Hydrobiologia

, Volume 687, Issue 1, pp 3–10 | Cite as

No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera

  • Eve Gazave
  • Pascal Lapébie
  • Alexander V. Ereskovsky
  • Jean Vacelet
  • Emmanuelle Renard
  • Paco Cárdenas
  • Carole Borchiellini
SPONGE RESEARCH DEVELOPMENTS Short Research Note

Abstract

Over the past few years, there has been growing interest among the sponge community in the phylogenetic position of the Homoscleromorpha (i.e. within or outside the class Demospongiae). Recent molecular analyses clearly show that the Homoscleromorpha forms a distinct clade separated from the Demospongiae and is composed of two families, Oscarellidae and Plakinidae. Within the currently more widely accepted hypothesis of a monophyletic Porifera, we formally propose here to raise Homoscleromorpha to the class rank (the fourth one). We, therefore, provide a definition and a formal diagnosis. In the supplementary materials, we also present an alternative classification of the Homoscleromorpha, following the PhyloCode.

Keywords

Porifera New class Homoscleromorpha Oscarellidae Plakinidae PhyloCode 

Notes

Acknowledgments

We thank the organizers of the conference in Girona for this excellent meeting and for giving us the opportunity to contribute to the special volume of Hydrobiologia dedicated to sponges. We are also very grateful to Dr. Nicole Boury-Esnault for stimulating discussions on the PhyloCode. We thank three anonymous reviewers for helpful comments. This work was partly supported by bilateral program RFBR-PICS No. 5581. The English language has been revised by Michael Paul.

Supplementary material

10750_2011_842_MOESM1_ESM.doc (32 kb)
Supplementary file 1: Alternative phylogenetic classification of Homoscleromorpha based on the draft PhyloCode Version 4c. (DOC 32 kb)
10750_2011_842_MOESM2_ESM.eps (1.4 mb)
Supplementary Fig. 1: Porifera simplified tree, following the monophyly hypothesis, mentioning the names of the Homoscleromorpha clades and species according to the PhyloCode. Homoscleromorpha species that do not have a PhyloCode definition are in light grey. (EPS 1434 kb)

