No longer Demospongiae: Homoscleromorph formal nimination as a fourth class of porifera Eve Gazave, Pascal Lapébie, Alexander Ereskovsky, Jean Vacelet, Emmanuelle Renard, Paco Cárdenas, Carole Borchiellini To cite this version: Eve Gazave, Pascal Lapébie, Alexander Ereskovsky, Jean Vacelet, Emmanuelle Renard, et al.. No longer Demospongiae: Homoscleromorph formal nimination as a fourth class of porifera. Hydrobiolo- gia, Springer, 2012, 687 (1), pp.3 - 10. 10.1007/s10750-011-0842-x. hal-01456632 HAL Id: hal-01456632 https://hal.archives-ouvertes.fr/hal-01456632 Submitted on 13 Apr 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Hydrobiologia (2012) 687:3–10 DOI 10.1007/s10750-011-0842-x SPONGE RESEARCH DEVELOPMENTS Short Research Note No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera Eve Gazave • Pascal Lape´bie • Alexander V. Ereskovsky • Jean Vacelet • Emmanuelle Renard • Paco Ca´rdenas • Carole Borchiellini Received: 22 February 2011 / Accepted: 30 July 2011 / Published online: 12 August 2011 Ó Springer Science+Business Media B.V. 2011 Abstract Over the past few years, there has been Demospongiae and is composed of two families, growing interest among the sponge community in the Oscarellidae and Plakinidae. Within the currently phylogenetic position of the Homoscleromorpha (i.e. more widely accepted hypothesis of a monophyletic within or outside the class Demospongiae). Recent Porifera, we formally propose here to raise Homos- molecular analyses clearly show that the Homoscler- cleromorpha to the class rank (the fourth one). We, omorpha forms a distinct clade separated from the therefore, provide a definition and a formal diagnosis. In the supplementary materials, we also present an alternative classification of the Homoscleromorpha, Electronic supplementary material The online version of following the PhyloCode. this article (doi:10.1007/s10750-011-0842-x) contains supplementary material, which is available to authorized users. Keywords Porifera Á New class Á Homoscleromorpha Á Oscarellidae Á Plakinidae Á Guest editors: M. Maldonado, X. Turon, M. A. Becerro & PhyloCode M. J. Uriz / Ancient animals, new challenges: developments in sponge research E. Gazave Institut Jacques Monod, Universite´ Paris Diderot, Past and current systematics CNRS UMR 7592, Paris, France E. Gazave Á P. Lape´bie Á A. V. Ereskovsky Á For two decades now, phylogenies using genetic and J. Vacelet Á E. Renard Á C. Borchiellini (&) morphological data have provided crucial informa- Centre d’Oce´anologie de Marseille, Station marine tion toward resolving sponge systematics (Erpenbeck ´ d’Endoume, Aix-Marseille Universite, CNRS UMR &Wo¨rheide, 2007). While the phylogenetic status of 6540-DIMAR, Marseille, France e-mail: [email protected] Porifera (monophyly vs. paraphyly) is still debated (Philippe et al., 2009; Sperling et al., 2009), internal P. Lape´bie phylogenies for the major sponge groups (i.e. the ´ Biologie du Developpement, Observatoire three Recent classes: Demospongiae, Calcarea, and Oce´anologique, Universite´ Pierre et Marie Curie-Paris 6, CNRS UMR 7009, Villefranche-sur-Mer, France Hexactinellida) are becoming better resolved (Bor- chiellini et al., 2004; Dohrmann et al., 2006, 2008). P. Ca´rdenas However, the affinities and rank of Homoscleromor- ´ Departement Milieux et Peuplements Aquatiques, pha remain unresolved within the Linnaean classifi- Muse´um National d’Histoire Naturelle, UMR 7208 ‘‘BOrEA’’, Paris, France cation (Muricy, 1999; Muricy & Diaz, 2002). 123 4 Hydrobiologia (2012) 687:3–10 Traditionally, Homoscleromorpha has been classi- group relationship of Homoscleromorpha and calcare- fied as a family or a suborder of the subclass Tetract- ous sponges (Calcarea, also known as Calcispongia) inellida, within the class Demospongiae, mainly due to (Dohrmann et al., 2008; Philippe et al., 2009; Pick et al., the shared presence of siliceous tetractinal-like calthrop 2010)(Fig.1). Alternatively, homoscleromorphs were spicules (Le´vi, 1956). Le´vi (1973) later proposed recovered as the sister group of Eumetazoa, albeit with classifying them as a distinct subclass of the Demo- low statistical support (Sperling et al., 2009). Although spongiae. Until 1995, two families were recognized analysis of complete mitochondrial genomes seemingly within the Homoscleromorpha, Plakinidae Schulze, supported the traditional placement within the Demo- 1880 and Oscarellidae Lendenfeld, 1887, distinguished spongiae (Lavrov et al., 2008; Wang & Lavrov, 2008), by the presence