An unexpectedly sophisticated, V-shaped spermatozoon in Demospongiae (Porifera): Reproductive and evolutionary implications

Biological Journal of the Linnean Society

Volumn 97, Issue 2, 2009, Pages 413-426

  Riesgo, Ana ^a   Maldonado, Manuel ^a  

^a CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

Author keywords

Early metazoans; Entaquaspermatozoon; Fertilization; Gamete evolution; Gametic biology; Invertebrate reproduction; Phoronidea; Spermatogenesis; Sponges; Striated rootlets

Indexed keywords

EVOLUTION; FERTILIZATION (REPRODUCTION); GAMETOGENESIS; REPRODUCTION; SPERM; SPONGE;

ANIMALIA; CRAMBE (PORIFERA); CRAMBE CRAMBE; DEMOSPONGIAE; EUKARYOTA; INVERTEBRATA; METAZOA; PHORONIFORMEA; PORIFERA;

EID: 66149130742     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2009.01214.x     Document Type: Article

References (51)

1. Afzelius B. 1972. Sperm morphology and fertilization biology. In : Beatty R, Gluecksohn-Waelsch S, eds. Proceedings of the international symposium of the genetics of the spermatozoon. EdInburgh and New York : Bogtrykkeriet Forum, 131 143.
2. Afzelius B. 1979. Sperm structure in relation to phylogeny in lower metazoa. In : Fawcett DW, Bedford JM, eds. The spermatozoon. Baltimore-Munich : Urban & Schwarzenberg, Inc., 243 251.
3. Alberti G. 1995. Comparative spermatology of Chelicerata: review and perspective. In : Jamieson BGM, Ausió J, Justine JL, eds. Advances in spermatozoan phylogeny and taxonomy. Paris : Mémoires du Muséum National d'Histoire Naturelle, 203 230.
4. Anakina RP, Drozdov AL. 2001. Gamete structure and fertilization in the Barents Sea sponge Leucosolenia complicata. Russian Journal of Marine Biology 27 : 143 150. (Pubitemid 33642580)
5. Baccetti B. 1979. The evolution of the acrosomal complex. In : Fawcett DW, Bedford JM, eds. The spermatozoon. Baltimore, Munich : Urban & Schwarzenberg, 305 328.
6. Baccetti B, Afzelius B. 1976. The biology of the sperm cell. Monographs in Developmental Biology 10 : 1 254.
7. Baccetti B, Gaino E, Sarà M. 1986. A sponge with acrosome: Oscarella lobularis. Journal of Ultrastructure and Molecular Structure Research 94 : 195 198.
8. Barthel D, Detmer A. 1990. The spermatogenesis of Halichondria panicea (Porifera, Demospongiae). Zoomorphology 110 : 9 15.
9. Bishop J, Pemberton A. 2006. The third way: spermcast mating in sessile marine invertebrates. Integrative and Comparative Biology 46 : 398 406. (Pubitemid 44290604)
10. Boury-Esnault N, Efremova S, Bézac C, Vacelet J. 1999. Reproduction of a hexactinellid sponge: first description of gastrulation by cellular delamination in the Porifera. Invertebrate Reproduction and Development 35 : 187 201. (Pubitemid 29407594)
11. Boury-Esnault N, Jamieson B. 1999. Porifera. In : Adiyodi KG, Adiyodi RG, eds. Reproductive biology of invertebrates. IX. Progress in male gamete ultrastructure and phylogeny. Chichester : John Wiley and Sons, 1 20.
12. De Vos L, Rützler K, Boury-Esnault N, Donadey C, Vacelet J. 1991. Atlas of sponge morphology. Washington, London : Smithsonian Institution Press.
13. Diaz JP, Connes R. 1980. Étude ultrastructurale de la spermatogenèse d'une. Démosponge. Biologie Cellulaire 38 : 225 230. (Pubitemid 11200840)
14. Efremova S, Papkovskaya MV. 1980. Spermatogenesis of the sponge Lubomirskia baicalensis (Pallas). Ultrastructural investigation. Arkiv Anatomii, Gistologii i Ehmbriologii 12 : 88 95.
