Skip to main content
SpringerLink
Log in

Polychaete sperm: phylogenetic and functional considerations

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The terminology used to describe the sperm of aquatic animals is discussed. It is argued that the use of the terms 'primitive′ and 'modified′ sperm confuse functional associations between sperm morphology and reproductive mode with perceived phylogenetic patterns. Therefore, terms describing sperm based on function should be preferred. This terminology is designed to avoid any a priori judgement of phylogenetic pattern. The various modes of sperm packaging and transfer in polychaetes are reviewed with regard to the morphology of the sperm. An example using an explicit phylogenetic hypothesis on the polychaete family Sabellidae is used to suggest ways to study the evolution of sperm structure, and to assess functional associations between sperm and reproductive mode.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ax, P., 1995. Multicellular animals. A new approach to the phylogenetic order in nature. Volume I. Springer, Berlin, 225 pp.

    Google Scholar 

  • Åkesson, B., 1973. Reproduction and larval morphology of five Ophryotrocha species (Polychaeta, Dorvilleidae). Zool. Scr. 2: 145–155.

    Google Scholar 

  • Bakke, T., 1990. Pogonophora. In Adiyodi, K. G. & R. G. Adiyodi (eds), Reproductive Biology of Invertebrates. Volume IV, Part B Fertilization, Development and Parental Care. John Wiley and Sons, Chichester: 37–48.

    Google Scholar 

  • Buckland-Nicks, J. & A. Scheltema, 1995. Was internal fertilization an innovation of early Bilateria? Evidence from sperm ultrastructure of a mollusc. Proc. R. Soc. Lond., ser. B 261: 11–18.

    Google Scholar 

  • Bührmann, C., W. Westheide & G. Purschke, 1996. Spermatogenesis and sperm ultrastructure in the interstitial syllid Petitia amphophthalma (Annelida, Polychaeta). Ophelia 45: 81–100.

    Google Scholar 

  • Carey, S. C., H. Felbeck & N. D. Holland, 1989. Observations of the reproductive biology of the hydrothermal vent tube worm Riftia pachyptila. Mar. Ecol. Prog. Ser. 52: 89–94.

    Google Scholar 

  • Degaulejac, B., M. Henry & N. Vicente, 1995. An ultrastructural study of gametogenesis of the marine bivalve Pinna nobilis (Linnaeus 1758). 2. Spermatogenesis. J. moll. Stud. 61: 393–403.

    Google Scholar 

  • Eeckhaut, I. & M. Jangoux, 1991. Fine structure of the spermatophore and intradermic penetration of sperm cells in Myzostoma cirriferum (Annelida, Myzostomida). Zoomorphology 111: 49–58.

    Google Scholar 

  • Ehlers, U., 1985. Das phylogenetische System der Plathelminthes. Gustav Fischer, Stuttgart, 317 pp.

    Google Scholar 

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

    Google Scholar 

  • Franzén, Å., 1973. The spermatozoon of Siboglinum. Acta zool. 54: 179–192.

    Google Scholar 

  • Franzén, Å. & S. A. Rice. 1988. Spermatogenesis, male gametes and gamete interaction. In Westheide, W. & C. O. Hermans (eds), The Ultrastructure of Polychaeta. Microfauna Mar. 4: 309–333.

  • Gardiner, S. L. & M. L. Jones, 1985. Ultrastructure of spermiogenesis in the vestimentiferan tube worm Riftia pachyptila (Pogonophora: Obturata). Trans. am. microsc. Soc. 104: 19–44.

    Google Scholar 

  • Giangrande, A., 1997. Polychaete reproduction patterns, life-cycles and life-histories: an overview. Oceanogr. mar. Biol. Ann. Rev. 35: 323–386.

    Google Scholar 

  • Giangrande, A. & A. Petraroli, 1994. Observations on reproduction and growth of Sabella spallanzanii (Polychaeta, Sabellidae) in the Mediterranean Sea. Mém. Mus. natn. Hist. nat., Paris 162: 51–56.

    Google Scholar 

  • Gidholm, L., 1965. On the morphology of the sexual stages, mating and egg-laying in Autolytus (Polychaeta). Zool. Bidr. Upps. 37: 1–44.

    Google Scholar 

  • Goodrich, E. S., 1930. A new hermaphrodite syllid. Q. J. Microsc. Sci. 73: 651–666.

    Google Scholar 

  • Gray, J. S., 1969. A new species of Saccocirrus (Archiannelida). Pac. Sci. 23: 238–251.

    Google Scholar 

  • Harvey, P. H. & M. Pagel, 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford, 239 pp.

