Embryogenesis and larval differentiation in sponges

Canadian Journal of Zoology

Volumn 84, Issue 2, 2006, Pages 262-287

  Leys, S P ^a   Ereskovsky, A V ^b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MATERIALS; CELL CULTURE; MICROORGANISMS;

ANTERIOR-POSTERIOR POLARITY; CELLULAR DIFFERENTIATION; MORPHOGENESIS; SPONGE LARVA;

GENETIC ENGINEERING;

EMBRYONIC DEVELOPMENT; LARVAL DEVELOPMENT; METAZOAN; MORPHOGENESIS; PHYLOGENETICS; SENSORY SYSTEM; SEXUAL REPRODUCTION; SPONGE;

ANIMALIA; METAZOA; PORIFERA;

EID: 33745180200     PISSN: 00084301     EISSN: None     Source Type: Journal    
DOI: 10.1139/z05-170     Document Type: Review

References (159)

1. Adell, T., Grebenjuk, V.A., Wiens, M., and Müller, W.E.G. 2003. Isolation and characterization of two T-box genes from sponges, the phylogenetically oldest metazoan taxon. Dev. Genes Evol. 213: 421-434.
2. Adell, T., Nefkens, I., and Müller, W.E.G. 2003. Polarity factor 'Frizzled' in the demosponge Suberites domuncula : identification, expression and localization of the receptor in the epithelium/pinacoderm. FEBS Lett. 554: 363-368.
3. Amano, S., and Hori, I. 1996. Transdifferentiation of larval flagellated cells to choanocytes in the metamorphosis of the demosponge Haliclona permollis. Biol. Bull. (Woods Hole), 190: 161-172.
4. Amano, S., and Hori, I. 2001. Metamorphosis of coeloblastula performed by multipotential larval flagellated cells in the calcareous sponge Leucosolenia laxa. Biol. Bull. (Woods Hole), 200: 20-32.
5. Anakina, R.P. 1997. The cleavage specificity in embryos of the Barents sea sponge Leucosolenia complicata Montagu (Calcispongiae, Calcaronea). In Modern problems of poriferan biology. Edited by A.V. Ereskovsky, H. Keupp, and R. Kohring. Berliner Geowissenschaftliche Abhandlung, Freie Universitat, Berlin. Band 20. pp. 45-53.
6. Baccetti, B., Gaino, E., and Sarà, M. 1986. A sponge with acrosome: Oscarella lobularis. J. Ultrastruct. Mol. Struct. Res. 94: 195-198.
7. Barrois, M.C. 1876. L'embryologie de quelques éponges de la manche. Ann. Sci. Nat. Zool. Paleontol. 3: 1-84.
8. Bavestrello, G., Benatti, U., Calcinai, B., Cattaneo-Vietti, R., Cerrano, C., Favre, A., Giovine, M., Lanza, S., Pronzato, R., and Sara, M. 1998. Body polarity and mineral selectivity in the demosponge Chondrosia reniformis. Biol. Bull. (Woods Hole), 195: 120-125.
9. Bebenek, I., Gates, R., Morris, J., Hartenstein, V., and Jacobs, D. 2004. Sine oculis in basal Metazoa. Dev. Genes Evol. 214: 342-351.
10. Bergquist, P.R. 1996. Porifera: Demospongiae. Part 5: Dendroceratida and Halisarcida. N.Z. Oceanogr. Inst. Mem. 107: 7-53.
11. Bergquist, P.R., and Kelly, M. 2004. Taxonomy of some Halisarcida and Homosclerophorida (Porifera: Demospongiae) from the Indo-Pacific. N.Z. J. Mar. Freshw. Res. 38: 51-66.
12. Borchiellini, C., Manuel, M., Alivon, E., Boury-Esnault, N., Vacelet, J., and Le Parco, Y. 2001. Sponge paraphyly and the origin of Metazoa. J. Evol. Biol. 14: 171-179.
13. Borchiellini, C., Chombard, C., Manuel, M., Alivon, E., Vacelet, J., and Boury-Esnault, N. 2004a. Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution. Mol. Phylogenet. Evol. 32: 823-837.
14. Borchiellini, C., Alvion, E., and Vacelet, J. 2004b. The systematic position of Alectona (Porifera, Demospongiae), a tetractinellid sponge. Boll. Mus. Ist. Biol. Univ. Genova, 68: 207-217.
