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Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Integrative taxonomy widens our knowledge of the diversity, distribution and biology of the genus Plakina (Homosclerophorida: Plakinidae)

Guilherme Muricy https://orcid.org/0000-0002-1705-3673 A F , Celso Domingos A E , Anaíra Lage A , Emilio Lanna B , Cristiane C. P. Hardoim A C D , Marinella S. Laport C and Carla Zilberberg E *
+ Author Affiliations
- Author Affiliations

A Departamento de Invertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro (UFRJ). Quinta da Boa Vista, s/no, São Cristóvão, CEP 20940-040 Rio de Janeiro, RJ, Brazil.

B Laboratório de Embriologia e Biologia Reprodutiva, Instituto de Biologia, Universidade Federal da Bahia (UFBA), CEP 40170-115, Salvador, BA, Brazil.

C Laboratório de Bacteriologia Molecular e Marinha, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro (UFRJ), CEP 21941-902, Rio de Janeiro, RJ, Brazil.

D Current address: Laboratório de Interações Hospedeiro-Microbiota, Instituto de Biociências, Universidade Estadual Paulista (UNESP), Praça Infante Dom Henrique s/n°- Parque Bitaru, CEP 11380-972, São Vicente, SP, Brazil.

E Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro (UFRJ), CEP 21941-090, Rio de Janeiro, RJ, Brazil.

F Corresponding author. Email: muricy@mn.ufrj.br

Invertebrate Systematics 33(2) 367-401 https://doi.org/10.1071/IS18027
Submitted: 27 March 2018  Accepted: 4 August 2018   Published: 9 April 2019

Abstract

Despite the evolutionary significance of Homoscleromorpha, their diversity and biology are largely unknown. Here we integrate data of morphology, cytology, microbiology, ecology, reproduction, and mitochondrial cox-1 and cob gene sequences to resolve a complex of sympatric species of Plakina in South-eastern Brazil. All datasets congruently supported the delimitation of three species, two of which are new to science. Plakina coerulea has its distribution extended from one locality to over 2360 km wide. Plakina cabofriense, sp. nov. also occurs in North-eastern Brazil. Plakina cyanorosea, sp. nov. occurs only in a single, small tide pool and may be critically endangered. Plakina cyanorosea, sp. nov. produces conspicuous, abundant larvae useful for laboratory investigations. A thin, bright orange organic coat covers some spicules of P. cabofriense, sp. nov. and P. cyanorosea, sp. nov. The three Plakina species harbour diverse microbial symbiont communities, including previously unknown morphologies. Molecular phylogenies and barcoding gaps based on cox-1 and cob sequences supported that each species is monophyletic and distinct from other congeners. The genus Plakina is paraphyletic and strongly needs redefinition. The integrative approach provides new data that widens our knowledge of Homoscleromorpha diversity, distribution and biology.

Additional keywords: Brazil, cox-1, cob, cytology, ecology, Homoscleromorpha, microbiology, morphology, Porifera, reproduction, SW Atlantic.


References

Agarwala, R., Barrett, T., Beck, J., Benson, D. A., Bollin, C., Bolton, E., Bourexis, D., Brister, J. R., Bryant, S. H., Canese, K., Charowhas, C., Clark, K., DiCuccio, M., Dondoshansky, I., Federhen, S., Feolo, M., Funk, K., Geer, L. Y., Gorelenkov, V., Hoeppner, M., Holmes, B., Johnson, M., Khotomlianski, V., Kimchi, A., Kimelman, M., Kitts, P., Klimke, W., Krasnov, S., Kuznetsov, A., Landrum, M. J., Landsman, D., Lee, J. M., Lipman, D. J., Lu, Z., Madden, T. L., Madej, T., Marchler-Bauer, A., Karsch-Mizrachi, I., Murphy, T., Orris, R., Ostell, J., O’Sullivan, C., Panchenko, A., Phan, L., Preuss, D., Pruitt, K. D., Rodarmer, K., Rubinstein, W., Sayers, E. W., Schneider, V., Schuler, G. D., Sherry, S. T., Sirotkin, K., Siyan, K., Slotta, D., Soboleva, A., Soussov, V., Starchenko, G., Tatusova, T. A., Todorov, K., Trawick, B. W., Vakatov, D., Wang, Y., Ward, M., Wilbur, W. J., Yaschenko, E., and Zbicz, K. (2016). Database resources of the National Centre for Biotechnology Information. Nucleic Acids Research 44, D7–D19.
Database resources of the National Centre for Biotechnology Information.Crossref | GoogleScholarGoogle Scholar |

Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J. H., Zhang, Z., Miller, W., and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.Crossref | GoogleScholarGoogle Scholar | 9254694PubMed |

Baccetti, B., Gaino, E., and Sarà, M. (1986). A sponge with acrosome: Oscarella lobularis. Journal of Ultrastructure and Molecular Structure Research 94, 195–198.
A sponge with acrosome: Oscarella lobularis.Crossref | GoogleScholarGoogle Scholar |

Belmonte, T., Alvim, J., Padula, V., and Muricy, G. (2015). Spongivory by nudibranchs on the coast of Rio de Janeiro state, southeastern Brazil. Spixiana 38, 187–195.

Borchiellini, C., Manuel, M., Alivon, E., Boury-Esnault, N., Vacelet, J., and Le Parco, Y. (2000). Sponge paraphyly and the origin of Metazoa. Journal of Evolutionary Biology 14, 171–179.
Sponge paraphyly and the origin of Metazoa.Crossref | GoogleScholarGoogle Scholar |

Borchiellini, C., Chombard, C., Manuel, M., Alivon, E., Vacelet, J., and Boury-Esnault, N. (2004). Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution. Molecular Phylogenetics and Evolution 32, 823–837.
Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution.Crossref | GoogleScholarGoogle Scholar | 15288059PubMed |

Boury-Esnault, N. (1973). Résultats scientifiques des campagnes de la ‘Calypso’. Campagne de la ‘Calypso’ au large des côtes atlantiques de l’Amérique du Sud (1961–1962). Spongiaires. Résultats Scientifiques des Campagnes de la ‘Calypso’ 10, 263–295.

Boury-Esnault, N. (2002). Order Chondrosida Boury-Esnault and Lopes, 1985. Family Chondrillidae Gray, 1872. In ‘Systema Porifera. A Guide to the Classification of Sponges. Vol. 1’. (Eds J. N. A. Hooper and R. W. M. van Soest.) pp. 291–298. (Kluwer Academic/Plenum Publishers: New York.)

Boury-Esnault, N., Solé-Cava, A. M., and Thorpe, J. P. (1992). Genetic and cytological divergence between colour morphs of the Mediterranean sponge Oscarella lobularis Schmidt (Porifera, Demospongiae, Oscarellidae). Journal of Natural History 26, 271–284.
Genetic and cytological divergence between colour morphs of the Mediterranean sponge Oscarella lobularis Schmidt (Porifera, Demospongiae, Oscarellidae).Crossref | GoogleScholarGoogle Scholar |

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.
Sponges without skeleton: a new Mediterranean genus of Homoscleromorpha (Porifera, Demospongiae).Crossref | GoogleScholarGoogle Scholar |

Boury-Esnault, N., Lavrov, D. V., Ruiz, C. A., and Pérez, T. (2013). The integrative taxonomic approach applied to Porifera: a case study of the Homoscleromorpha. Integrative and Comparative Biology 53, 416–427.
The integrative taxonomic approach applied to Porifera: a case study of the Homoscleromorpha.Crossref | GoogleScholarGoogle Scholar | 23670632PubMed |

Boute, N., Exposito, J. Y., Boury-Esnault, N., Vacelet, J., Noro, N., Miyazaki, K., Yoshizato, K., and Garrone, R. (1996). Type IV collagen in sponges, the missing link in basement membrane ubiquity. Biologie Cellulaire 88, 37–44.
Type IV collagen in sponges, the missing link in basement membrane ubiquity.Crossref | GoogleScholarGoogle Scholar |

Cedro, V. R., Hajdu, E., and Correia, M. D. (2013). Three new intertidal sponges (Porifera: Demospongiae) from Brazil’s fringing urban reefs (Maceió, Alagoas, Brazil), and support for Rhabderemia’s exclusion from Poecilosclerida. Journal of Natural History 47, 2151–2174.
Three new intertidal sponges (Porifera: Demospongiae) from Brazil’s fringing urban reefs (Maceió, Alagoas, Brazil), and support for Rhabderemia’s exclusion from Poecilosclerida.Crossref | GoogleScholarGoogle Scholar |