    Google Scholar 

  • Haswell, W. A., 1914. Notes on the Histriobdellidae. Q. J. Micr. Sci. 59: 197–226.

    Google Scholar 

  • Herpin, R., 1925. La ponte et la développement chez une Annélide polychète sédentaire Nicolea zostericola. C. r. hebd. Séanc. Acad. Sci., Paris 180: 864–866.

    Google Scholar 

  • Hodgson, A. N. & F. S. Chia, 1993. Spermatozoon structure of some North American prosobranchs from the families Lottiidae (Patellogastropoda) and Fissurellidae (Archaeogastropoda). Mar. Biol. 116: 97–101.

    Google Scholar 

  • Höglund, J., 1989. Size and plumage dimorphism in lek-breeding birds: A comparative analysis. Am. Nat. 134: 72–87.

    Google Scholar 

  • Hsieh, H.-L., 1997. Self-fertilization – a potential fertilization mode in an estuarine sabellid polychaete. Mar. Ecol. Progr. Ser. 147: 143–148.

    Google Scholar 

  • Hsieh, H.-L. & J. L. Simon, 1990. The sperm transfer system in Kinbergonuphis simoni (Polychaeta: Onuphidae). Biol. Bull. 178: 85–93.

    Google Scholar 

  • Jägersten, G., 1972. Evolution of the Metazoan Life Cycle. Academic Press, New York.

    Google Scholar 

  • Jamieson, B. G. M., 1991a. Fish Evolution and Systematics: Evidence from Spermatozoa. Cambridge University Press, Cambridge, 319 pp.

    Google Scholar 

  • Jamieson, B. G. M., 1991b. Ultrastructure and phylogeny of crustacean spermatozoa. Mem. Q'ld Mus. 31: 109–142.

    Google Scholar 

  • Jamieson, B. G. M., B. A. Afzelius & A. Franzén, 1985. Ultrastructure of the acentriolar, aflagellate spermatozoa and the eggs of Histriobdella homari and Stratiodrilus novaehollandiae (Histriobdellidae, Polychaeta). J. Submicr. Cyt. 17: 363–380.

    Google Scholar 

  • Jamieson, B. G. M. & G. W. Rouse, 1989. The spermatozoa of the Polychaeta (Annelida): An ultrastructural review. Biol. Rev. 64: 93–157.

    Google Scholar 

  • Jones, M. L., 1981. Riftia pachyptila, new genus, new species, the vestimentiferan worm from the Galápagos Rift geothermal vents (Pogonophora). Proc. biol. Soc. Wash. 93: 1295–1313.

    Google Scholar 

  • Jones, M. L. & S. L. Gardiner, 1985. Light and scanning electron microscopic studies of spermatogenesis in the vestimentiferan tube worm Riftia pachyptila (Pogonophora: Obturata). Trans. am. microsc. Soc. 104: 1–18.

    Google Scholar 

  • Kluge, A. G., 1989. A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst. Zool. 38: 7–25.

    Google Scholar 

  • Kluge, A. G. & A. J. Wolf, 1993. Cladistics: what's in a word? Cladistics 9: 183–199.

    Google Scholar 

  • Kuper, M. & W. Westheide, 1997a. Ultrastructure of the male reproductive organs in the interstitial annelid Sphaerosyllis hermaphrodita (Polychaeta, Syllidae). Zoomorphology 117: 13–22.

    Google Scholar 

  • Kuper, M. & W. Westheide, 1997b. Sperm ultrastructure and spermatogenesis in the interstitial polychaete Sphaerosyllis hermaphrodita (Syllidae: Exogoninae). Invert. Reprod. Dev. 32: 189–200.

    Google Scholar 

  • Nielsen, C., 1995. Animal Evolution. Oxford University Press, Oxford, 467 pp.

    Google Scholar 

  • Okuda, S., 1946. Studies on the development of Annelida Polychaeta I. J. Fac. Sci. Hokkaido Imp. Uni., Ser. VI 9: 115–219.

    Google Scholar 

  • Olive, P. J. W., 1983. Annelida-Polychaeta. In Adiyodi, K. G. & R. G. Adiyodi (eds), Reproductive Biology of Invertebrates. Volume II: Spermatogenesis and Sperm Function. Wiley, Chichester: 321–342. 224

    Google Scholar 

  • Pfannenstiel, H.-D. & C. Grünig, 1990. Spermatogenesis and sperm ultrastructure in the polychaete genus Ophryotrocha (Dorvilleidae). Helgoländer wiss. Meeresunters. 44: 159–171.

