Integrative taxonomy of <em>Tethya</em>: description of four new species based on morphology, phylogeny and microbiome diversity

The genus Tethya, one of the most iconic groups in the phylum Porifera. includes nearly 100 valid species. Tethya shows a nearly cosmopolitan distribution, and thus this clade could help elucidate global mechanisms of speciation in sponges. Contrasting with many other marine organisms, Tethya peaks in diversity in the temperate region, with only ∼30% of diversity occurring in the tropics. This pattern may however be related to a lack of studies in the tropics, masked by dubious taxonomic identifications. To address this question, we studied new collections from the Western Atlantic (Caribbean and Brazil) and the Northeastern Atlantic, as well as museum material from the Indian Ocean. Combining morphological investigation with molecular phylogenetics and the study of the sponge’s microbial communities, we conclude that four constitute new species that we describe here: Tethya martini Riesgo, Giribet, & Santodomingo, sp. nov.; Tethya simoni Santodomingo, Zea, & Riesgo, sp. nov.; Tethya erici Díez-Vives, Santodomingo, Moles, & Riesgo, sp. nov.; Tethya orioni Kenny, Santodomingo & Riesgo, sp. nov. Some species thought to be widespread (e.g., T. aurantium and T. seychellensis), each represent multiple species with unique geographic distributions. A phylogenetic analysis of Tethya (based on COI and 28S rRNA sequence data) recovered five main clades, which were also characterized by distinct prokaryotic communities. This suggests that microbiomes could be used as a guide for taxonomic identification in Tethya. We finally explored the existence of a phylosymbiotic pattern in sponges at different levels of prokaryotic taxonomic resolution (i.e., at phylum, class, and genus-level analysis of prokaryotes). Remarkably, our analysis revealed high levels of coevolution of Tethya and their associated microbial communities, even when microbiomes were analysed at the genus level. Our findings support the use of an integrative approach to better understand the evolutionary history of sponges.