Cruz-Barraza, J. A., Vega, C., and Carballo, J. L. (2014). Taxonomy of family Plakinidae (Porifera: Homoscleromorpha) from eastern Pacific coral reefs, through morphology and cox1 and cob mtDNA data. Zoological Journal of the Linnean Society 171, 254–276.
Taxonomy of family Plakinidae (Porifera: Homoscleromorpha) from eastern Pacific coral reefs, through morphology and cox1 and cob mtDNA data.Crossref | GoogleScholarGoogle Scholar |

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 22847109PubMed |

Dayrat, B. (2005). Towards an integrative taxonomy. Biological Journal of the Linnean Society. Linnean Society of London 85, 407–415.
Towards an integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |

De Vos, L., Rützler, K., Boury-Esnault, N., Donadey, C., and Vacelet, J. (1991). ‘Atlas of Sponge Morphology. Atlas de Morphologie des Éponges.’ (Smithsonian Institution Press: Washington, DC, USA.)

DeSalle, R., Egan, M. G., and Siddall, M. (2005). The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 1905–1916.
The unholy trinity: taxonomy, species delimitation and DNA barcoding.Crossref | GoogleScholarGoogle Scholar | 16214748PubMed |

Desqueyroux-Faúndez, R., and van Soest, R. W. M. (1997). Shallow water Demosponges of the Galápagos Islands. Revue Suisse de Zoologie 104, 379–467.
Shallow water Demosponges of the Galápagos Islands.Crossref | GoogleScholarGoogle Scholar |

Domingos, C., Lage, A., and Muricy, G. (2016). Overview of the biodiversity and distribution of the Class Homoscleromorpha in the tropical western Atlantic. Journal of the Marine Biological Association of the United Kingdom 96, 379–389.
Overview of the biodiversity and distribution of the Class Homoscleromorpha in the tropical western Atlantic.Crossref | GoogleScholarGoogle Scholar |

Ereskovsky, A. V., Tokina, D. B., Bézac, C., and Boury-Esnault, N. (2007). Metamorphosis of cinctoblastula larvae (Homoscleromorpha, Porifera). Journal of Morphology 268, 518–528.
Metamorphosis of cinctoblastula larvae (Homoscleromorpha, Porifera).Crossref | GoogleScholarGoogle Scholar | 17427974PubMed |

Ereskovsky, A. V., Borchiellini, C., Gazave, E., Ivanisevic, J., Lapébie, P., Pérez, T., Renard, E., and Vacelet, J. (2009). The Homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology. BioEssays 31, 89–97.
The Homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology.Crossref | GoogleScholarGoogle Scholar | 19154007PubMed |

Ereskovsky, A. V., Lavrov, D. V., and Willenz, P. (2014). Five new species of Homoscleromorpha (Porifera) from the Caribbean Sea and re-description of Plakina jamaicensis. Journal of the Marine Biological Association of the United Kingdom 94, 285–307.
Five new species of Homoscleromorpha (Porifera) from the Caribbean Sea and re-description of Plakina jamaicensis.Crossref | GoogleScholarGoogle Scholar |

Ereskovsky, A. V., Richter, D. J., Lavrov, D. V., Schippers, K. J., and Nichols, S. A. (2017). Transcriptome sequencing and delimitation of sympatric Oscarella species (O. carmela and O. pearsei sp. nov.) from California, USA. PLoS One 12, e0183002.
Transcriptome sequencing and delimitation of sympatric Oscarella species (O. carmela and O. pearsei sp. nov.) from California, USA.Crossref | GoogleScholarGoogle Scholar | 28892487PubMed |

Feuda, R., Dohrmann, R., Pett, W., Philippe, H., Rota-Stabelli, O., Lartillot, N., Wörheide, G., and Pisani, D. (2017). Improved modeling of compositional heterogeneity supports sponges as sister to all other animals. Current Biology 27, 3864–3870.
Improved modeling of compositional heterogeneity supports sponges as sister to all other animals.Crossref | GoogleScholarGoogle Scholar | 29199080PubMed |

