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The ultrastructure of spermatozoa and spermiogenesis in pyramidellid gastropods, and its systematic importance

Helgoländer Meeresuntersuchungen volume 42, pages 303–318 (1988)Cite this article

Abstract

Ultrastructural observations on spermiogenesis and spermatozoa of selected pyramidellid gastropods (species ofTurbonilla, Pyrgulina, Cingulina andHinemoa) are presented. During spermatid developement, the condensing nucleus becomes initially anterio-posteriorly compressed or sometimes cup-shaped. Concurrently, the acrosomal complex attaches to an electrondense layer at the presumptive anterior pole of the nucleus, while at the opposite (posterior) pole of the nucleus a shallow invagination is formed to accommodate the centriolar derivative. Midpiece formation begins soon after these events have taken place, and involves the following processes: (1) the wrapping of individual mitochondria around the axoneme/coarse fibre complex; (2) later internal metamorphosis resulting in replacement of cristae by paracrystalline layers which envelope the matrix material; and (3) formation of a glycogen-filled helix within the mitochondrial derivative (via a secondary wrapping of mitochondria). Advanced stages of nuclear condensation (elongation, transformation of fibres into lamellae, subsequent compaction) and midpiece formation proceed within a microtubular sheath (‘manchette’). Pyramidellid spermatozoa consist of an acrosomal complex (round to ovoid apical vesicle; column-shaped acrosomal pedestal), helically-keeled nucleus (short, 7–10 μm long, shallow basal invagination for axoneme/coarse fibre attachment), elongate helical midpiece (composed of axoneme, coarse fibres, paracrystalline and matrix materials, glycogen-filled helix), glycogen piece (length variable, preceeded by a dense ring structure at junction with midpiece). The features of developing and mature spermatozoa observed in the Pyramidellidae are as observed in opisthobranch and pulmonate gastropods indicating that the Pyramidelloidea should be placed within the Euthyneura/Heterobranchia, most appropriately as a member group of the Opisthobranchia.

Literature Cited

  • André, J., 1962. Contribution à la connaissance du chondriome. Étude de ses modifications ultrastructurales pendant spermiogenèse. — J. Ultrastruct. Res. (Suppl.)3, 1–185.

    Google Scholar 

  • Baccetti, B. & Afzelius, B. A., 1976. Biology of the sperm cell. Karger, Basel, 254 pp.

    Google Scholar 

  • Boss, K. J., 1982. Mollusca. In: Synopsis and classification of living organisms. Ed. by S. P. Parker. McGraw-Hill, New York,2, 945–1166.

    Google Scholar 

  • Buckland-Nicks, J. A. & Chia, F. S., 1976. Spermatogenesis of a marine snailLittorina sitkana. — Cell Tiss. Res.170, 455–475.

    Article  CAS  Google Scholar 

  • Climo, F. M., 1975. The anatomy ofGegania valkyrie Powell (Mollusca: Heterogastropoda: Mathildiade) with notes on other heterogastropods. — Jl R. Soc. N.Z.5, 275–288.

    Google Scholar 

  • Cox, L. R., 1960a. Gastropoda. General characteristics of Gastropoda. In: Treatise on invertebrate paleontology. Ed. by R. C. Moore. Univ. of Kansas Press, Lawrence, 84–169.

    Google Scholar 

  • Cox, L. R., 1960b. Thoughts on the classification of the Gastropoda. — Proc. malacol. Soc. Lond.33, 239–261.

    Google Scholar 

  • Dan, J. C. & Takaichi, S., 1979. Spermiogenesis in the pulmonate snailEuhadra hickonis. III. Flagellum formation. — Dev. Growth Differ.21, 71–86.

    Google Scholar 

  • Eckelbarger, K. J. & Eyster, L. S., 1981. An ultrastructural study on spermatogenesis in the nudibranch molluskSpurilla neapolitana. — J. Morph.170, 283–300.

    Google Scholar 

  • Franzén, Å., 1955. Comparative morphological investigations into the spermiogenesis among Mollusca. — Zool. Bidr. Uppsala.30, 399–456.

    Google Scholar 

  • Fretter, V., 1980. The evolution of some higher taxa in gastropods. — J. malacol. Soc. Aust.4, 226–227.