15. Borojevic, R. 1967. La ponte et le développement de Polymastia robusta (Démosponges). Cah. Biol. Mar. 7: 1-6.
16. Borojevic, R. 1969. Étude du développement et de la différenciation cellulaire d'éponges calcaires calcinèennes (genres Clathrina et Ascandra). Ann. Embryol. Morphog. 2: 15-36.
17. Borojevic, R. 1970. Différenciation cellulaire dans l'embyogénèse et la morphogenèse chez les spongiaires. Zool. Soc. Lond. 25: 467-490.
18. Borojevic, R. 1979. Evolution des spongiares Calcarea. Colloq. Int. Cent. Natl. Rech. Sci. 291: 527-530.
19. Borojevic, R., Boury-Esnault, N., Manuel, M., and Vacelet, J. 2002. Order Leucosolenida Hartman, 1958. In Systema Porifera: a guide to the classification of sponges. Edited by J.N.A. Hooper and R.W.M. van Soest. Kluwer Academic/Plenum Publishers, New York. pp. 1157-1184.
20. Boury-Esnault, N., and Jamieson, B.G.M. 1999. Porifera. In Reproductive biology of invertebrates. Edited by B.G.M. Jamieson. Oxford and IBH Publishing Co. Pvt. Ltd., New Delhi, Calcutta. pp. 1-20.
21. Boury-Esnault, N., and Vacelet, J. 1994. Preliminary studies on the organization and development of a hexactinellid sponge from a Mediterranean cave, Oopsacas minuta. In Sponges in time and space. Edited by R.W.M. van Soest, T.M.G. Van Kempen, and J. Braekman. AA Balkema, Rotterdam, the Netherlands. pp. 407-416.
22. Boury-Esnault, N., De Vos, L., Donadey, C., and Vacelet, J. 1984. Comparative study of the choanosome of Porifera: the Homoscleromorpha. J. Morphol. 180: 3-17.
23. Boury-Esnault, N., Muricy, G., Gallissian, M.-F., and Vacelet, J. 1995. Sponges without skeleton: a new Mediterranean genus of Homoscleromorpha (Porifera, Demospongiae). Ophelia, 43: 25-43.
24. Boury-Esnault, N., Efremova, S., Bézac, C., and Vacelet, J. 1999. Reproduction of a hexactinellid sponge: first description of gastrulation by cellular delamination in the Porifera. Invertebr. Reprod. Dev. 35: 187-201.
25. Boury-Esnault, N., Ereskovsky, A., Bézac, C., and Tokina, D. 2003. Larval development in the Homoscleromorpha (Porifera, Demospongiae). Invertebr. Biol. 122: 187-202.
26. Boute, N., Exposito, J.Y., Boury-Esnault, N., Vacelet, J., Nor, N., Miyazaki, K., Yoshizato, K., and Garrone, R. 1996. Type IV collagen in sponges, the missing link in basement membrane ubiquity. Biol. Cell, 88: 37-44.
27. Brien, P. 1967. Les éponges. Leur nature metazoaire, leur gastrulation, leur état colonial. Ann. Soc. R. Zool. Belg. 97: 197-235.
28. Brien, P. 1973. Les Démosponges. In Traité de zoologie. Edited by P.-P. Grassé. Masson et Cie, Paris. pp. 133-461.
29. Brien, P., and Meewis, H. 1938. Contribution à l'étude de l'embryogénèse des Spongillidae. Arch. Biol. 49: 177-250.
30. Byrum, C.A., and Martindale, M.Q. 2004. Gastrulation in the Cnidaria and Ctenophora. In Gastrulation: from cells to embryos. Edited by C. Stern. Cold Spring Harbor Laboratory Press, Woodbury, N.Y. pp. 33-50.
31. Cavalier-Smith, T., and Chao, E.E. 1995. The opalozoan Apusomonas is related to the common ancestor of animals, fungi, and choanoflagellates. Proc. R. Soc. Lond. B Biol. Sci. 261: 1-6.
32. Cavalier-Smith, T., Allsopp, M.T.E.P., Chao, E.E., Boury-Esnault, N., and Vacelet, J. 1996. Sponge phylogeny, animal monophyly, and the origin of the nervous system. Can. J. Zool. 74: 2031-2045.
33. Chen, W.-T. 1976. Reproduction and speciation in Halisarca. In Aspects of sponge biology. Edited by F.W. Harrison and R.R. Cowden. Academic Press, London. pp. 113-139.
