Integrative taxonomy of Tethya: description of four new species based on morphology, phylogeny and microbiomes

The genus Tethya is one of the most iconic groups in the phylum Porifera. With nearly 100 valid species and a cosmopolitan distribution, they can help elucidate mechanisms of speciation in sponges. Recent studies have uncovered high levels of endemism, in particular in temperate waters (>60% at the species level) that contrast with the tropics (~30%). This biogeographic disparity is related to a lack of studies so that the true diversity of Tethya in the tropics remains masked by dubious taxonomic identifications. To answer this question, we studied new collections from the Western Atlantic (Caribbean and Brazil) and the North East Atlantic, as well as museum material from the Indian Ocean. Our integrative approach includes detailed morphological descriptions, molecular phylogenetics, and the study of their associated microbial communities. We found that some species thought to be widespread (e.g. Tethya aurantium and Tethya seychellensis) each represent multiple species with distinct geographic distributions. Thus, we describe four new species: two new species from the Caribbean/Brasil, one from the North East Atlantic and one from the Persian Gulf. The Tethya phylogenetic tree (based on COI and 28S rRNA) recovered four main clades. Even though Tethya are low microbial abundance (LMA) sponges, distinctive prokaryotic communities characterized each of the clades, suggesting that microbiomes could be considered an additional taxonomic feature. For the first time, we explored the presence of a phylosymbiotic pattern at different levels of resolution (i.e. at phylum, class and genus-level analysis of prokaryotes) on a wide array of species from the same sponge genus. Remarkably, our analysis revealed high levels of coevolution of the Tethya host species and their associated microbial communities, even at genus-level. Our findings highlight the importance of using an integrative approach to better understand the diversity and evolutionary history of Tethya.