    Google Scholar 

  • Fretter, V. & Graham, A., 1949. The structure and mode of life of the Pyramidellidae, parasitic opisthobranchs. — J. mar. biol. Ass. U.K.48, 493–532.

    Google Scholar 

  • Fretter, V. & Graham, A., 1962. British prosobranch molluscs. Ray Society, London, 755 pp.

    Google Scholar 

  • Fretter, V., Graham, A. & Andrews, E. B., 1986. The prosobranch molluscs of Britain and Denmark. Part 9. Pyramidellacea. — J. moll. Stud. (Suppl.)16, 557–649.

    Google Scholar 

  • Ghiselin, M. T., 1966. Reproductive function and the phylogeny of opisthobranch gastropods. —Malacologia,3, 327–378.

    Google Scholar 

  • Golikov, A. N. & Starobogatov, Y. I., 1975. Systematics of prosobranch gastropods. — Malacologia,15, 185–232.

    Google Scholar 

  • Gosliner, T. M., 1981. Origins and relationships of primitive members of the Opisthobranchia (Mollusca: Gastropoda). — Biol. J. Linn. Soc.16, 197–225.

    Google Scholar 

  • Haszprunar, G., 1985a. The fine morphology of the osphradial sense organs of the Mollusca. II. Allogastropoda (Architectonicidae, Pyramidellidae). — Phil. Trans. R. Soc. (B).307, 497–505.

    Google Scholar 

  • Haszprunar, G., 1985b. The Heterobranchia — a new concept of the phylogeny of the higher Gastropoda. — Z. zool. Syst. Evolutionsforsch.23, 15–37.

    Google Scholar 

  • Haszprunar, G., 1985c. Zur Anatomie und systematischen Stellung der Architectonicidae (Mollusca, Allogastropoda). — Zool. Scr.14, 25–43.

    Google Scholar 

  • Haszprunar, G., 1985d. On the anatomy and systematic position of the Mathildidae (Mollusca, Allogastropoda). — Zool. Scr.14, 201–213.

    Google Scholar 

  • Healy, J. M., 1982a. An ultrastructural examination of developing and mature euspermatozoa inPyrazus ebeninus (Mollusca, Gastropoda, Potamididae). — Zoomorphology100, 157–175.

    Article  Google Scholar 

  • Healy, J. M., 1982b. Ultrastructure of spermiogenesis ofPhilippia (Psilaxis) oxytropis with special reference to the taxonomic position of the Architectonicidae (Gastropoda). — Zoomorphology101, 197–214.

    Article  Google Scholar 

  • Healy, J. M., 1982c. Ultrastructure of the spermatozoon of an opisthobranch,Tornatina sp. (Mollusca, Gastropoda, Retusidae). — Zool. Scr.11, 221–226.

    Google Scholar 

  • Healy, J. M., 1983a. An ultrastructural study of basommatophoran spermatozoa (Mollusca, Gastropoda). — Zool. Scr.12, 57–66.

    Google Scholar 

  • Healy, J. M., 1983b. Ultrastructure of euspermiogenesis in the mesogastropodStenothyra sp. (Prosobranchia, Rissoacea, Stenothyridae). — Zool. Scr.12, 203–214.

    Google Scholar 

  • Healy, J. M., 1984. The ultrastructure of gastropod spermatozoa and spermiogenesis. Ph. D. Thesis, Univ. of Queensland, Brisbane, 370 pp.

    Google Scholar 

  • Healy, J. M., 1986. Electron microscopic observations on the spermatozoa of a marine pulmonate slugOnchidium damelli (Gastropoda, Onchidiacea). — J. submicrosc. Cytol.18, 587–594.

    Google Scholar 

  • Healy, J. M., 1988. Sperm morphology and its systematic importance in the Gastropoda. — Malacol. Rev. (Suppl.)4 (In press.)

  • Healy, J. M. & Willan, R. C., 1984. Ultrastructure and phylogenetic significance of notaspidean spermatozoa (Mollusca, Gastropoda, Opisthobranchia). — Zool. Scr.13, 107–120.

    Article  Google Scholar 

  • Hyman, L., 1967. The invertebrates. McGraw-Hill, New York,6, 1–792.

