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Insights into evolution of freshwater sponges: molecular life of stygobitic sponge Eunapius subterraneus

The sponges, as the most basal group in the animal phylogeny, laid the foundation for all animal life to follow. These simple animals with a plain morphology have an essential role in studying genome evolution of Metazoa. Sponges are predominantly marine, with the notable exception of the family Spongillidae, an extant group of freshwater demosponges whose fossil record begins in the Cretaceous. Cave fauna stands out among all other freshwater biota owning peculiar species which are usually distinct from that of surrounding freshwater habitats. Eunapius subterraneus inhabits caves in the Ogulin karst area (Croatia) and is the only known stygobitic representative of the phylum Porifera in the world. In order to elucidate the problematic taxonomic position of Eunapius subterraneus, three genetic markers (18S rDNA, ITS2 and COI) with different evolutionary rates were used in phylogenetic analyses. All genetic markers undoubtedly exclude this sponge from the genus Eunapius. E. subterraneus shows much higher sequence similarity with other freshwater sponge genera, thus raising the question of true taxonomical designation of Eunapius subterraneus. To further assess phylogenetical position of Eunapius subterraneus the complete mitochondrial DNA (mtDNA) sequence was analyzed and compared with mt genomes of other related sponge species. Analysis on primary and secondary structure supported with phylogenetic analysis showed remarkable similarity of mtDNA genomes of Eunapius subterraneus and Ephydatia muelleri. The presence of numerous small open reading frames in intergenic regions implies that some of them may have been transmitted horizontally from a bacterial or fungus donor. Our results strongly support the placement of E. subterraneus outside the Eunapius genus and they clearly show a high level of disagreement between current freshwater sponge classification based on morphology and molecular data. Furthermore, hypothesis that endemic sponge species might have originated from a cosmopolitan founder species such as Ephydatia. (Meixner et al.2007) was acknowledged. The question remains whether this phenomenon is common to other endemic sponges.

Porifera; Spongillidae; stygobitic; mitochondrial evolution

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