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 7881515PubMed |

Fukami, H., Budd, A. F., Levitan, D. R., Jara, J., Kersanach, R., and Knowlton, N. (2004). Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58, 324–337.
Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers.Crossref | GoogleScholarGoogle Scholar | 15068349PubMed |

Gazave, E., Lapébie, P., Renard, E., Vacelet, J., Rocher, C., Ereskovsky, A. V., Lavrov, D. V., and Borchiellini, C. (2010). Molecular phylogeny restores the supra-generic subdivision of homoscleromorph sponges (Porifera, Homoscleromorpha). PLoS One 5, e14290.
Molecular phylogeny restores the supra-generic subdivision of homoscleromorph sponges (Porifera, Homoscleromorpha).Crossref | GoogleScholarGoogle Scholar | 21179486PubMed |

Gazave, E., Lapébie, P., Ereskovsky, A. V., Vacelet, J., Renard, E., Cárdenas, P., and Borchiellini, C. (2012). No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera. Hydrobiologia 687, 3–10.
No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera.Crossref | GoogleScholarGoogle Scholar |

Gazave, E., Lavrov, D. V., Cabrol, J., Renard, E., Rocher, C., Vacelet, J., Adamska, M., Borchiellini, C., and Ereskovsky, A. V. (2013). Systematics and molecular phylogeny of the Oscarellidae family (Homoscleromorpha) with description of two new Oscarella species. PLoS One 8, e63976.
Systematics and molecular phylogeny of the Oscarellidae family (Homoscleromorpha) with description of two new Oscarella species.Crossref | GoogleScholarGoogle Scholar | 23737959PubMed |

Gloeckner, V., Hentschel, U., Ereskovsky, A. V., and Schmitt, S. (2013). Unique and species-specific microbial communities in Oscarella lobularis and other Mediterranean Oscarella species (Porifera: Homoscleromorpha). Marine Biology 160, 781–791.
Unique and species-specific microbial communities in Oscarella lobularis and other Mediterranean Oscarella species (Porifera: Homoscleromorpha).Crossref | GoogleScholarGoogle Scholar |

Gloeckner, V., Wehrl, M., Moitinho-Silva, L., Gernert, C., Schupp, P., Pawlik, J. R., Lindquist, N. L., Erpenbeck, D., Wörheide, G., and Hentschel, U. (2014). The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. The Biological Bulletin 227, 78–88.
The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species.Crossref | GoogleScholarGoogle Scholar | 25216505PubMed |

Guindon, S., and Gascuel, O. (2003). A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52, 696–704.
A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood.Crossref | GoogleScholarGoogle Scholar | 14530136PubMed |

Hajdu, E., and Lopes, D. A. (2007). Checklist of Brazilian deep-sea sponges. In ‘Porifera Research: Biodiversity, Innovation and Sustainability’. (Eds M.R. Custódio, G. Lobo-Hajdu, E. Hajdu, and G. Muricy.) pp. 353–359. Série Livros 28. (Museu Nacional: Rio de Janeiro, Brazil.)

Huelsenbeck, J. P., and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
MrBayes: Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar | 11524383PubMed |

Lage, A., Gerovasileiou, V., Voultsiadou, E., and Muricy, G. (2018). Taxonomy of Plakina (Porifera: Homoscleromorpha) from Aegean submarine caves, with descriptions of three new species and new characters for the genus. Marine Biodiversity , .
Taxonomy of Plakina (Porifera: Homoscleromorpha) from Aegean submarine caves, with descriptions of three new species and new characters for the genus.Crossref | GoogleScholarGoogle Scholar |

Lavrov, D. V., Wang, X., and Kelly, M. (2008). Reconstructing ordinal relationships in the Demospongiae using mitochondrial genomic data. Molecular Phylogenetics and Evolution 49, 111–124.
Reconstructing ordinal relationships in the Demospongiae using mitochondrial genomic data.Crossref | GoogleScholarGoogle Scholar | 18583159PubMed |

Marcus, E., and Marcus, E. (1967). American opisthobranch mollusks. Part I. Tropical American opisthobranchs. Part II. Opisthobranchs from the Gulf of California. Studies in Tropical Oceanography 6, 1–256.

Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE) 2010’, 14 November 2010, New Orleans, LA, USA. pp. 1–8. 10.1109/GCE.2010.5676129

Miralles, A., and Vences, M. (2013). New metrics for comparison of taxonomies reveal striking discrepancies among species delimitation methods in Madascincus lizards. PLoS One 8, e68242.
New metrics for comparison of taxonomies reveal striking discrepancies among species delimitation methods in Madascincus lizards.Crossref | GoogleScholarGoogle Scholar | 23874561PubMed |

Moraes, F. C., Ventura, M., Klautau, M., Hajdu, E., and Muricy, G. (2006). Biodiversidade de esponjas das ilhas oceânicas brasileiras. In ‘Ilhas Oceânicas Brasileiras: da pesquisa ao manejo’. (Eds R. J. V. Alves and J. W. A. Castro.) pp. 147–178. (Ministério do Meio Ambiente: Brasília, Brazil.)

Muricy, G., and Díaz, M. C. (2002). Order Homosclerophorida Dendy, 1905, family Plakinidae Schulze, 1880. In ‘Systema Porifera. A Guide to the Classification of Sponges. Vol. 1’. (Eds J. N. A. Hooper and R. W. M. van Soest.) pp. 71–82. (Kluwer Academic/Plenum Publishers: New York.)

Muricy, G., and Moraes, F. C. (1998). Marine sponges of Pernambuco State, NE Brazil. Revista Brasileira de Oceanografia 46, 213–217.
Marine sponges of Pernambuco State, NE Brazil.Crossref | GoogleScholarGoogle Scholar |

Muricy, G., Boury-Esnault, N., Bézac, C., and Vacelet, J. (1996a). Cytological evidence for cryptic speciation in Mediterranean Oscarella species (Porifera, Homoscleromorpha). Canadian Journal of Zoology 74, 881–896.
Cytological evidence for cryptic speciation in Mediterranean Oscarella species (Porifera, Homoscleromorpha).Crossref | GoogleScholarGoogle Scholar |

Muricy, G., Solé-Cava, A. M., Thorpe, J. P., and Boury-Esnault, N. (1996b). Genetic evidence for extensive cryptic speciation in the subtidal sponge Plakina trilopha (Porifera: Demospongiae: Homoscleromorpha) from the Western Mediterranean. Marine Ecology Progress Series 138, 181–187.
Genetic evidence for extensive cryptic speciation in the subtidal sponge Plakina trilopha (Porifera: Demospongiae: Homoscleromorpha) from the Western Mediterranean.Crossref | GoogleScholarGoogle Scholar |

Muricy, G., Boury-Esnault, N., Bézac, C., and Vacelet, J. (1998). Taxonomic revision of the Mediterranean Plakina Schulze (Porifera, Demospongiae, Homoscleromorpha). Zoological Journal of the Linnean Society 124, 169–203.
Taxonomic revision of the Mediterranean Plakina Schulze (Porifera, Demospongiae, Homoscleromorpha).Crossref | GoogleScholarGoogle Scholar |

Muricy, G., Bézac, C., Gallissian, M. F., and Boury-Esnault, N. (1999). Anatomy, cytology and symbiotic bacteria of four Mediterranean species of Plakina (Demospongiae: Homosclerophorida). Journal of Natural History 33, 159–176.
Anatomy, cytology and symbiotic bacteria of four Mediterranean species of Plakina (Demospongiae: Homosclerophorida).Crossref | GoogleScholarGoogle Scholar |

Muricy, G., Santos, C. P., Batista, D., Lopes, D. A., Pagnoncelli, D., Monteiro, L. C., Oliveira, M. V., Moreira, M. C. F., Carvalho, M. de S., Melão, M., Klautau, M., Rodriguez, P. R. D., Costa, R. N., Silvano, R. G., Schwientek, S., Ribeiro, S. M., Pinheiro, U. S., and Hajdu, E. (2006). Filo Porifera. In ‘Biodiversidade Bentônica da Região Central da Zona Econômica Exclusiva Brasileira’. (Eds H. P. Lavrado and B. L. Ignacio.) pp. 109–145. (Série Livros 18, Museu Nacional: Rio de Janeiro, Brazil.)