    Google Scholar 

  • Purschke, G. & C. Jouin, 1988. Anatomy and ultrastructure of the ventral pharyngeal organs of Saccocirrus (Saccocirridae) and Protodriloides (Protodriloidae fam. n.) with remarks on the phylogenetic relationships within Protodrilida (Annelida: Polychaeta). J. Zool. (Lond.) 215: 405–432.

    Google Scholar 

  • Retzius, G., 1904. Zur Kenntnis der Spermien der Evertebraten. I. Biologische Untersuchungen N.F. 11: 1–32.

    Google Scholar 

  • Retzius, G., 1905. Zur Kenntnis der Spermien der Evertebraten. II. Biologische Untersuchungen N.F. 11: 79–102.

    Google Scholar 

  • Rice, S. A., 1978. Spermatophores and sperm transfer in spionid polychaetes. Trans. am. microsc. Soc. 97: 160–170.

    Google Scholar 

  • Rice, S. A., 1981. Spermatogenesis and sperm ultrastructure in three species of Polydora and in Streblospio benedicti (Polychaeta: Spionidae). Zoomorphology 97: 1–16.

    Google Scholar 

  • Rice, S. A., 1987. Reproductive biology, systematics and evolution in the polychaete family Alciopidae. Bull. biol. Soc. Wash. 7: 114–127.

    Google Scholar 

  • Rice, S. A., 1992. Polychaeta: Spermatogenesis and spermiogenesis. In Harrison, F. W. & S. L. Gardiner (eds), Microscopic Anatomy of Invertebrates Volume 7: Annelida. Wiley-Liss, New York: 129–151

    Google Scholar 

  • Rice, S. A. & K. J. Eckelbarger, 1989. An ultrastructural investigation of spermatogenesis in the holopelagic polychaetes Vanadis formosa and Krohnia lepidota (Polychaeta: Alciopidae). Biol. Bull. 176: 123–134.

    Google Scholar 

  • Richards, S. L., 1970. Spawning and reproductive morphology of Scolelepis squamata (Spionidae: Polychaeta). Can. J. Zool. 48: 1369–1379.

    Google Scholar 

  • Ridley, M., 1983. The explanation of organic diversity: the comparative method and adaptations for mating. Oxford University Press, 272 pp.

  • Ridley, M., 1986. The number of males in a primate troop. Anim. Behav. 34: 1848–1858.

    Google Scholar 

  • Rouse, G. W., 1992a. Ultrastructure of sperm and spermathecae in Micromaldane spp. (Polychaeta: Capitellida: Maldanidae). Mar. Biol. 113: 155–168.

    Google Scholar 

  • Rouse, G. W., 1992b. Ultrastructure of the spermathecae of Parafabricia ventricingulata and three species of Oriopsis (Polychaeta: Sabellidae). Acta zool. 73: 141–151.

    Google Scholar 

  • Rouse, G. W., 1995. Is sperm ultrastructure useful in polychaete systematics? An example using 20 species of the Fabriciinae (Sabellidae, Polychaeta). Acta zool. 76: 57–74.

    Google Scholar 

  • Rouse, G. W., 1996a. A new species of Perkinsiana (Sabellidae, Polychaeta) from Papua New Guinea; with a description of larval development. Ophelia 45: 101–114.

    Google Scholar 

  • Rouse, G. W., 1996b. Variability of sperm storage by females in the Sabellidae and Serpulidae (Polychaeta). Zoomorphology 116: 179–193.

    Google Scholar 

  • Rouse G. W., 1999. Polychaeta, including Pogonophora and Myzostomida. In Adiyodi, K. G. & R. G. Adiyodi, (series eds), Reproductive Biology of Invertebrates, Vol. 9. In Jamieson, B. B. G. M. (ed.) Progress in Male Gamete Ultrastructure and Phylogeny. John Wiley, Chichester: in press.

  • Rouse, G. W. & K. Fitzhugh, 1994. Broadcasting fables: Is external fertilization really primitive? Sex, size and larvae in sabellid polychaetes. Zool. Scr. 23: 271–312.

    Google Scholar 

  • Rouse, G. W. & B. G. M. Jamieson, 1987. An ultrastructural study of the spermatozoa of the polychaetes Eurythoe complanata (Amphinomidae), Clymenella sp. and Micromaldane sp. (Maldanidae), with definition of sperm types in relation to reproductive biology. J. Submicrosc. Cytol. 19: 573–584.