34. Cherdantsev, V.G., and Krauss, Y.A. 1996. Gastrulation in the marine hydroid Dynamena pumila: an example of evolutionary anticipation based on developmental self-organization. Evol. Theory Rev. 11: 89-98.
35. Collins, A.G. 1998. Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence. Proc. Natl. Acad. Sci. U.S.A. 95: 15458-15463.
36. Coutinho, C.C., Seack, J., Van De Vyver, G., Borojevic, R., and Müller, W.E.G. 1994. Origin of the metazoan bodyplan: characterization and functional testing of the promoter of the homeobox gene EmH-3 from the freshwater sponge Ephydatia muelleri in Mouse 3T3 cells. Biol. Chem. 379: 1243-1251.
37. Coutinho, C.C., Fonseca, R.N., Mansure, J.J.C., and Borojevic, R. 2003. Early steps in the evolution of multicellularity: deep structural and functional homologies among homeobox genes in sponges and higher metazoans. Mech. Dev. 120: 429-440.
38. Davidson, E.H., Peterson, K.J., and Cameron, R.A. 1995. Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science (Washington, D.C.), 270: 1319-1325.
39. Degnan, B.M., Leys, S.P., and Larroux, C. 2005. Sponge development and antiquity of animal pattern formation. Integr. Comp. Biol. 45: 335-341.
40. Delage, Y. 1892. Embryogénie des éponges. Développement post-larvaire. Arch. Zool. Exp. Gen. 10: 345-498.
41. Diaz, J.P., and Connes, R. 1980. Etude ultrastructurale de la spermatogénese d'une Démosponge. Biol. Cell, 38: 225-230.
42. Diaz, J.P., Connes, R., and Paris, J. 1973. Etude ultrastructurale de l'ovogenése d'une demosponge: Suberites massa Nardo. J. Microscr. (Oxf.), 24: 105-116.
43. Duboscq, O., and Tuzet, O. 1935. Un nouveau stade du développement des Éponges calcaires. C. R. Acad. Sci. Paris, 200: 1788-1790.
44. Duboscq, O., and Tuzet, O. 1937. L'ovogenèse, la fécondation et les premiers stades du développement des éponges calcaires. Arch. Zool. Exp. Gen. 79: 157-316.
45. Duboscq, O., and Tuzet, O. 1941. Sur les cellules en croix des Sycon (Sycon ciliatum Fabr., Sycon coronatum Ellis et Sol., Sycon elegans Bower) et leur signification. Arch. Zool. Exp. Gen. 81: 151-163.
46. Efremova, S.M. 1997. Once more on the position among Metazoa - gastrulation and germinal layers of sponges. Berl. Geowiss. Abh. 20: 7-15.
47. Elliott, G.R.D., Macdonald, T.A., and Leys, S.P. 2004. Sponge larval phototaxis: a comparative study. In Sponge science in the new millennium. Edited by M. Pansini, R. Pronzato, G. Bavestrello, and R. Manconi. Boll. Mus. Ist. Biol. Univ. Genova. Vol. 68. pp. 291-300.
48. Ereskovsky, A.V. 1999. Development of sponges of the order Haplosclerida. Russ. J. Mar. Biol. 25: 361-371. [Formerly, Biol. Morya (Vladivost.).]
49. Ereskovsky, A.V. 2000. Reproduction cycles and strategies of the cold-water sponges Halisarca dujardini (Demospongiae, Halisarcida), Myxilla incrustans and Iophon piceus (Demospongiae, Poecilosclerida) from the White Sea. Biol. Bull. (Woods Hole), 198: 77-87.
50. Ereskovsky, A.V. 2002. Polyaxial cleavage in sponges (Porifera): a new pattern of metazoan cleavage. Dokl. Biol. Sci. 386: 472-474.
51. Ereskovsky, A.V. 2004. Comparative embryology of sponges and its application for poriferan phylogeny. Boll. Mus. Ist. Biol. Univ. Genova, 68: 301-318.
52. Ereskovsky, A.V. 2005. Comparative embryology of sponges. Sanct-Petersburg University Press, St. Petersburg.
53. Ereskovsky, A.V., and Boury-Esnault, N. 2002. Cleavage pattern in Oscarella species (Porifera, Demospongiae, Homoscleromorpha) transmission of maternal cells and symbiotic bacteria. J. Nat. Hist. 36: 1761-1775.
