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The most diverse and species-rich class of the phylum Porifera is Demospongiae. In recent years, the systematics of this clade, which contains more than 7000 species, has developed rapidly in light of new studies combining molecular and morphological observations. We add more than 500 new, nearly complete 18S sequences (an increase of more than 200%) in an attempt to further enhance understanding of the phylogeny of Demospongiae. Our study specifically targets representation of type species and genera that have never been sampled for any molecular data in an effort to accelerate progress in classifying this diverse lineage. Our analyses recover four highly supported subclasses of Demospongiae: Keratosa, Myxospongiae, Haploscleromorpha, and Heteroscleromorpha. Within Keratosa, neither Dendroceratida, nor its two families, Darwinellidae and Dictyodendrillidae, are monophyletic and Dictyoceratida is divided into two lineages, one predominantly composed of Dysideidae and the second containing the remaining families (Irciniidae, Spongiidae, Thorectidae, and Verticillitidae). Within Myxospongiae, we find Chondrosida to be paraphyletic with respect to the Verongida. We amend the latter to include species of the genus Chondrosia and erect a new order Chondrillida to contain remaining taxa from Chondrosida, which we now discard. Even with increased taxon sampling of Haploscleromorpha, our analyses are consistent with previous studies; however, Haliclona species are interspersed in even more clades. Haploscleromorpha contains five highly supported clades, each more diverse than previously recognized, and current families are mostly polyphyletic. In addition, we reassign Janulum spinispiculum to Haploscleromorpha and resurrect Reniera filholi as Janulum filholi comb. nov. Within the large clade Heteroscleromorpha, we confirmed 12 recently identified clades based on alternative data, as well as a sister-group relationship between the freshwater Spongillida and the family Vetulinidae. We transfer Stylissa flabelliformis to the genus Scopalina within the family Scopalinidae, which is of uncertain position. Our analyses uncover a large, strongly supported clade containing all heteroscleromorphs other than Spongillida, Vetulinidae, and Scopalinidae. Within this clade, there is a major division separating Axinellidae, Biemnida, Tetractinellida, Bubaridae, Stelligeridae, Raspailiidae, and some species of Petromica, Topsentia, and Axinyssa from Agelasida, Polymastiidae, Placospongiidae, Clionaidae, Spirastrellidae, Tethyidae, Poecilosclerida, Halichondriidae, Suberitidae, and Trachycladus. Among numerous results: (1) Spirophorina and its family Tetillidae are paraphyletic with respect to a strongly supported Astrophorina within Tetractinellida; (2) Agelasida is the earliest diverging lineage within the second clade listed above; and (3) Merlia and Desmacella appear to be the earliest diverging lineages of Poecilosclerida.

Siliceous spicules in demosponges exist in a variety of shapes, some of which look like minute spheres of glass. They are called “sterrasters” when they belong to the Geodiidae family (Tetractinellida order) and “selenasters” when they belong to the Placospongiidae family (Clionaida order). Today, the Geodiidae represent a highly diverse sponge family with more than 340 species, occurring in shallow to deep waters worldwide, except for the Antarctic. The molecular phylogeny of Geodiidae is currently difficult to interpret because we are lacking morphological characters to support most of its clades. To fill this knowledge gap, the surface microornamentations of sterrasters were compared in different genera. Observations with scanning electron microscopy revealed four types of surfaces, which remarkably matched some of the Geodiidae genera: type I characteristic of Geodia , type II characteristic of Pachymatisma, Caminus , and some Erylus ; type III characteristic of other Erylus ; type IV characteristic of Caminella . Two subtypes were identified in Geodia species: warty vs. smooth rosettes. These different microornamentations were mapped on new Geodiidae COI (Folmer fragment) and 28S (C1–D2) phylogenetic trees. The monophyly of the Geodiidae was once again challenged, thereby suggesting that sterrasters have evolved independently at least three times: in the Geodiinae, in the Erylinae and in Caminella . Surface microornamentations were used to review the fossil record of sterrasters and selenasters through the paleontology literature and examination of fossils. It was concluded that “rhaxes” in the literature may represent mixes of sterrasters and selenasters: while Rhaxella spicules may belong to the Placospongiidae, Rhaxelloides spicules belong to the Geodiidae. The putative Geodiidae fossil genera, Geoditesia , and Geodiopsis , are reallocated to Tetractinellida incertae sedis . Isolated Miocene-Pliocene fossil sterrasters Hataina ( Huang, 1967 ), Silicosphaera ( Hughes, 1985 ) and Conciliaspongia ( Robinson and Haslett, 1995 ) become junior synonyms of Geodia ( Lamarck, 1815 ). Overall, the fossil record suggested that Geodiidae was present at least since the Middle Jurassic (163–166 Mya), while Geodia sterrasters were present since the Santonian/Campanian boundary, Late Cretaceous (83.6 Mya).

Recent phylogenetic analyses of demosponges have suggested that the order Poecilosclerida is monophyletic and nested within the paraphyletic ‘order’ Hadromerida. Until now, this result has rested upon very limited taxon sampling of SSU sequences and partial LSU sequences. We collected and analysed additional full-length SSU and LSU sequences to test the validity and position of the poecilosclerid/hadromerid clade within demosponges, and we sampled a short segment of the LSU from diverse hadromerids to explore the internal relationships of Hadromerida. Our data strongly support the existence of a hadromerid/poecilosclerid clade that is sister to a poorly characterized group of halichondrid and agelasid species (‘Clade C’). We find support for the monophyly of the hadromerid families Polymastiidae, Placospongiidae and Timeidae, and conditional support for the family Suberitidae. Furthermore, both LSU and SSU data support a clade that includes a mixture of species assigned to the families Tethyidae and Hemiasterellidae (TETH/HEM) and a mixed clade including members of the families Clionaidae and Spirastrellidae (CLIO/SPIR). The family Placospongiidae is reconstructed as sister to the clade CLIO/SPIR and the family Timeidae is supported as sister to the clade TETH/HEM. The order Poecilosclerida is most closely allied with the Placospongiidae/CLIO/SPIR clade.