15. Fell P. 1974. Porifera. In : Giese A, Pearse J, eds. Reproduction of marine invertebrates: acoelomate and pseudocoelomate metazoans. New York : Academic Press, 51 132.
16. Ferraguti M, Balsamo M. 1995. Comparative spermatology of Gastrotricha. In : Jamieson B, Ausió J, Justine J, eds. Advances in spermatozoal phylogeny and taxonomy. Paris : Mémoires du Muséum National d'Histoire Naturelle, 105 117.
17. Franzén Å. 1956. On spermiogenesis, morphology of spermatozoon and biology of fertilization among invertebrates. Zoologiska bidrag från Uppsala 3 : 355 482.
18. Franzén Å. 1970. Phylogenetic aspects of the morphology of spermatozoa and spermiogenesis. In : Baccetti B, ed. Comparative spermatology. New York : Academic Press, 29 46.
19. Franzén Å. 1987. Spermatogenesis. In : Giese AC, Pearse JS, Pearse VB, eds. Reproduction in marine invertebrates. Pacific Groove, CA : Boxwood Press, 1 47.
20. Franzén Å. 1996. Ultrastructure of spermatozoa and spermiogenesis in the hydrozoan Cordylophora caspia, with comments on structure and evolution of the sperm in the Cnidaria and the Porifera. Invertebrate Reproduction and Development 29 : 19 26. (Pubitemid 26263562)
21. Franzén Å, Ahlfors K. 1980. Ultrastructure of spermatids and spermatozoa in Phoronis, Phylum Phoronida. Journal of Submicroscopical Cytology and Pathology 12 : 585 597. (Pubitemid 11221286)
22. Gaino E, Burlando B, Buffa P, Sarà M. 1986. Ultrastructural study of spermatogenesis in Oscarella lobularis (Porifera, Demospongiae). International Journal of Invertebrate Reproduction and Development 10 : 297 305.
23. Gaino E, Burlando B, Zunino L, Pansini M, Buffa P. 1984. Origin of male gametes from choanocytes in Spongia offcinalis (Porifera, Demospongiae). International Journal of Invertebrate Reproduction and Development 7 : 83 93.
24. Gatenby J. 1927. Further notes on the gametogenesis and fertilization of sponges. Quarterly Journal of Microscopical Science 71 : 173 188.
25. Giménez-Bonafé P, Ribes E, Sautière P, González A, Kasinsky HE, Kouach M, Sautière P-E, Ausió J, Chiva M. 2002. Chromatin condensation, cysteine-rich protamine, and establishment of disulphide interprotamine bonds during spermiogenesis of Eledone cirrhosa (Cephalopoda). European Journal of Cell Biology 81 : 341 349. (Pubitemid 34692945)
26. Harrison FW, De Vos L. 1991. Porifera. In : Harrison FW, eds. Microscopic anatomy of invertebrates. New York : Wiley-Liss, 29 89.
27. Hinsch G. 1974. Comparative ultrastructure of cnidarian sperm. Integrative and Comparative Biology 14 : 457 465.
28. Maldonado M. 2004. Choanoflagellates, choanocytes and animal multicellularity. Invertebrate Biology 123 : 1 22. (Pubitemid 38355687)
29. Maldonado M, Carmona M, Velásquez Z, Puig M, Cruzado A, López A, Young C. 2005. Siliceous sponges as a Silicon sink: an overlooked aspect of benthopelagic coupling in the marine Silicon cycle. Limnology and Oceanography 50 : 799 809. (Pubitemid 40764367)
30. Maldonado M, Durfort M, McCarthy DA, Young CM. 2003. The cellular basis of photobehaviour in the tufted parenchymella larva of demosponges. Marine Biology 143 : 427 441. (Pubitemid 37269074)
31. Mohri H, Kubo-Irie M, Irie M. 1995. Outer arm dynein of sperm flagella and cilia in the animal kingdom. Mémoires Museé Nationale Histoire Naturelle 166 : 15 22.
32. Nakamura Y, Okada K, Watanabe Y. 1998. The ultrastructure of spermatozoa and its structural change in the choanocytes of Sycon calcaravis Hozawa. In : Watanabe Y, Fusetani N, eds. Sponge sciences. Tokyo : Springer Verlag, 179 191.