Muricy, G., Lopes, D.A., Hajdu, E., Carvalho, M.S., Moraes, F.C., Klautau, M., Menegola, C., and Pinheiro, U.S. (2011). ‘Catalogue of Brazilian Porifera.’ (Série Livros 46, Museu Nacional: Rio de Janeiro, Brazil.)

Nielsen, C. (2008). Six major steps in animal evolution: are we derived sponge larvae? Evolution & Development 10, 241–257.
Six major steps in animal evolution: are we derived sponge larvae?Crossref | GoogleScholarGoogle Scholar |

Nielsen, C. (2012). ‘Animal Evolution: Interrelationships of the Living Phyla.’ 3rd edn. (Oxford University Press: Oxford, UK.)

Padial, J., Miralles, A., de la Riva, I., and Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology 7, 1–14.
The integrative future of taxonomy.Crossref | GoogleScholarGoogle Scholar |

Pérez, T., and Ruiz, C. (2018). Description of the first Caribbean Oscarellidae (Porifera: Homoscleromorpha). Zootaxa 4369, 501–514.
Description of the first Caribbean Oscarellidae (Porifera: Homoscleromorpha).Crossref | GoogleScholarGoogle Scholar | 29689869PubMed |

Pérez, T., Ivanišević, J., Dubois, M., Pedel, L., Thomas, O. P., Tokina, D., and Ereskovsky, A. V. (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.
Oscarella balibaloi, a new sponge species (Homoscleromorpha: Plakinidae) from the western Mediterranean Sea: cytological description, reproductive cycle and ecology.Crossref | GoogleScholarGoogle Scholar |

Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G. (2012). ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
ABGD, automatic barcode gap discovery for primary species delimitation.Crossref | GoogleScholarGoogle Scholar | 21883587PubMed |

Reveillaud, J., Allewaert, C., Pérez, T., Vacelet, J., Banaigs, B., and Vanreusel, A. (2012). Relevance of an integrative approach for taxonomic revision in sponge taxa: case study of the shallow-water Atlanto-Mediterranean Hexadella species (Porifera: Ianthellidae: Verongida). Invertebrate Systematics 26, 230–248.
Relevance of an integrative approach for taxonomic revision in sponge taxa: case study of the shallow-water Atlanto-Mediterranean Hexadella species (Porifera: Ianthellidae: Verongida).Crossref | GoogleScholarGoogle Scholar |

Rodríguez, F., Oliver, J. L., Marin, A., and Medina, J. R. (1990). The general stochastic-model of nucleotide substitution. Journal of Theoretical Biology 142, 485–501.
The general stochastic-model of nucleotide substitution.Crossref | GoogleScholarGoogle Scholar | 2338834PubMed |

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 12912839PubMed |

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |

Ruiz, C., Ivanišević, J., Chevaldonné, P., Ereskovsky, A. V., Boury-Esnault, N., Vacelet, J., Thomas, O. P., and Pérez, T. (2015). Integrative taxonomic description of Plakina kanaky, a new polychromatic sponge species from New Caledonia (Porifera: Homoscleromorpha). Marine Ecology (Berlin) 36, 1129–1143.
Integrative taxonomic description of Plakina kanaky, a new polychromatic sponge species from New Caledonia (Porifera: Homoscleromorpha).Crossref | GoogleScholarGoogle Scholar |

Ruiz, C., Muricy, G., Lage, A., Domingos, C., Chenesseau, S., and Pérez, T. (2017). Descriptions of new sponge species and genus, including aspiculate Plakinidae, overturn the Homoscleromorpha classification. Zoological Journal of the Linnean Society 179, 707–724.
Descriptions of new sponge species and genus, including aspiculate Plakinidae, overturn the Homoscleromorpha classification.Crossref | GoogleScholarGoogle Scholar |

Schmidt, O. (1862). ‘Die Spongien des Adriatischen Meeres.’ (Wilhelm Engelmann: Leipzig, Germany.)

Schulze, F. E. (1880). Untersuchungen über den Bau und die Entwicklung der Spongien. Neunte Mittheilung. Die Plakiniden. Zeitschrift fur Wissenschartliche Zoologie 34, 407–451.