54. Ereskovsky, A.V., and Gonobobleva, E.L. 2000. New data on embryonic development of Halisarca dujardini Johnston, 1842 (Demospongiae:Halisarcida). Zoosystema, 22: 355-368.
55. Ereskovsky, A.V., and Korotkova, G.P. 1997. The reasons of sponge sexual morphogenesis peculiarities. Berl. Geowiss. Abh. 20: 25-33.
56. Ereskovsky, A.V, and Tokina, D.B. 2004. Morphology and fine structure of the swimming larvae of Ircinia oros (Porifera, Demospongiae, Dictyoceratida). Invertebr. Reprod. Dev. 45: 137-150.
57. Ereskovsky, A.V., Gonobobleva, E.L., and Vishnyakov, A. 2005. Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarcida). Mar. Biol. (Berl.), 146: 869-875.
58. Fell, P.E. 1969. The involvement of nurse cells in oogenesis and embryonic development in the marine sponge Haliclona ecbasis. J. Morphol. 127: 133-149.
59. Fell, P.E. 1974. Porifera. In Reproduction of marine invertebrates. Edited by A.C. Giese and J.S. Pearse. Academic Press, New York. pp. 51-132.
60. Fell, P.E. 1976. The reproduction of Haliclona loosanoffi and its apparent relationship to water temprerature. Biol. Bull. (Woods Hole), 150: 200-210.
61. Fell, P.E. 1989. Porifera. In Reproductive biology of invertebrates. IV A. Fertilization, development, and parental care. Edited by K.G. Adiyodi and R.G. Adiyodi. Oxford and IBH Publishing, Calcutta. pp. 1-41.
62. Fell, P.E. 1993. Porifera. In Reproductive biology of invertebrates. VI A. Asexual propagation and reproductive strategies. Edited by K.G. Adiyodi and R.G. Adiyodi. John Wiley and Sons Ltd., Chichester, U.K. pp. 1-44.
63. Fell, P.E., and Jacob, W.F. 1979. Reproduction and development of Halichondria sp. in the Mystic estuary, Connecticut. Biol. Bull. (Woods Hole), 156: 62-75.
64. Finnerty, J.R., and Martindale, M.Q. 1998. The evolution of the Hox cluster: insights from outgroups. Curr. Opin. Genet. Dev. 8: 681-687.
65. Fischel Johnson, M. 1979. Gametogenesis and embryonic development in the calcareous sponges Clathrina coriacea and C. blanca from Santa Catalina Island, California. Bull. South. Calif. Acad. Sci. 78: 183-191.
66. Franzen, W. 1988. Oogenesis and larval develoment of Scypha ciliata (Porifera, Calcarea). Zoomorphology (Berl.), 107: 349-357.
67. Gaino, E., and Sara, M. 1994. An ultrastructural comparative study of the eggs of two species of Tethya (Porifera, Demospongiae). Invertebr. Reprod. Dev. 26: 99-106.
68. Gaino, E., Burlando, B., Buffa, P., and Sara, M. 1986. Ultrastructural study of spermatogenesis in Oscarella lobularis (Porifera, Demospongiae). Invertebr. Reprod. Dev. 10: 297-305.
69. Gallissian, M.F. 1983. Étude ultrastructurale du developpement embryonnaire chez Grantia compressa F. (Porifera, Calcarea). Arch. Anat. Microsc. 72: 59-75.
70. Gallissian, M.F., and Vacelet, J. 1992. Ultrastructure of the oocyte and embryo of the calcified sponge, Petrobiona massiliana (Porifera, Calcarea). Zoomorphology (Berl.), 112: 133-141.
71. Garrone, R. 1974. Ultrastructure d'une "gemmule armée" planctonique d'éponge Clionidae. Inclusions fibrillaires et genèse du collagène. Arch. Anat. Microsc. Morphol. Exp. 63: 163-182.
72. Gatenby, J.B. 1920. The germ-cells, fertilization, and early development of Grantia (Sycon) compressa. Linn. J. Zool. 34: 261-297.
73. Gilbert, R., and Raunio, A.M. 1997. Embryology: constructing the organism. Sinauer Associates, Inc., Sunderland, Mass.
74. Gonobobleva, E.L., and Ereskovsky, A.V. 2004a. Metamorphosis of the larva of Halisarca dujardini (Demospongiae, Halisarcida). Bull. Inst. R. Sci. Nat. Belg. 74: 101-115.