    Google Scholar 

  • Knight, J. B., Batten, R. L., Yochelson, E., & Cox, L. R., 1960. Paleozoic and some Mesozoic Caenogastropoda and Opisthobranchia (supplement). In: Treatise on invertebrate paleontology. Ed. by R. C. Moore. Univ. of Kansas Press, Lawrence, 310–324.

    Google Scholar 

  • Kubo, M. & Ishikawa, M., 1981. Organization of the acrosome and helical structures in sperm of the aplysiidAplysia kurodai (Gastropoda, Opisthobranchia). — Differentiation20, 131–140.

    Google Scholar 

  • Medina, A., Moreno, J. & Lopez-Camps, J. L., 1985. Acrosome evolution inHypselodoris tricolor (Gastropoda: Nudibranchia). — J. submicrosc. Cytol.17, 403–411.

    Google Scholar 

  • Medina, A., Moreno, J. & Lopez-Camps, J. L., 1986. Nuclear morphogenesis during spermiogenesis in the nudibranch molluscHypselodoris tricolor (Gastropoda, Opisthobranchia). — Gamete Res.13, 159–171.

    Article  Google Scholar 

  • Morton, J. E. & Yonge, C. M., 1964. Classification and structure of the Mollusca. In: Physiology of mollusca. Ed. by K. M. Wilbur & C. M. Yonge. Acad. Press, New York. 2–58.

    Google Scholar 

  • Ponder, W. F., 1973.Pseudoskenella depressa gen. et sp. nov., an ectoparasite onGaleolaria. —Malacol. Rev.6, 119–123.

    Google Scholar 

  • Ponder, W. F. & Warén, A., 1988. Classification of the Caenogastropoda and Heterostropha — a list of the family-group and higher category names. — Malacol. Rev. (Suppl.)4 (In press.)

  • Robertson, R., 1973. The biology of the Architectonicidae: gastropods combining prosobranch and opisthobranch traits. — Malacologia.14, 215–220.

    Google Scholar 

  • Robertson, R., 1978. Spermatophores of six eastern North American pyramidellid gastropods and their systematic significance (with the new genusBoonea). — Biol. Bull. mar. biol. Lab., Woods Hole155, 360–382.

    Google Scholar 

  • Robertson, R., 1985. Four characters and the higher category systematics of gastropods. — Am. malcol. Bull.1, 1–22.

    Google Scholar 

  • Takaichi, S. & Dan, J. C., 1977. Spermiogenesis in the pulmonate snailEuhadra hickonis. I. Acrosome formation. — Dev. Growth Differ.19, 1–14.

    Article  Google Scholar 

  • Takaichi, S. & Sawada, N., 1973. An electron microscope study on sperm formation inEuhadra hickonis. — Mem. Ehime Univ. (B)7, 17–58.

    Google Scholar 

  • Taylor, D. W. & Sohl, N., 1962. An outline of gastropod classification. — Malacologia1, 7–32.

    Google Scholar 

  • Terakado, K., 1981. Chromatin arrangement and axis formation in the spermiogenesis of a pulmonate snail. — Dev. Growth Differ.23, 381–399.

    Article  Google Scholar 

  • Thiele, J., 1931. Handbuch der systematischen Weichtierkunde. Fischer, Jena,1, 1–376.

    Google Scholar 

  • Thompson, T. E., 1973. Euthyneuran and other molluscan spermatozoa. — Malacologia14, 167–206; 243–244.

    Google Scholar 

  • Wenz, W., 1938. Gastropoda 1. Allgemeiner Teil und Prosobranchia. In: Handbuch der Paläozoologie. Ed. by O. H. Schindewolf. Borntraeger, Berlin,6, 1–240.

    Google Scholar 

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Author notes

  1. John M. Healy

    Present address: Department of Zoology, University of Queesland, St. Lucia, 4067, Brisbane, Queensland, Australia

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  1. School of Biological Sciences (Zoology, A08), University of Sydney, 2006, New South, Wales, Australia

    John M. Healy

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Healy, J.M. The ultrastructure of spermatozoa and spermiogenesis in pyramidellid gastropods, and its systematic importance. Helgolander Meeresunters 42, 303–318 (1988). https://doi.org/10.1007/BF02366047

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Helgoland Marine Research

ISSN: 1438-3888

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