or absence of the mineral skeleton, these studies were hampered by a lack of data from respectively. However, in 1990, the discovery of a Calcarea, preventing a true test of the phylogenetic skeleton-less Corticium-like species led Sole´ Cava et al. position of Homoscleromorpha. In any case, the number (1992) to propose the rejection of the family Oscarel- of homoscleromorph species included in the above- lidae. Later, when this species was described as a mentioned studies was very low (one or two). member of a new genus Pseudocorticium (Boury- Recently, molecular phylogenetic taxon sampling Esnault et al., 1995), all homoscleromorph genera were of Homoscleromorpha was substantially improved to merged into a single family, the Plakinidae. Pseudo- include 18S, 28S rDNA sequences and mitochondrial corticium is indeed devoid of a mineral skeleton like the genomes of six of the seven presently described genera genus Oscarella, but is more similar in histological traits (Gazave et al., 2010a). This study greatly contributed (notably the leuconoid aquiferous system and a well- to resolve internal relationships of the group, restored developed ectosome with cortex) to the spiculate genus the supra-generic classification of Homoscleromorpha Corticium. abandoned in 1995 (Boury-Esnault et al., 1995), and Nowadays, according to the two current synopses of reinstated the families Oscarellidae and Plakinidae on the poriferan classification, Systema Porifera (Hooper the basis of molecular and morphological evidence et al., 2002) and the World Porifera Database (http:// (Fig. 1). Uncertainties remain concerning the mono- www.marinespecies.org/porifera/;VanSoest,2011), phyly of Oscarella but it clearly appears that Corticium Homoscleromorpha is a subclass of the class Demo- and Plakinastrella are monophyletic genera. The spongiae, containing one order Homosclerophorida Plakina issue is more challenging and calls for further Dendy, 1905, one family Plakinidae Schulze, 1880, and detailed molecular investigations (Fig. 1). seven genera: Oscarella Vosmaer, 1884; Plakina Schulze, 1880; Plakortis Schulze, 1880; Plakinastrella Schulze, 1880; Corticium Schmidt, 1862; Pseudocorti- Linnaean classification of Homoscleromorpha cium Boury-Esnault et al., 1995; Placinolopha Topsent, 1897. Taking into account the recent molecular studies, we consider that it is now well-established that Homoscler- omorpha is not closely related to other demosponges. New insights from molecular phylogenies/ We feel that these new insights should be reflected in the phylogenomics studies Linnaean classification. In this classification system, the rank of both Homoscleromorpha and Calcarea is Since these two synopses were compiled, molecular directly dependent on the phylogenetic status of Porif- phylogenies have challenged these traditional classifi- era. The most complete and robust molecular study of cation schemes. Indeed, in 2004, the first molecular Porifera to date clearly supports the hypothesis of its phylogeny of an extensive sampling of Demospongiae monophyly, a hypothesis that is also consistent with sensu lato (based on 18S and 28S rDNA) suggested that morphological characters (Philippe et al., 2009; Pick Homoscleromorpha should form a clade on its own, et al., 2010). We thus formally propose, in the present clearly separated from the rest of the Demospongiae paper, to raise Homoscleromorpha from subclass within (Borchiellini et al., 2004). Subsequent phylogenic/ Demospongiae to a fourth Recent class of Porifera (there phylogenomic studies using several nuclear markers is also a fifth extinct class of Porifera, the Archaeocyatha corroborated this hypothesis and suggested a sister- e.g. Debrenne et al., 2002). 123 Hydrobiologia (2012) 687:3–10 5 Hexasterophora Hexactinellida Amphidiscophora G4 G3 Demospongiae G2 G1 Oscarella * Oscarellidae Pseudocorticium * Plakinastrella Homoscleromorpha Plakortis * Plakinidae Corticium Plakina * Calcinea Calcispongiae Calcaronea Outgroups Fig. 1 Porifera simplified tree, following the monophyly are not monophyletic or from which uncertainties subsist are hypothesis, mentioning the Linnaean names of the Homoscler- identified with an asterisk omorpha families and genera. Homoscleromorpha genera that Definition (modified from Hooper & Van Soest, Definition 2002) Porifera with cinctoblastula larvae and embryonic Class Homoscleromorpha Bergquist, 1978 incubation; flagellated exo- and endopinacocytes; a Other names. Microsclerophora Sollas, 1885. basement membrane