75. Gonobobleva, E.L., and Ereskovsky, A.V. 2004b. Polymorphism in free-swimming larvae of Halisarca dujardini (Demosponge, Halisarcida). Boll. Mus. Ist. Biol. Univ. Genova, 68: 349-356.
76. Haeckel, E. 1872. Die Kalkschwämme, Eine Monographie. Verlag von Georg Reimer, Berlin.
77. Haeckel, E. 1874. Die Gastraea-Theorie, die phylogenetische Classification des Thierreichs und die Homologie der Keimblätter. Z. Natwiss. 8: 1-55.
78. Heider, K. 1886. Zur Metamorphose der Oscarella lobularis O. Schmidt. Arb. Zool. Inst. Univ. Wien, 6: 175-236.
79. Hill, A., Tetrault, J., and Hill, M. 2004. Isolation and expression analysis of a poriferan Antp-class Bar-/Bsh-like homeobox gene. Dev. Genes Evol. 214: 515-523.
80. Hoppe, W.F. 1988. Reproductive patterns in three species of large coral reef sponges. Coral Reefs, 7: 45-50.
81. Hooper, J.N.A., and Soest, R.W.M., van (Editors). 2002. Systema Porifera: a guide to the classification of sponges. Kluwer Academic/Plenum Publishers, New York.
82. Hoppe, W.F., and Reichert, M.J.M. 1987. Predictable annual mass release of gametes by the coral reef sponge Neofibularia nolitangere (Porifera: Demospongiae). Mar. Biol. (Berl.), 94: 277-285.
83. Hoshiyama, D., Suga, H., Iwabe, N., Koyanagi, M., Nikoh, N., Kuma, K., Matsuda, F., Honjo, T., and Miyata, T. 1998. Sponge Pax cDNA related to Pax 2-5-8 and ancient gene duplications in the Pax family. J. Mol. Evol. 47: 640-648.
84. Ijima, I. 1901. Studies on the Hexactinellida. Contribution I (Euplectellidae). J. Coll. Sci. Imp. Univ. Tokyo, 15: 1-299.
85. Ilan, M., and Loya, Y. 1990. Sexual reproduction and settlement of the coral reef sponge Chalinula sp. from the Red Sea. Mar. Biol. (Berl.), 105: 25-31.
86. Ivanova-Kazas, O.M. 1995. Evolutionary embryology of animals. Nauka Press, St. Petersburg.
87. Kaye, H. 1991. Sexual reproduction in four Caribbean commercial sponges. II. Oogenesis and transfer of bacterial symbionts. Invertebr. Reprod. Dev. 19: 13-24.
88. Kilian, E.F. 1952. Wasserströmung und Nahrungsaufnahme beim Süsswasserschwamm Ephydatia fluviatilis. Z. Vgl. Physiol. 34: 407-447.
89. King, N., Hittinger, C.T., and Carroll, S.B. 2003. Evolution of key cell signaling and adhesion protein families predates animal origins. Science (Washington, D.C.), 301: 361-363.
90. Korotkova, G.P. (Editor). 1981. Sexual embryogenesis of sponges and objective laws of its evolution. In Morphogenesis in sponges. Leningrad University, Leningrad. pp. 108-136.
91. Korotkova, G.P., and Apalkova, L.V. 1975. Oogenesis of the Barents Sea sponge Halisarca dujardini. In Comparative and experimental morphology of the sea organisms. Edited by I.B. Tokin. Kolske filial Academy of Sciences Apatiti. pp. 9-26. [In Russian.]
92. Kruse, M., Leys, S.P., Müller, I.M., and Müller, W.E.G. 1998. Phylogenetic position of the hexactinellida within the phylum Porifera based on the amino acid sequence of the protein kinase C from Rhabdocalyptus dawsoni. J. Mol. Evol. 46: 721-728.
93. Lafay, F., Boury-Esnault, N., Vacelet, J., and Christen, R. 1992. An analysis of partial 28s ribosomal RNA sequences suggests early radiations of sponges. Biosystems, 28: 139-151.
94. Larroux, C., Fahey, B., Liubicich, D., Hinman, V.F., Gauthier, M., Gongora, M., Green, K., Wörheide, G., Leys, S.P., and Degnan, B.M. 2006. Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evol. Dev. 8(2): 150-173.