Simion, P., Philippe, H., Baurain, D., Jager, M., Richter, D. J., di Franco, A., Roure, B., Satoh, N., Queinnec, E., Ereskovsky, A., Lapébie, P., Corre, E., Delsuc, F., King, N., Wörheide, G., and Manuel, M. (2017). A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Current Biology 27, 958–967.
A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals.Crossref | GoogleScholarGoogle Scholar | 28318975PubMed |

Spalding, M. D., Fox, H. E., Allen, G. R., Davidson, N., Ferdaña, Z. A., Finlayson, M., Halpern, B. S., Jorge, M. A., Lombana, A., Lourie, S. A., Martin, K. D., McManus, E., Molnar, J., Recchia, C. A., and Robertson, J. (2007). Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57, 573–583.
Marine ecoregions of the world: a bioregionalization of coastal and shelf areas.Crossref | GoogleScholarGoogle Scholar |

Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar | 24451623PubMed |

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 24132122PubMed |

Topsent, E. (1895). Étude monographique des Spongiaires de France. II. Carnosa. Archives de Zoologie expérimentale et générale 3, 493–590.

Turque, A. S., Cardoso, A. M., Silveira, C. B., Vieira, R. P., Freitas, F. A. D., Albano, R. M., Gonzalez, A. M., Paranhos, R., Muricy, G., and Martins, O. B. (2008). Bacterial communities of the marine sponges Hymeniacidon heliophila and Polymastia janeirensis and their environment in Rio de Janeiro, Brazil. Marine Biology 155, 135–146.
Bacterial communities of the marine sponges Hymeniacidon heliophila and Polymastia janeirensis and their environment in Rio de Janeiro, Brazil.Crossref | GoogleScholarGoogle Scholar |

Vacelet, J. (1971). L’ultrastructure de la cuticule d’éponges cornées du genre Verongia. Journal de Microscopie 10, 113–116.

Vacelet, J., Pérez, T., and Hooper, J. N. A. (2002). Demospongiae incertae sedis. In ‘Systema Porifera. A Guide to the Classification of Sponges. Vol. 1’. (Eds J. N. A. Hooper and R. W. M. van Soest.) pp. 1099–1101. (Kluwer Academic/Plenum Publishers: New York.)

van Soest, R. W. M., Boury-Esnault, N., Hooper, J. N. A., Rützler, K., de Voogd, N. J., Alvarez, B., Hajdu, E., Pisera, A. B., Manconi, R., Schönberg, C., Klautau, M., Picton, B., Kelly, M., Vacelet, J., Dohrmann, M., Díaz, M. C., Cárdenas, P., Carballo, J. L., Ríos, P., and Downey, R. (2018). World Porifera database. Available at http://www.marinespecies.org/porifera [verified 13 February 2018].

Vosmaer, G. C. J. (1884). Porifera. In ‘Die Klassen und Ordnungen des Thierreichs’. (Ed. H. G. Bronn.) Vol. II, 65–176.

Wang, X., and Lavrov, D. V. (2007). Mitochondrial genome of the homoscleromorph Oscarella carmela (Porifera, Demospongiae) reveals unexpected complexity in the common ancestor of sponges and other animals. Molecular Biology and Evolution 24, 363–373.
Mitochondrial genome of the homoscleromorph Oscarella carmela (Porifera, Demospongiae) reveals unexpected complexity in the common ancestor of sponges and other animals.Crossref | GoogleScholarGoogle Scholar | 17090697PubMed |

Wang, X., and Lavrov, D. V. (2008). Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PLoS ONE 3, E2723.
Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae.Crossref | GoogleScholarGoogle Scholar | 18628961PubMed |

Willenz, P., Ereskovsky, A. V., and Lavrov, D. V. (2016). Integrative taxonomic re-description of Halisarca magellanica and description of a new species of Halisarca (Porifera, Demospongiae) from Chilean Patagonia. Zootaxa 4208, 501–533.
Integrative taxonomic re-description of Halisarca magellanica and description of a new species of Halisarca (Porifera, Demospongiae) from Chilean Patagonia.Crossref | GoogleScholarGoogle Scholar |