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Exploring marine sponges from shallow tropical reefs of the Caribbean and western Central Pacific, as part of large biodiversity (Moorea Biocode Project) and evolutionary (Porifera Tree of Life) research projects, we encountered 13 skeleton-less specimens, initially divided in two morphological groups, which had patterns of coloration and oxidation typical of taxa of the order Verongida (Demospongiae). The first group of samples inhabited open and cryptic habitats of shallow (15–20 m) Caribbean reefs at Bocas del Toro Archipelago, Panama. The second group inhabited schiophilous (e.g., inner coral framework and crevices) habitats on shallow reefs (0.5–20 m deep) in Moorea Island, French Polynesia. We applied an integrative approach by combining analyses of external morphology, histological observations, 18S rDNA, and mtCOI to determine the identity and the relationships of these unknown taxa within the order Verongida. Molecular analyses revealed that none of the species studied belonged to Hexadella (Ianthellidae, Verongida), the only fibreless genus of the Order Verongida currently recognized. The species from the Caribbean locality of Bocas del Toro (Panama) belong to the family Ianthellidae and is closely related to the Pacific genera Ianthella and Anomoianthella, both with well-developed fiber reticulations. We suggest the erection of a new generic denomination to include this novel eurypylous, fibreless ianthellid. The species collected in Moorea were all diplodal verongid taxa, with high affinities to a clade containing Pseudoceratina, Verongula, and Aiolochroia, a Pacific and two Caribbean genera, respectively. These unknown species represented at least three different taxa distinguished by DNA sequence analysis and morphological characteristics. Two new genera and a new species of Pseudoceratina are here proposed to accommodate these novel biological discoveries. The evolutionary and ecological meaning of having or lacking a fiber skeleton within Verongida is challenged under the evidence of the existence of fibreless genera within various verongid clades. Furthermore, the discovery of a fibreless Peudoceratina suggests that the possession of a spongin-chitin fiber reticulation is an “ecological” plastic trait that might be lost under certain conditions, such us growing within another organism’s skeletal framework. These results raise new questions about the ecological and evolutionary significance of the development of a fiber skeleton and of sponges’ adaptability to various environmental conditions. [ABSTRACT FROM PUBLISHER]