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

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.

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References

  • Baccetti, B., E. Gaino & M. Sara, 1986. A sponge with acrosome: Oscarella lobularis. Journal of Ultrastructure and molecular structure research 94: 195–198.

    Article  Google Scholar 

  • Bergquist, P. R., 1978. Sponges. Hutchinson & Co, London.

    Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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 

  • Boury-Esnault, N., A. V. Ereskovsky, C. Bezac & D. B. Tokina, 2003. Larval development in Homoscleromorpha (Porifera, Demospongiae). Invertebrate Biology 122: 187–202.

    Article  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

  • 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 

  • 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 

  • Dendy, A., 1905. Report on the sponges collected by Professor Herdman, at Ceylon, in 1902. Royal Society, London.

    Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • Ereskovsky, A. V., 2005. Comparative Embryology of Sponges (Porifera). Sanct-Petersburg University Press, Sanct-Petersburg.

    Google Scholar 

  • Ereskovsky, A. V., 2006. A new species of Oscarella (Demospongiae: Plakinidae) from the Western Sea of Japan. Zootaxa 1376: 37–51.

    Google Scholar 

  • Ereskovsky, A. V., 2010. The Comparative Embryology of Sponges. Springer-Verlag, Dordrecht, Heidelberg, London, New York.

    Book  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Ereskovsky, A. V. & D. B. Tokina, 2007. Asexual reproduction in homoscleromorph sponges (Porifera; Homoscleromorpha). Marine Biology 151: 425–434.

    Article  Google Scholar 

  • Ereskovsky, A. V. & P. Willenz, 2008. Larval development in Guancha arnesenae (Porifera, Calcispongiae, Calcinea). Zoomorphology 127: 175–187.

    Article  Google Scholar 

  • Ereskovsky, A. V., D. B. Tokina, C. Bezac & N. Boury-Esnault, 2007. Metamorphosis of Cinctoblastula Larvae (Homoscleromorpha, Porifera). Journal of Morphology 268: 518–528.

    PubMed  Article  Google Scholar 

  • 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 

  • 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.

    PubMed  Article  Google Scholar 

  • Erpenbeck, D. & G. Wörheide, 2007. On the molecular phylogeny of sponges. Zootaxa 1668: 107–126.

    Google Scholar 

  • 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 

  • Gallissian, M. F. & J. Vacelet, 1992. Ultrastructure of the oocyte and embryo of the calcified sponge, Petrobiona massiliana (Porifera, Calcarea). Zoomorphology 112: 133–141.

    Article  Google Scholar 

  • 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.

  • 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.

    PubMed  Article  Google Scholar 

  • Hooper JNA, van Soest RWM (2002) Systema Porifera: A Guide to the Classification of Sponges. New York: Kluwer Academic/Plenum Publishers.

  • 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 

  • 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.

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • Lendenfeld, R. V., 1887. On the systematic position and classification of sponges. Proceedings of the Zoological Society of London 1887: 558–662.

    Google Scholar 

  • Lévi, C., 1956. Etude des Halisarca de Roscoff. Embryologie et systématique des démosponges. Archives de Zoology Experimentale et Generale 93: 1–184.

    Google Scholar 

  • Lévi, C., 1973. Systématique de la classe des Demospongiaria (Démosponges). In Grassé, P. P. (ed.), Spongiaires. Masson & Compagnie, Paris: 577–632.

    Google Scholar 

  • Leys, S. P., S. A. Nichols & E. D. M. Adams, 2009. Epithelia and integration in sponges. Integrative and Comparative Biology 49: 167–177.

    PubMed  Article  Google Scholar 

  • Maldonado, M. & A. Riesgo, 2007. Intraepithelial spicules in a homosclerophorid sponge. Cell and Tissue Research 328: 639–650.

    PubMed  Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Schmidt, O., 1862. Die Spongien des Adriatischen Meeres. Verlag Von Wilhelm Engelmann, Leipzig: 88.

    Google Scholar 

  • 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 

  • 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 

  • Sollas, W. J., 1885. A classification of the sponges. Annals and Magazine of Natural History 5: 395.

    Article  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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 

  • Uriz, M. J., 2006. Mineral skeletogenesis in sponges. Canadian Journal of Zoology 84: 322–356.

    Article  CAS  Google Scholar 

  • 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.

  • Vosmaer, G. C. J., 1884. Studies on sponges: II–IV. Mitteilungen aus der Zoologischen Station zu Neapel 5: 483–493.

    Google Scholar 

  • Wang, X. & D. V. Lavrov, 2008. Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PLoS ONE 3: e2723.

    PubMed  Article  Google Scholar 

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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.

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Correspondence to Carole Borchiellini.

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Guest editors: M. Maldonado, X. Turon, M. A. Becerro & M. J. Uriz / Ancient animals, new challenges: developments in sponge research

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10750_2011_842_MOESM1_ESM.doc

Supplementary file 1: Alternative phylogenetic classification of Homoscleromorpha based on the draft PhyloCode Version 4c. (DOC 32 kb)

10750_2011_842_MOESM2_ESM.eps

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)

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Gazave, E., Lapébie, P., Ereskovsky, A.V. et al. No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera. Hydrobiologia 687, 3–10 (2012). https://doi.org/10.1007/s10750-011-0842-x

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Keywords

  • Porifera
  • New class
  • Homoscleromorpha
  • Oscarellidae
  • Plakinidae
  • PhyloCode