Embryonic development of verongid demosponges supports the independent acquisition of spongin skeletons as an alternative to the siliceous skeleton of sponges

Approximately 85% of extant sponges (phylum Porifera) belong to the class Demospongiae, which contains 14 taxonomic orders. In the orders Verongida, Dictyoceratida, and Dendroceratida, jointly referred to as 'keratose demosponges', the skeleton does not contain siliceous spicules but only spongin fibres. This shared trait has encouraged placement of these orders together within Demospongiae, although their relationships remain uncertain. The present study documents for the first time embryo development in the order Verongida (Aplysina aerophoba), providing some clues for phylogenetic inference. Spawned eggs were enveloped by a follicle of maternal cells. Embryos and larvae were chimeric organisms, the blastocoel of which was filled with symbionts and maternal cells migrated from the follicle. The ultrastructure of epithelial larval cells revealed: (1) a basal apparatus characterized by a peculiar, angling accessory centriole; (2) a pear-shaped nucleus with a protruding beak connected to the rootlets of the basal body; and (3) a distinctive Golgi apparatus encircling the nuclear apex. Developmental and ultrastructural findings support the concept, in congruence with recent molecular studies, that Verongida are more closely related to Halisarcida (askeletal sponges) and Chondrosida (askeletal sponges + sponges with spongin + spiculate sponges) than to the remaining 'keratose' orders, making a monophyletic 'supra-ordinal unit' equivalent to a subclass (Myxospongia, new subclass). Hence, spongin skeletons have evolved at least twice in Demospongiae. Independent acquisition of 'corneous' materials as an alternative to silica could have been stimulated by the radiation of diatoms at the Cretaceous-Tertiary boundary (approximately 65 Mya), which depleted silicon in the photic zone of the world's ocean. (C) 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 427-447.