33. Nielsen C. 2001. Animal evolution. Interrelationships of the living phyla. Oxford : Oxford University Press.
34. Paulus W. 1989. Ultrastructural investigation of spermatogenesis in Spongilla lacustris and Ephydatia fluviatilis (Porifera, Spongillidae). Zoomorphology 109 : 123 130.
35. Reiswig H. 1970. Porifera: sudden sperm release by tropical Demospongiae. Science 170 : 538 539.
36. Reiswig HM. 1983. Porifera. In : Adiyodi KG, Adiyodi RG, Reproductive biology of invertebrates II spermatogenesis and sperm function. Chichester : John Wiley and Sons Ltd., 1 21.
37. Reunov A. 2001. Is the 'flagellated' pattern of spermatogenesis plesiomorphic in Metazoa? Invertebrate Reproduction and Development 40 : 239 242. (Pubitemid 34763062)
38. Reunov A. 2005. Problem of terminology in characteristics of spermatozoa of Metazoa. Russian Journal of Developmental Biology 36 : 335 351. (Pubitemid 43228122)
39. Reunov A, Klepal W. 2004. Ultrastructural study of spermatogenesis in Phoronopsis harmeri (Lophophorata, Phoronida). Helgoland Marine Research 58 : 1 10. (Pubitemid 38345822)
40. Riesgo A, Taylor C, Leys S. 2007a. Reproduction in a carnivorous sponge: the significance of the absence of an aquiferous system to the sponge body plan. Evolution and Development 9 : 618 631. (Pubitemid 350045757)
41. Riesgo A, Maldonado M, Durfort M. 2007b. Dynamics of gametogenesis, embryogenesis, and larval release in a Mediterranean homosclerophorid demosponge. Marine and Freshwater Research 58 : 398 417. (Pubitemid 46639920)
42. Rouse G, Jamieson B. 1987. An ultrastructural study of the spermatozoa of the polychaetes Eurythoe complanata (Amphinomidae), Clymenella sp. and Micromaldane sp. (Maldanidae). Journal of Submicroscopical Cytology and Pathology 19 : 573 584.
43. Simpson T. 1984. Gamete, embryo, larval development. In : Simpson T, ed. The cell biology of sponges. Berlin : Springer Verlag, 341 413.
44. Tripepi S, Longo O, La Camera R. 1984. A new pattern of spermiogenesis in the sponge Crambe crambe: preliminary observations. In : Csanády A, Röhlich P, Szabó D, eds. Proceedings of the Eighth European Congress on Electron Microscopy. Budapest : Programme Committee, 2073 2074.
45. Tuzet O. 1930. Sur la fécondation de l'eponge siliceuse Cliona viridis Schmidt. Comptes Rendus de l'Academie des Sciences, Paris 191 : 1095 1097.
46. Tuzet O. 1947. L'ovogenèse et la fécondation de l'éponge calcaire Leucosolenia (Clathrina) coriacea Mont. et de l'éponge siliceuse Reniera elegans Bow. Archives de zoologie expérimentale et génerale 85 : 127 148.
47. Tuzet O. 1964. L'origine de la ligneé germinale et la gametogénèse chez les spongiaires. In : Wolff E, ed. L'origine de la Ligneé Germinale. Paris : Hermann, 79 111.
48. Tuzet O, Paris J. 1964. La spermatogenèse, l'ovogenèse, la fécondation et les premiers stades du développement chez Octavella galangaui. Vie et Milieu 15 : 309 327.
49. Woollacott R, Pinto R. 1995. Flagellar basal apparatus and its utility in phylogenetic analyses of the Porifera. Journal of Morphology 226 : 247 265. (Pubitemid 3008395)
50. Ying X, Yang W, Jiang N, Zhang Y. 2004. Ultrastructure of spermatozoa of Bullacta exarata (Philippi) and its significance on reproductive evolution and physioecological adaptation. Z Zhejiang Univ SCI 5 : 1211 1217.
51. Zimmer R. 1991. Phoronida. In : Giese AC, Pearse JS, Pearse VB, eds. Reproduction of marine invertebrates. Pacific Grove : The Boxwood Press, 1 45.