References

  1. Baccetti, B., E. Gaino & M. Sara, 1986. A sponge with acrosome: Oscarella lobularis. Journal of Ultrastructure and molecular structure research 94: 195–198.CrossRefGoogle Scholar
  2. Bergquist, P. R., 1978. Sponges. Hutchinson & Co, London.Google Scholar
  3. Borchiellini, C., C. Chombard, M. Manuel, E. Alivon, J. Vacelet & N. Boury-Esnault, 2004. Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution. Molecular phylogenetics and evolution 32: 823–837.PubMedCrossRefGoogle Scholar
  4. Boury-Esnault, N., G. Muricy, M. F. Gallissian & J. Vacelet, 1995. Sponges without skeleton: a new Mediterranean genus of Homoscleromorpha (Porifera, Demospongiae). Ophelia 43: 25–43.Google Scholar
  5. Boury-Esnault, N., A. V. Ereskovsky, C. Bezac & D. B. Tokina, 2003. Larval development in Homoscleromorpha (Porifera, Demospongiae). Invertebrate Biology 122: 187–202.CrossRefGoogle Scholar
  6. Boute, N., J. Y. Exposito, N. Boury-Esnault, J. Vacelet, N. Noro, K. Miyazaki, K. Yoshizato & R. Garrone, 1996. Type IV collagen in sponges, the missing link in basement membrane ubiquity. Biology of the Cell 88: 37–44.PubMedCrossRefGoogle Scholar
  7. Cárdenas, P., H. T. Rapp, C. Schander & O. S. Tender, 2010. Molecular taxonomy and phylogeny of the Geodiidae (Porifera, Demospongiae, Astrophorida)—combining phylogenetic and Linnaean classification. Zoologica scripta 39: 89–106.CrossRefGoogle Scholar
  8. Cárdenas, P., J. R. Xavier, J. Reveillaud, C. Schander & H. T. Rapp, 2011. Molecular phylogeny of the astrophorida (Porifera, Demospongiaep) reveals an unexpected high level of spicule homoplasy. PLoS ONE 6(4): e18318. doi: 10.1371/journal.pone.0018318.
  9. Carter, H. J., 1875. Notes introductory to the study and classification of the Spongida. The Annals and Magazine of Natural History 4: 1–40 (126–145, 177–200).Google Scholar
  10. Debrenne, F., A. Y. Zhuravlev & P. D. Kruse, 2002. Class Archaeocyatha Bornemann, 1884. In Hooper, J. N. A. & R. W. M. Van Soest (eds), Systema Porifera: A Guide to the Classification of Sponges. Kluwer Academic/Plenum Publishers, New York: 1539–1699.Google Scholar
  11. Dendy, A., 1905. Report on the sponges collected by Professor Herdman, at Ceylon, in 1902. Royal Society, London.Google Scholar
  12. Dohrmann, M., O. Voigt, D. Erpenbeck & G. Wörheide, 2006. Non-monophyly of most supraspecific taxa of calcareous sponges (Porifera, Calcarea) revealed by increased taxon sampling and partitioned Bayesian analysis of ribosomal DNA. Molecular Phylogenetics and Evolution 40: 830–843.PubMedCrossRefGoogle Scholar
  13. Dohrmann, M., D. Janussen, J. Reitner, A. G. Collins & G. Wörheide, 2008. Phylogeny and evolution of glass sponges (Porifera, Hexactinellida). Systematic Biology 57: 388–405.PubMedCrossRefGoogle Scholar
  14. Ereskovsky, A. V., 2005. Comparative Embryology of Sponges (Porifera). Sanct-Petersburg University Press, Sanct-Petersburg.Google Scholar
  15. Ereskovsky, A. V., 2006. A new species of Oscarella (Demospongiae: Plakinidae) from the Western Sea of Japan. Zootaxa 1376: 37–51.Google Scholar
  16. Ereskovsky, A. V., 2010. The Comparative Embryology of Sponges. Springer-Verlag, Dordrecht, Heidelberg, London, New York.CrossRefGoogle Scholar
  17. Ereskovsky, A. V. & N. Boury-Esnault, 2002. Cleavage pattern in Oscarella species (Porifera, Demospongiae, Homoscleromorpha): transmission of maternal cells and symbiotic bacteria. Journal of Natural History 36: 1761–1775.CrossRefGoogle Scholar
  18. Ereskovsky, A. V. & D. B. Tokina, 2007. Asexual reproduction in homoscleromorph sponges (Porifera; Homoscleromorpha). Marine Biology 151: 425–434.CrossRefGoogle Scholar
  19. Ereskovsky, A. V. & P. Willenz, 2008. Larval development in Guancha arnesenae (Porifera, Calcispongiae, Calcinea). Zoomorphology 127: 175–187.CrossRefGoogle Scholar
  20. Ereskovsky, A. V., D. B. Tokina, C. Bezac & N. Boury-Esnault, 2007. Metamorphosis of Cinctoblastula Larvae (Homoscleromorpha, Porifera). Journal of Morphology 268: 518–528.PubMedCrossRefGoogle Scholar
  21. Ereskovsky, A. V., K. Sanamyan & A. E. Vishnyakov, 2009a. Oscarella kamchatkensis sp nov. from the North-West of Pacific. Cahiers de Biologie marine 50: 369–381.Google Scholar
  22. Ereskovsky, A. V., C. Borchiellini, E. Gazave, J. Ivanisevic, P. Lapebie, T. Perez, E. Renard & J. Vacelet, 2009b. The Homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology. Bioessays 31: 89–97.PubMedCrossRefGoogle Scholar
