Glass Sponges and Bilaterian Animals Share Derived Mitochondrial Genomic Features: A Common Ancestry or Parallel Evolution?

Glass sponges (Hexactinellida) are a group of deep-water benthic animals that have a unique syncytial organization and possess a characteristic siliceous skeleton. Although hexactinellids are traditionally grouped with calcareous and demosponges in the phylum Porifera, the monophyly of sponges and the phylogenetic position of the Hexactinellida remain contentious. We determined and analyzed the nearly complete mitochondrial genome sequences of the hexactinellid sponges Iphiteon panicea and Sympagella nux. Unexpectedly, our analysis revealed several mitochondrial genomic features shared between glass sponges and bilaterian animals, including an Arg --> Ser change in the genetic code, a characteristic secondary structure of one of the serine tRNAs, highly derived tRNA and rRNA genes, and the presence of a single large noncoding region. At the same time, glass sponge mtDNA contains atp9, a gene previously found only in the mtDNA of demosponges (among animals), and encodes a tRNA(Pro);(UGG) with an atypical A11-U24 pair that is also found in demosponges and placozoans. Most of our sequence-based phylogenetic analyses place Hexactinellida as the sister group to the Bilateria; however, these results are suspect given accelerated rates of mitochondrial sequence evolution in these groups. Thus, it remains an open question whether shared mitochondrial genomic features in glass sponges and bilaterian animals reflect their close phylogenetic affinity or provide a remarkable example of parallel evolution.