    Google Scholar 

  • Rouse, G. W. & D. McHugh, 1994. Ultrastructure of spermatids and spermatozoa in Ramex californiensis and Nicolea zostericola (Terebellidae; Polychaeta). Ophelia 39: 225–238.

    Google Scholar 

  • Scheltema, A. H., 1996. Phylogenetic position of Sipuncula, Mollusca and the progenetic Aplacophora. In Taylor, J. (ed.), Origin and Evolutionary Radiation of the Mollusca. Oxford University Press, Oxford: 53–58.

    Google Scholar 

  • Schroeder, P. C., 1989. Annelida-Polychaeta. In Adiyodi, K. G. & R. G. Adiyodi (eds), Reproductive Biology of Invertebrates. Volume IV Part A: Fertilization, Development and Parental Care. Wiley and Sons Ltd., Chichester: 383–442.

    Google Scholar 

  • Schroeder, P. C. & C. O. Hermans, 1975. Annelida: Polychaeta. In Giese, A. C. & J. S. Pearse (eds), Reproduction of Marine Invertebrates. III. Annelids and Echiurans. Academic Press, New York: 1–213.

    Google Scholar 

  • Simon, J. L., 1967. Reproduction and larval development of Spio setosa (Spionidae; Polychaeta). Bull. mar. Sci. 17: 398–431.

    Google Scholar 

  • Sordino, P. & M. C. Gambi, 1992. Prime osservazioni sulla biologia riproduttiva e sul ciclo vitale di Branchiomma luctuosum (Grube 1869) (Polychaeta Sabellidae). Oebalia Suppl. 17: 425–427.

    Google Scholar 

  • Sousa, M. & E. Oliveira, 1994. An ultrastructural study of Crassostrea angulata (Mollusca, Bivalvia) spermatogenesis. Mar. Biol. 120: 545–551.

    Google Scholar 

  • Southward, E. C. & K. A. Coates, 1989. Sperm masses and sperm transfer in a vestimentiferan, Ridgeia piscesae Jones 1985 (Pogonophora Obturata). Can. J. Zool. 67: 2776–2781.

    Google Scholar 

  • Stecher, H. J., 1968. Zur Organisation und Fortpflanzung von Pisione remota (Southern). Z. Morph. Tiere 61: 347–410.

    Google Scholar 

  • Sundberg, P. & R. Hylbom, 1994. Phylogeny of the nemertean subclass Palaeonemertea (Anopla, Nemertea). Cladistics 10: 347–402.

    Google Scholar 

  • Van Dover, C. L., 1994. In situ spawning of hydrothermal vent tubeworms (Riftia pachyptila). Biol. Bull. 186: 134–135.

    Google Scholar 

  • Westheide, W., 1984. The concept of reproduction in polychaetes with small body size: adaptations in interstitial species. Fortsch. Zool. 29: 265–287.

    Google Scholar 

  • Westheide, W., 1988a. Genital organs. In Westheide, W. & C.O. Hermans (eds), The Ultrastructure of Polychaeta. Mikrofauna Mar. 4: 263–279.

  • Westheide, W., 1988b. The ultrastructure of the spermatozoon of Pisione remota (Annelida: Pisionidae) and its transformation in the receptaculum seminis. J. Submicrosc. Cytol. Pathol. 20: 169–178.

    Google Scholar 

  • Westheide, W., G. Purschke & W. Mangerich, 1994. Sinohesione genitaliphora gen. et sp. n. (Polychaeta, Hesionidae), an interstitial annelid with unique dimorphous external genital organs. Zool. Scr. 23: 95–105.

    Google Scholar 

  • Wilson, W. H., 1991. Sexual reproductive modes in polychaetes: classification and diversity. Bull. mar. Sci. 48: 500–516.

    Google Scholar 

  • Young, C. M., E. Vásquez, A. Metaxas & P. A. Tyler, 1996. Embryology of vestimentiferan tube worms from deep-sea methane/ sulphide seeps. Nature 381: 514–516.

    Google Scholar 

  • Zal, F., D. Desbruyères & C. Jouin-Toulmond, 1994. Sexual dimorphisms in Paralvinella grasslei, a polychaete annelid from deep-sea hydrothermal vents. C. r. Acad. Sci., Paris 317: 42–48.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biological Sciences, University of Sydney, N.S.W, 2006, Australia

    G. W. Rouse

Authors
  1. G. W. Rouse
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rouse, G.W. Polychaete sperm: phylogenetic and functional considerations. Hydrobiologia 402, 215–224 (1999). https://doi.org/10.1023/A:1003700827759

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1003700827759

Search

Navigation