  23. Erpenbeck, D. & G. Wörheide, 2007. On the molecular phylogeny of sponges. Zootaxa 1668: 107–126.Google Scholar
  24. Gaino, E., B. Burlando, P. Buffa & M. Sara, 1986. Ultrastructural study of spermatogenesis in Oscarella lobularis (Porifera, Demospongiae). International Journal of Invertebrates Reproduction and Development 10: 297–305.Google Scholar
  25. Gallissian, M. F. & J. Vacelet, 1992. Ultrastructure of the oocyte and embryo of the calcified sponge, Petrobiona massiliana (Porifera, Calcarea). Zoomorphology 112: 133–141.CrossRefGoogle Scholar
  26. Gazave, E., P. Lapébie, E. Renard, J. Vacelet, C. Rocher, A. V. Ereskovsky, D. V. Lavrov & C. Borchiellini, 2010a. Molecular phylogeny restores the supra-generic subdivision of Homoscleromorph sponges (Porifera, Homoscleromorpha). PLoS ONE. doi: 10.1371/journal.pone.0014290.
  27. Gazave, E., S. Carteron, E. Richelle-Maurer, N. Boury-Esnault & C. Borchiellini, 2010b. Polyphyly of the genus Axinella and of the family Axinellidae (Porifera: Demospongiae). Molecular Phylogenetics and Evolution 57: 35–47.PubMedCrossRefGoogle Scholar
  28. Hooper JNA, van Soest RWM (2002) Systema Porifera: A Guide to the Classification of Sponges. New York: Kluwer Academic/Plenum Publishers.Google Scholar
  29. Hooper, J. N., R. W. M. Van Soest & F. Debrenne (eds), 2002. Phylum Porifera Grant, 1836; Systema Porifera: A Guide to the Classification of Sponges. Kluwer Academic/Plenum Publishers, New York.Google Scholar
  30. Ivanisevic, J., O. P. Thomas, C. Lejeusne, P. Chevaldonné & T. Pérez, 2010. Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics. doi: 10.1007/s11306-010-0239-2.
  31. Lavrov, D. V., X. Wang & M. Kelly, 2008. Reconstructing ordinal relationships in the Demospongiae using mitochondrial genomic data. Molecular Phylogenetics and Evolution 49: 111–124.PubMedCrossRefGoogle Scholar
  32. Lendenfeld, R. V., 1887. On the systematic position and classification of sponges. Proceedings of the Zoological Society of London 1887: 558–662.Google Scholar
  33. Lévi, C., 1956. Etude des Halisarca de Roscoff. Embryologie et systématique des démosponges. Archives de Zoology Experimentale et Generale 93: 1–184.Google Scholar
  34. Lévi, C., 1973. Systématique de la classe des Demospongiaria (Démosponges). In Grassé, P. P. (ed.), Spongiaires. Masson & Compagnie, Paris: 577–632.Google Scholar
  35. Leys, S. P., S. A. Nichols & E. D. M. Adams, 2009. Epithelia and integration in sponges. Integrative and Comparative Biology 49: 167–177.PubMedCrossRefGoogle Scholar
  36. Maldonado, M. & A. Riesgo, 2007. Intraepithelial spicules in a homosclerophorid sponge. Cell and Tissue Research 328: 639–650.PubMedCrossRefGoogle Scholar
  37. Maldonado, M. & A. Riesgo, 2008. Reproductive output in a Mediterranean population of the homosclerophorid Corticium candelabrum (Porifera, Demospongiae), with notes on the ultrastructure and behavior of the larva. Marine Ecology 29: 298–316.CrossRefGoogle Scholar
  38. Manuel, M., C. Borchiellini, E. Alivon, Y. Le Parco, J. Vacelet & N. Boury-Esnault, 2003. Phylogeny and evolution of calcareous sponges: monophyly of Calcinea and Calcaronea, high level of morphological homoplasy, and the primitive nature of axial symmetry. Systematic Biology 52: 311–333.PubMedCrossRefGoogle Scholar
  39. Moraes, F. C. & G. Muricy, 2003. Taxonomy of Plakortis and Plakinastrella (Demospongiae: Plakinidae) from oceanic islands off north-eastern Brazil, with description of three new species. Journal of the Marine Biological Association of the United Kingdom 83: 385–397.CrossRefGoogle Scholar
  40. Muricy, G., 1999. An evaluation of morphological and cytological data sets for the phylogeny of Homosclerophorida (Porifera: Demospongiae). Memoirs of the Queensland Museum 44: 399–409.Google Scholar
  41. Muricy, G., 2011. Diversity of Indo-Australian Plakortis (Demospongiae: Plakinidae), with description of four new species. Journal of the Marine Biological Association of the United Kingdom 91: 303–319.CrossRefGoogle Scholar
  42. Muricy, G. & M. C. Diaz, 2002. Order Homosclerophorida Dendy, 1905, Family Plakinidae Schulze, 1880. In Systema Porifera. In Hooper, J. N. A. & R. W. M. Van Soest (eds), A Guide to the Classification of Sponges. Kluwer Academic/Plenum Publishers, New York: 71–82.Google Scholar
