Sperm ultra-structure of <i>Odontosyllis ctenostoma</i> (Polychaeta: Syllidae) with inferences on syllid phylogeny and reproductive biology

Adriana Giangrande; Miriam Gherardi; Elena Lepore; Maria Mercurio; Margherita Sciscioli

doi:10.3989/scimar.2008.72n3421

Authors

Adriana Giangrande Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento
Miriam Gherardi Dipartimento di Zoologia, Università di Bari
Elena Lepore Dipartimento di Zoologia, Università di Bari
Maria Mercurio Dipartimento di Zoologia, Università di Bari
Margherita Sciscioli Dipartimento di Zoologia, Università di Bari

DOI:

https://doi.org/10.3989/scimar.2008.72n3421

Keywords:

sperm morphology, ultrastructure, Polychaeta, Eusyllinae, reproduction, phylogeny

Abstract

The analysis of the complex reproductive patterns of Syllidae may drastically change the taxonomic hierarchy of the family. To further contribute to the knowledge of Syllidae we have described the sperm ultra-structure and some steps of spermiogenesis of Odontosyllis ctenostoma Claparède, 1868, the first non interstitial eusylline investigated. The mature sperm has a bell-shaped acrosome and contains electron-dense granular material and thin filaments. The barrel-shaped nucleus bears two depressions: one anterior facing the acrosome and the other posterior partially containing the distal centriole and up to six mitochondria. Odontosyllis ctenostoma spermatozoa can be ascribed to the ect-aquasperm type typical of species practising external fertilisation. This morphology is not in complete accordance either with the particular brood protection reported for the species or the egg size. The sperm is similar to those of the Syllinae species thus far investigated, but the acrosome resembles that of the exogonine spermatid. Some authors consider Odontosyllis to be phylogenetically closer to Syllinae, though it shares epigamy with Exogoninae. Others have hypothesised that the exogonine sperm could have been derived from sylline sperm by simplification. In our hypothesis this could have happened through a gradual passage from an Odontosyllis-like eusylline ancestor.

Downloads

Download data is not yet available.

References

Bührmann, C., W. Westheide and G. Purschke. – 1996. Spermatogenesis and sperm ultra-structure in the interstitial syllid Petitia amphophtalma (Annelida, Polychaeta). Ophelia, 45: 201-211.

Daly, J.M. – 1975. Reversible epitoky in the life history of the polychaete Odontosyllis polycera (Schmarda, 1861). J. Mar. Biol. Ass. UK. 55: 327-344.

Fischer, A. and U. Fischer. – 1995. On the life-style and the lifecycle of the luminescent polychaete Odontosyllis enopla (Annelida: Polychaeta). Invertebr. Biol., 114(3): 236-247. doi:10.2307/3226878

Franke, H. D. – 1999. Reproduction of Syllidae (Annelida: Polychaeta). Hydrobiologia, 402: 39-55. doi:10.1023/A:1003732307286

Franke, H.D. and H.D. Pfannenstiel. – 1984. Some aspects of endocrine control of polychaete reproduction. In: A. Fischer and H.D. Pfannenstiel (eds.), Polychaete Reproduction. Fortschr. Zool., 29: 53-72.

Franzén, Å. – 1956. On spermiogenesis, morphology and the spermatozoon, and biology of fertilisation among invertebrates. Zool. Bijdr., 31: 355-482.

Franzén, Å. – 1974. Sperm structure in some Polychaeta. In: B.A. Afzelius (ed.), The Functional Anatomy of the Spermatozoon, pp. 267-278. Pergamon Press, Oxford.

Franzén, Å. – 1982. Ultra-structure of spermatids and spermatozoa in three polychaetes with modified biology of reproduction: Autolytus sp, Chitinopoma serrula and Capitella capitata. Int. J. Invertebr. Reprod., 5: 185-200.

Garwood, P.R. – 1991. Reproduction and the classification of the family Syllidae (Polychaeta). Ophelia, Suppl., 5: 81-87.

Giangrande, A. – 1997. Polychaete reproductive patterns, life cycle and life histories: an overview. Oceanogr. Mar. Biol. Annu. Rev., 35: 323-386.

Giangrande, A., M. Sciscioli, E. Lepore, M. Mastrodonato, P. Lupetti and R. Dallai. – 2002. Sperm ultra-structure and spermiogenesis in two Exogone species (Polychaeta, Syllidae, Exogoninae). Invertebr. Biol., 121(4): 339-349.

