgeschichte der socialen Ascidien. Jenaische Zeitschr Naturwiss 18:45–110 + 528–596

    Google Scholar 

  • Shimizu T (1984) Dynamics of the actin microfilament system in the Tubifex egg during ooplasmic segregation. Dev Biol 106:414–426

    Google Scholar 

  • Spudich A, Wrenn JT, Wessells NK (1988) Unfertilized sea urchin eggs contain a discrete cortical shell of actin that is subdivided into two organizational states. Cell Motility Cytoskeleton 9:85–96

    Google Scholar 

  • Tilney LG (1976) The polymerization of actin. II. How non-filamentous actin becomes non-randomly distributed in sperm. Evidence for the association of this actin with membranes. J Cell Biol 69:51–72

    Google Scholar 

  • Tilney LG (1985) The acrosomal reaction. In: Metz CB and Monroy A (eds) Biology of fertilization, Vol 2: Biology of the sperm. Academic Press, Orlando, pp 157–213

    Google Scholar 

  • Uljanin B (1884) Die Arten der Gattung Dioliolum im Golfe von Neapel und den angrenzenden Meeresabschnitten. Fauna und Flora des Golfes von Neapel Monographie 140 pp

  • Ursprung H, Schabtach E (1965) Fertilization in tunicates: loss of the paternal mitochondrion prior to sperm entry. J Exp Zool 159:379–384

    Google Scholar 

  • Wall DA, Patel S (1987) Multivesicular bodies play a key role in vitellogenin endocytosis by Xenopus oocytes. Dev Biol 119:275–289

    Google Scholar 

  • Wirth U (1984) Die Struktur der Metazoen-Spermien und ihre Bedeutung für die Phylogenetik. Verh Naturwiss Ver Hamburg 27:295–362

    Google Scholar 

  • Zalokar M, Sardet C (1984) Tracing of cell lineage in embryonic development of Phallusia mammillata (Ascidia) by vital staining of mitochondria. Dev Biol 102:195–205

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Holland, L.Z., Gorsky, G. & Fenaux, R. Fertilization in Oikopleura dioica (Tunicata, Appendicularia): Acrosome reaction, cortical reaction and sperm-egg fusion. Zoomorphology 108, 229–243 (1988). https://doi.org/10.1007/BF00312223

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00312223

Keywords

Navigation