The systematics of carnivorous sponges

Abstract

Carnivorous sponges are characterized by their unique method of capturing mesoplanktonic prey coupled with the complete or partial reduction of the aquiferous system characteristic of the phylum Porifera. Current systematics place the vast majority of carnivorous sponges within Cladorhizidae, with certain species assigned to Guitarridae and Esperiopsidae. Morphological characters have not been able to show whether this classification is evolutionary accurate, and whether carnivory has evolved once or in several lineages. In the present paper we present the first comprehensive molecular phylogeny of the carnivorous sponges, interpret these results in conjunction with morphological characters, and propose a revised classification of the group. Molecular phylogenies were inferred using 18S rDNA and a combined dataset of partial 28S rDNA, COI and ALG11 sequences. The results recovered carnivorous sponges as a clade closely related to the families Mycalidae and Guitarridae, showing family Cladorhizidae to be monophyletic and also including carnivorous species currently placed in other families. The genus Lycopodina is resurrected for species currently placed in the paraphyletic subgenus Asbestopluma (Asbestopluma) featuring forceps spicules and lacking sigmas or sigmancistras. The genera Chondrocladia and Cladorhiza are found to be monophyletic. However, results indicate that the subgenus Chondrocladia is polyphyletic with respect to the subgenera Meliiderma and Symmetrocladia. Euchelipluma, formerly Guitarridae, is retained, but transferred to Cladorhizidae. The four known carnivorous species currently in Esperiopsis are transferred to Abyssocladia. Neocladia is a junior homonym and is here renamed Koltunicladia. Our results provide strong evidence in support of the hypothesis that carnivory in sponges has evolved only once. While spicule characters mostly reflect monophyletic groups at the generic level, differences between genera represent evolution within family Cladorhizidae rather than evolution of carnivory in separate lineages. Conflicting spicule characters can be reinterpreted to support the inclusion of all carnivorous sponges within Cladorhizidae, and a carnivorous habit should thus be considered the main diagnostic character in systematic classification.

Microbiomes of the Arctic carnivorous sponges Chondrocladia grandis and Cladorhiza oxeata suggest a specific, but differential involvement of bacterial associates

“…Taxonomy of the collected carnivorous sponges was established by sequencing the host 18S rRNA gene, 28S rRNA gene C1-D2 partition, the overlapping "Folmer" and "Erpenbeck" mitochondrial COI gene fragments, and part of the asparaginelinked glycosylation 11 homolog (ALG11) gene, amplified using primers described in Hestetun et al (2016b). PCR products were obtained using Dream Taq polymerase (Thermo Fisher Scientific, Waltham, Massachusetts, USA), purified using Agencourt AMPure XP Phylogenetic analysis was performed as described by Verhoeven et al (2017).…”

“…However, our current understanding of the global biogeography of the Cladorhizidae is still rudimentary, although a bipolar cold-water distribution pattern has been suggested, and a high number of species have been reported within northeast Atlantic and Arctic regions (Hestetun et al 2015). Cladorhizids are commonly encountered at shallow to mid-bathyal depths at high latitudes (Hestetun et al 2016b) and may be dominant members of certain benthic communities. For example, Chondrocladia was a defining taxon for one of 10 biotopes identified in the Norwegian MAREANO seabed mapping program; this biotope was associated with mixed sediments along canyons and steep slopes at a mean depth of 1390 m (Buhl-Mortensen et al 2015).…”

The cladorhizid fauna (Porifera, Poecilosclerida) of the Caribbean and adjacent waters

“…Sigmancistras and basal acanthotylostyles are also present with a few exceptions. Never forceps spicules (modified from Hestetun et al, 2016b). Type species.…”

Three new species of Cladorhiza (Demospongiae, Poecilosclerida, Cladorhizidae) from the Northeast Pacific Ocean

“…There are currently 161 species of Cladorhizidae recognized from 9 genera (Van Soest et al 2017). Using molecular techniques and morphological characters, Hestetun et al revised the phylogeny of the Cladorhizidae, reassigning several carnivorous taxa from other families in the Poecilosclerida to genera within the Cladorhizidae, demonstrating 1) that carnivory has evolved in one familial lineage within the Poecilosclerida and 2) monophyly for the family Cladorhizidae (Hestetun et al 2016). Trochirhabd spicules from two recently described species of Chondrocladia closely match fossil spicules described from early Jurassic sedimentary deposits, suggesting that the Cladorhizidae may have been present 200-250 mya (Vacelet and Kelly 2008).…”

“…Cladorhiza is a monophyletic genus within the Cladorhizidae with 41 described species, defined by the presence of trident anchorate anisochelae (Hestetun et al 2016). Cladorhiza species are known to have arborescent, pinnate, flagelliform, crinorhiza (parasol), and stipitate morphologies (Boury-Esnault & Rutzler 1997).…”