95. Le Pennec, G., Perovic, S., Ammar, M., Grebenjuk, V., Steffen, R., Brummer, F., and Müller, W.E.G. 2003. Cultivation of primmorphs from the marine sponge Suberites domuncula: morphogenetic potential of silicon and iron. J. Biotechnol. 100: 93-108.
96. Lévi, C. 1956. Étude des Halisarca de Roscoff émbryologie et systématique des démosponges. Arch. Zool. Exp. Gen. 93: 1-184.
97. Lévi, C. 1963. Gastrulation and larval phylogeny in sponges. In The Lower Metazoa: comparative biology and phylogeny. Edited by E.C. Dougherty. University of California Press, Los Angeles. pp. 375-382.
98. Lévi, C. 1970. Les cellules des éponges. Symp. Zool. Soc. Lond. 25: 353-364.
99. Lévi, C., and Lévi, P. 1976. Embryogénèse de Chondrosia reniformis (Nardo), démosponge ovipare, et transmission des bactéries symbiotiques. Ann. Sci. Nat. Zool. 18: 367-380.
100. Lévi, C., and Porte, A. 1962. Etude au microscope électronique de l'éponge Oscarella lobularis Schmidt et de sa larve amphiblastula. Cah. Biol. Mar. 3: 307-315.
101. Leys, S.P. 2003. Comparative study of spiculogenesis in demosponge and hexactinellid Larvae. Microsc. Res. Tech. 62: 300-311.
102. Leys, S.P. 2004. Gastrulation in sponges. In Gastrulation: from cells to embryo. Edited by C. Stern. Cold Spring Harbor Laboratory Press, Woodbury, N.Y. pp. 23-31.
103. Leys, S.P., and Degnan, B.M. 2001. The cytological basis of photoresponsive behaviour in a sponge larva. Biol. Bull. (Woods Hole), 201: 323-338.
104. Leys, S.P., and Degnan, B.M. 2002. Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes. Invertebr. Biol. 121: 171-189.
105. Leys, S.P., and Eerkes-Medrano, D.I. 2005. Gastrulation in calcareous sponges: in search of Haeckel's Gastraea. Integr. Comp. Biol. 45: 342-351.
106. Leys, S.P., Cheung, E., and Boury-Esnault, N. 2006. Embryogenesis in the glass sponge Oopsacas minuta: formation of syncytia by fusion of blastomeres. Integr. Comp. Biol. 46(1). In press.
107. Lufty, R.G. 1957. On the placental membrane of calcareous sponges. Cellule, 58: 239-246.
108. Maldonado, M. 2004. Choanoflagellates, choanocytes, and animal multicellularity. Invertebr. Biol. 123: 1-22.
109. Maldonado, M. 2006. The ecology of the sponge larva. Can. J. Zool. 84: 175-194.
110. Maldonado, M., and Bergquist, P.R. 2002. Phylum Porifera. In Atlas of marine invertebrate larvae. Edited by C.M. Young, M.A. Sewell, and M.E. Rice. Academic Press, San Diego. pp. 21-50.
111. Manuel, M., and Le Parco, Y. 2000. Homeobox gene diversification in the calcareous sponge Sycon raphanus. Mol. Phylogenet. Evol. 17: 97-107.
112. Manuel, M., Borojevic, R., Boury-Esnault, N., and Vacelet, J. 2002. Class Calcarea Bowerbank, 1864. In Systema Porifera: a guide to the classification of sponges. Edited by J.N.A. Hooper and R.W.M. van Soest. Kluwer Academic/Plenum Publishers, New York. pp. 1103-1110.
113. Manuel, M., Le Parco, Y., and Borchiellini, C. 2004. Comparative analysis of Brachyury T-domains, with the characterization of two new sequences, from a hexactinellid and a calcisponge. Gene (Amst.), 340: 291-301.
114. Mariani, S., Uriz, M.-J., and Turon, X. 2000. Larval bloom of the oviparous sponge Cliona viridis: coupling of larval abundance and adult distribution. Mar. Biol. (Berl.), 137: 783-790.
115. Medina, M., Collins, A.G., Silberman, J., and Sogin, M.L. 2001. Evaluating hypotheses of basal animal phytogeny using complete sequences of large and small subunit rRNA. Proc. Natl. Acad. Sci. U.S.A. 98: 9707-9712.