  43. Muricy, G. & J. S. Pearse, 2004. A new species of Oscarella (Demospongiae: Plakinidae) from California. Proceedings of the California Academy of Sciences 55: 598–612.Google Scholar
  44. Muricy, G., N. Boury-Esnault, C. Bézac & J. Vacelet, 1998. Taxonomic revision of the Mediterranean Plakina Schulze (Porifera, Demospongiae, Homoscleromorpha). Zoological Journal of the Linnean Society 124: 169–203.CrossRefGoogle Scholar
  45. Pérez, T., J. Ivanisevic, M. Dubois, L. Pedel, O. P. Thomas, D. Tokina & A. V. Ereskovsky, 2011. Oscarella balibaloi, a new sponge species (Homoscleromorpha: Plakinidae) from the Western Mediterranean Sea: cytological description, reproductive cycle and ecology. Marine Ecology 32: 174–187.CrossRefGoogle Scholar
  46. Philippe, H., R. Derelle, P. Lopez, K. Pick, C. Borchiellini, N. Boury-Esnault, J. Vacelet, E. Renard, E. Houliston, E. Queinnec, C. Da Silva, P. Wincker, H. Le Guyader, S. Leys, D. J. Jackson, F. Schreiber, D. Erpenbeck, B. Morgenstern, G. Wörheide & M. Manuel, 2009. Phylogenomics revives traditional views on deep animal relationships. Current Biology 19: 706–712.PubMedCrossRefGoogle Scholar
  47. Pick, K. S., H. Philippe, F. Schreiber, D. Erpenbeck, D. J. Jackson, P. Wrede, M. Wiens, A. Alié, B. Morgenstern, M. Manuel & G. Wörheide, 2010. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Molecular Biology and Evolution 27: 1983–1987. doi: 10.1093/molbev/msq089.PubMedCrossRefGoogle Scholar
  48. Riesgo, A., M. Maldonado & M. Durfort, 2007. Dynamics of gametogenesis, embryogenesis, and larval release in a Mediterranean homosclerophorid demosponge. Marine and Freshwater Research 58: 398–417.CrossRefGoogle Scholar
  49. Schmidt, O., 1862. Die Spongien des Adriatischen Meeres. Verlag Von Wilhelm Engelmann, Leipzig: 88.Google Scholar
  50. Schulze, F. E., 1880. Untersuchungen über den Bau und die Entwicklung der Spongien. Neunte Mittheilung. Die Plakiniden. Zeitschrift fur Wissenschaftliche Zoologie Abt A 34: 407–451.Google Scholar
  51. Solé Cava, A. M., N. Boury-Esnault, J. Vacelet & J. P. Thorpe, 1992. Biochemical genetic divergence and systematics in sponges of the genera Corticium and Oscarella (Demospongiae: Homoscleromorpha) in the Mediterranean Sea. Marine Biology 113: 299–304.Google Scholar
  52. Sollas, W. J., 1885. A classification of the sponges. Annals and Magazine of Natural History 5: 395.CrossRefGoogle Scholar
  53. Sperling, E. A., K. J. Peterson & D. Pisani, 2009. Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Molecular Biology and Evolution 26: 2261–2274.PubMedCrossRefGoogle Scholar
  54. Topsent, E., 1897. Spongiaires de la Baie d’Amboine. (Voyage de MM. M. Bedot et C. Pictet dans l’Archipel Malais). Revue Suisse de Zoology 4: 421–487.Google Scholar
  55. Uriz, M. J., 2006. Mineral skeletogenesis in sponges. Canadian Journal of Zoology 84: 322–356.CrossRefGoogle Scholar
  56. Van Soest, R., 2011. Homoscleromorpha. In: Van Soest, R. W. M., N. Boury-Esnault, J. N. A. Hooper, K. Rützler, N. J. de Voogd, B. Alvarez de Glasby, E. Hajdu, A. B. Pisera, R. Manconi, C. Schoenberg, D. Janussen, K. R. Tabachnick, M. Klautau, B. Picton, M. Kelly (eds), World Porifera database. http://www.marinespecies.org/porifera/porifera.php?p=taxdetails&id=131587, on April 26, 2011.
  57. Vosmaer, G. C. J., 1884. Studies on sponges: II–IV. Mitteilungen aus der Zoologischen Station zu Neapel 5: 483–493.Google Scholar
  58. Wang, X. & D. V. Lavrov, 2008. Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PLoS ONE 3: e2723.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Eve Gazave
    • 1
    • 3
  • Pascal Lapébie
    • 2
    • 3
  • Alexander V. Ereskovsky
    • 3
  • Jean Vacelet
    • 3
  • Emmanuelle Renard
    • 3
  • Paco Cárdenas
    • 4
  • Carole Borchiellini
    • 3
  1. 1.Institut Jacques MonodUniversité Paris Diderot, CNRS UMR 7592ParisFrance
  2. 2.Biologie du Développement, Observatoire OcéanologiqueUniversité Pierre et Marie Curie-Paris 6, CNRS UMR 7009Villefranche-sur-MerFrance
  3. 3.Centre d’Océanologie de Marseille, Station marine d’EndoumeAix-Marseille Université, CNRS UMR 6540-DIMARMarseilleFrance
  4. 4.Département Milieux et Peuplements AquatiquesMuséum National d’Histoire Naturelle, UMR 7208 “BOrEA”ParisFrance

Personalised recommendations