Gravier C. and J.L. Dantan. – 1928. Peches nocturnes a la lumière dans la Baie d’Alger. Annélides polychètes. Ann. Inst. Océanogr. Paris Nouv. ser., 5: 1-187

Hardege, J.D., Müller, C., Beckmann, M., H.D. Bartels-Hardege and M.G. Bentley. – 1998. Timing of reproduction in marine polychaetes: the role of sex pheromones. Ecoscience, 5: 395-404.

Heacox, A.E. and P.C. Schroeder. – 1981a. A light- and electronmicroscopic investigation of gametogenesis in Typosyllis pulchra (Berkeley and Berkeley) (Polychaeta: Syllidae) I. Gonad structure and spermatogenesis. Cell Tissue Res., 218: 623-639.

Heacox, A.E. and P.C. Schroeder. – 1981b. A light- and electron-microscopic investigation of gametogenesis in Typosyllis pulchra (Berkeley and Berkeley) (Polychaeta: Syllidae) II. Oogenesis. Cell Tissue Res., 218: 641-658.

Jamieson, B.G.M. and G.W. Rouse. – 1989. The spermatozoa of the Polychaeta (Annelida): an ultrastructural review. Biol. Rev. Camb. Philos. Soc., 64: 93-157. doi:10.1111/j.1469-185X.1989.tb00673.x

Kuper, M. and W. Westheide. – 1997. Sperm ultra-structure and spermatogenesis in the interstitial Polychaete Sphaerosyllis hermaphrodita (Syllidae: Exogoninae). Invertebr. Reprod. Dev., 32(3): 189-200.

Lepore, E., Sciscioli M, Mastrodonato M., Gherardi M., A. Giangrande and L. Musco. – 2006. Sperm ultra-structure and spermiogenesis in Syllis krohni (Polychaeta: Syllidae), with some observations on its reproductive biology. Sci. Mar., 70(4): 585-592.

Mastrodonato, M., M. Sciscioli, E. Lepore, M. Gherardi, A. Giangrande, D. Mercati, R. Dallai and P. Lupetti. – 2003. External gestation of Exogone naidina Oersted, 1845 (Polychaeta, Syllidae): ventral attachment of eggs and embryos. Tissue Cell., 35(4): 297-305. doi:10.1016/S0040-8166(03)00051-X

Millonig, G. – 1976. Laboratory manual of biological electron microscopy. Edizioni Saviolo. Vercelli.

Nygren, A. – 1999. Phylogeny and reproduction in Syllidae (Polychaeta). Zool. J. Linn. Soc., 126(3): 365-386.

Patti, P., M.C. Gambi and A. Giangrande. – 2003. Preliminary study on the systematic relationships of Sabellinae (Polychaeta: Sabellidae), based on the C1 domain of the 28S rDNA, with discussion of reproductive features. Ital. J. Zool., 70: 269-278.

Pierantoni, U. – 1903. La Gestazione esterna (Contributo alla biologia e all’embriologia dei Sillidi). Arch. Zool. Ital., 1: 231-252.

Rice, S.A. – 1992. Polychaeta. Spermatogenesis and sperm structure. In: Harrison F. W. and Gardiner S. (eds.), Microcopic Anatomy of Invertebrates Vol. VII (Annelida), pp. 129-151. Wiley-Liss Inc., Wilmington.

San Martín, G. – 2003. Annelida, Polychaeta II: Syllidae. In: M.A. Ramos Sánchez, J. Alba Tercedor, X. Bellés i Ros, J. Gosálbez i Noguera, A. Guerra Sierra, E. Macpherson Mayol, F. Martín Piera, J. Serrano Marino and J. Templado González (eds.), Fauna Ibérica, Vol 21, pp. 1-554. Museo Nacional de Ciencias Naturales. CSIC, Madrid.

Schiedges, K.L. – 1979. Reproductive Biology and Ontogenesis in the Polychaete Genus Autolytus (Annelida: Syllidae): observations on Laboratory cultured individuals. Mar. Biol., 54: 239-250. doi:10.1007/BF00395786

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

Vortsepneva, E.V., A.E. Zhadan and A.B. Tzetlin. – 2006. Spermiogenesis and sperm ultrastructure of Asetocalamyzas laonicola Tzetlin, 1985 (Polychaeta), an ectoparasite of the large spionid Scolelepis cf. matsugae Sikorsfi, 1994, from the White Sea. Sci. Mar., 70S3: 343-350.

Wilkens, L.A. and J.J. Wolken. – 1981. Electroretinograms from Odontosyllis enopla (Polychaeta; Syllidae): Initial observations on the visual system of the bioluminescent fireworm of Bermuda. Mar. Behav. Physiol., 8: 55-66.