116. Meewis, H. 1938. Contribution a l'étude de l'embryogé nèse des Myxospongidae: Halisarca lobularis Schmidt. Arch. Biol. 50: 1-66.
117. Meewis, H. 1939. Contribution a l'étude de l'embryogé nèse des Chalinidae : Haliclona limbata (Mont.). Ann. Soc. R. Zool. Belg. 70: 201-243.
118. Metschnikoff, E. 1879. Spongiologische Studien. Z. Wiss. Zool. 32: 349-387.
119. Minchin, E.A. 1900. The Porifera and Coelenterata. Adam and Charles Black, London.
120. Nassonow, N. 1883. Zur Biologie und Anatomie der Clione. Z. Wiss. Zool. 39: 295-308.
121. Nikko, E., Van De Vyver, G., and Richelle-Maurer, E. 2001. Retinoic acid down-regulates the expression of EmH-3 homeobox-containing gene in the freshwater sponge Ephydatia muelleri. Mech. Ageing Dev. 122: 779-794.
122. Okada, Y. 1928. On the development of a hexactinellid sponge, Farrea sollasii. J. Fac. Sci. Imp. Univ. Tokyo, 4: 1-29.
123. Paulus, W., and Weissenfels, N. 1986. The spermatogenesis of Ephydatia fluviatilis (Porifera). Zoomorphology (Berl.), 106: 155-162.
124. Perovic, S., Schroder, H.C., Sudek, S., Grebenjuk, V.A., Batel, R., Stifanic, M., Müller, I.M., and Müller, W.E.G. 2003. Expression of one sponge Iroquois homeobox gene in primorphs from Suberites domuncula during canal formation. Evol. Dev. 5: 240-250.
125. Price, A.L., and Patel, N.H. 2004. The evolution of gastrulation: cellular and molecular aspects. In Gastrulation. From cells to embryos. Edited by C. Stern. Cold Spring Harbor Laboratory Press, Woodbury, N.Y. pp. 695-701.
126. Rasmont, R. 1979. Les eponges : Des métazoaires et des sociétés de cellules. Colloq. Int. Cent. Natl. Rech. Sci. 291: 21-29.
127. Reiswig, H.M. 1976. Natural gamete release and oviparity in Caribbean Demospongiae. In Aspects of sponge biology. Edited by F.W. Harrison and R.W. Cowden. Academic Press, New York. pp. 99-112.
128. Richelle-Maurer, E., and Van De Vyver, G. 1999. Temporal and spatial expression of EmH-3, a homeobox-containing gene isolated from the freshwater sponge Ephydatia muelleri. Mech. Ageing Dev. 109: 203-219.
129. Rosell, D. 1993. Effects of reproduction in Cliona viridis (Hadromerida) on zooxanthellae. Sci. Mar. 57: 405-413.
130. Saller, U. 1988. Oogenesis and larval development of Ephydatia fluviatilis (Porifera, Spongillidae). Zoomorphology (Berl.), 108: 23-28.
131. Saller, U., and Weissenfels, N. 1985. The development of Spongilla lacustris from the oocyte to the free larva (Porifera, Spongillidae). Zoomorphology (Berl.), 105: 367-374.
132. Scholz, C.B., and Technau, U. 2003. The ancestral role of Brachyury: expression of NemBra 1 in the basal cnidarian Nematostella vectensis (Anthozoa). Dev. Genes Evol. 212: 563-570.
133. Schulze, F.E. 1875. Ueber den Bau und die Entwicklung von Sycandra raphanus Haeckel. Z. Wiss. Zool. 25: 247-280.
134. Schulze, F.E. 1877. Untersuchungen über den Bau und die Entwicklung der Spongien. Die Gattung Halisarca. Z. Wiss. Zool. 28: 1-48.
135. Schulze, F.E. 1878. Untersuchungen über den Bau und die Entwicklung der Spongien. Die Metamorphose von Sycandra raphanus. Z. Wiss. Zool. 31: 262-295.
136. Schulze, F.E. 1880. On the structure and arrangement of the soft parts in Euplectella aspergillum. Trans. R. Soc. Edinb. 29: 661-673.
137. Sciscioli, M., Scalera-Liaci, L., Lepore, E., Gherardi, M., and Simpson, T.L. 1991. Ultrastructural study of the mature egg of the marine sponge Stelletta grubii (Porifera Demospongiae). Mol. Reprod. Dev. 28: 346-350.
138. Seimiya, M., Ishiguro, H., Miura, K., Watanabe, Y., and Kurosawa, Y. 1994. Homeobox-containing genes in the most primitive Metazoa, the sponges. Eur. J. Biochem. 221: 219-225.
139. Seimiya, M., Watanabe, Y., and Kurosawa, Y. 1997. Identification of POU-class homeobox genes in a freshwater sponge and the specific expression of these genes during differentiation. Eur. J. Biochem. 243: 27-31.
140. Sidri, M., Milanese, M., and Brümmer, F. 2005. First observations on egg release in the oviparous sponge Chondrilla nucula (Demospongiae, Chondrosida, Chondrillidae) in the Mediterranean Sea. Invertebr. Biol. 124(2): 91-97.
141. Siewing, R. 1979. Homology of cleavage types? Z. Zool. Syst. Evolutionsforsch. 1: 7-18.
142. Snell, E., Furlong, R., and Holland, P. 2001. Hsp70 sequences indicate that choanoflagellates are closely related to animals. Curr. Biol. 11: 967-970.
143. Tuzet, O. 1963. The phylogeny of sponges according to embryological, histological, and seological data, and their affinities with the Protozoa and the Cnidaria. In The Lower Metazoa: comparative biology and phylogeny. Edited by E.G. Dougherty. The University of California Press, San Diego. pp. 129-148.
144. Tuzet, O. 1970. La polarité de l'oeuf et la symétrie de la larve des éponges calcaires. Symp. Zool. Soc. Lond. 25: 437-448.
145. Tuzet, O. 1973. Éponges calcaires. In Traité de Zoologie. Edited by P.-P. Grassé. Masson et Cie, Paris. pp. 27-132.
146. Tuzet, O., and Paris, J. 1964. La spermatogenèse, l'ovogenèse, la fécondation et les premiers stades du développement chez Octavella galangaui. Vie Milieu, 15: 309-327.
147. Usher, K.M., and Ereskovsky, A.V. 2005. Larval development, ultrastructure and metamorphosis in Chondrilla australiensis Carter, 1873 (Demospongiae, Chondrosia, Chondrillidae). Invertebr. Reprod. Dev. 47(1): 51-62.
148. Usher, K.M., Sutton, D., Toze, S., Kuo, J., and Fromont, J. 2004. Sexual reproduction in Chondrilla australiensis (Porifera: Demospongiae). Mar. Freshw. Res. 55: 123-134.
149. Vacelet, J. 1999. Planktonic armoured propagules of the excavating sponge Alectona (Porifera: Demospongiae) are larvae: evidence from Alectona wallichii and A. mesatlantica sp. nov. Mem. Queensl. Mus. 44: 627-642.
150. Valentine, J.W. 1997. Cleavage patterns and the topology of the metazoan tree of life. Proc. Natl. Acad. Sci. U.S.A. 94: 8001-8005.
151. Warburton, F.E. 1961. Inclusion of parental somatic cells in sponge larvae. Nature (London), 191: 1371.
152. Watanabe, Y. 1957. Development of Tethya serica Lebwohl, a tetraxonian sponge. I. Observations on external changes. Nat. Sci. Rep. Ochanomizu Univ. 8: 97-104.
153. Watanabe, Y. 1978. The development of two species of Tetilla (Demosponge). Nat. Sci. Rep. Ochanomizu Univ. 29: 71-106.
154. Witte, U. 1996. Seasonal reproduction in deep-sea sponges - triggered by vertical particle flux? Mar. Biol. (Berl.), 124: 571-581.
155. Woollacott, R.M. 1990. Structure and swimming behavior of the larva of Halichondria melanadocia (Porifera: Demospongiae). J. Morphol. 205: 135-145.
156. Woollacott, R.M. 1993. Structure and swimming behavior of the larva of Haliclona tubifera (Porifera: Demospongiae). J. Morphol. 218: 301-321.
157. Woollacott, R.M., and Hadfield, M.G. 1989. Larva of the sponge Dendrilla cactus (Demospongiae: Dendroceratida). Trans. Am. Microsc. Soc. 108: 410-413.
158. Woollacott, R.M., and Pinto, R.L. 1995. Flagellar basal apparatus and its utility in phylogenetic analyses of the porifera. J. Morphol. 226: 247-265.
159. Zrzavy, J., Mihulka, S., Kepka, P., Bezdek, A., and Tietz, D. 1998. Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics, 14: 249-285.