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Orthonectids Are Highly Degenerate Annelid Worms

2018; Elsevier BV; Volume: 28; Issue: 12 Linguagem: Inglês

10.1016/j.cub.2018.04.088

1879-0445

Philipp H. Schiffer, Helen E. Robertson, Maximilian J. Telford,

Marine Ecology and Invasive Species

The animal groups of Orthonectida and Dicyemida are tiny, extremely simple, vermiform endoparasites of various marine animals and have been linked in the Mesozoa (Figure 1). The Orthonectida (Figures 1A and 1B) have a few hundred cells, including a nervous system of just ten cells [2Slyusarev G.S. Starunov V.V. The structure of the muscular and nervous systems of the female Intoshia linei (Orthonectida).Org. Divers. Evol. 2015; 16: 65-71Crossref Scopus (16) Google Scholar], and the Dicyemida (Figure 1C) are even simpler, with ∼40 cells [3Furuya H. Hochberg F.G. Tsuneki K. Cell number and cellular composition in infusoriform larvae of dicyemid mesozoans (Phylum Dicyemida).Zoolog. Sci. 2004; 21: 877-889Crossref PubMed Scopus (30) Google Scholar]. They are classic "Problematica" [4Nielsen C. Animal Evolution. Oxford University Press, 2011Crossref Google Scholar]—the name Mesozoa suggests an evolutionary position intermediate between Protozoa and Metazoa (animals) [5Dodson E.O. A note on the systematic position of the Mesozoa.Syst. Zool. 1956; 5: 37-40Crossref Google Scholar] and implies that their simplicity is a primitive state, but molecular data have shown they are members of Lophotrochozoa within Bilateria [6Suzuki T.G. Ogino K. Tsuneki K. Furuya H. Phylogenetic analysis of dicyemid mesozoans (phylum Dicyemida) from innexin amino acid sequences: dicyemids are not related to Platyhelminthes.J. Parasitol. 2010; 96: 614-625Crossref PubMed Scopus (22) Google Scholar, 7Hanelt B. Van Schyndel D. Adema C.M. Lewis L.A. Loker E.S. The phylogenetic position of Rhopalura ophiocomae (Orthonectida) based on 18S ribosomal DNA sequence analysis.Mol. Biol. Evol. 1996; 13: 1187-1191Crossref PubMed Scopus (63) Google Scholar, 8Lu T.-M. Kanda M. Satoh N. Furuya H. The phylogenetic position of dicyemid mesozoans offers insights into spiralian evolution.Zoological Lett. 2017; 3https://doi.org/10.1186/s40851-017-0068-5Crossref PubMed Scopus (22) Google Scholar, 9Mikhailov K.V. Slyusarev G.S. Nikitin M.A. Logacheva M.D. Penin A.A. Aleoshin V.V. Panchin Y.V. The genome of Intoshia linei affirms orthonectids as highly simplified spiralians.Curr. Biol. 2016; 26: 1768-1774Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar], which means that they derive from a more complex ancestor. Their precise affinities remain uncertain, however, and it is disputed whether they even constitute a clade. Ascertaining their affinities is complicated by the very fast evolution observed in their genes, potentially leading to the common systematic error of long-branch attraction (LBA) [10Philippe H. Brinkmann H. Copley R.R. Moroz L.L. Nakano H. Poustka A.J. Wallberg A. Peterson K.J. Telford M.J. Acoelomorph flatworms are deuterostomes related to Xenoturbella.Nature. 2011; 470: 255-258Crossref PubMed Scopus (319) Google Scholar]. Here, we use mitochondrial and nuclear gene sequence data and show that both dicyemids and orthonectids are members of the Lophotrochozoa. Carefully addressing the effects of unequal rates of evolution, we show that the Mesozoa is polyphyletic. While the precise position of dicyemids remains unresolved within Lophotrochozoa, we identify orthonectids as members of the phylum Annelida. This result reveals one of the most extreme cases of body-plan simplification in the animal kingdom; our finding makes sense of an annelid-like cuticle in orthonectids [2Slyusarev G.S. Starunov V.V. The structure of the muscular and nervous systems of the female Intoshia linei (Orthonectida).Org. Divers. Evol. 2015; 16: 65-71Crossref Scopus (16) Google Scholar] and suggests that the circular muscle cells repeated along their body [11Slyusarev G.S. Fine structure and development of the cuticle of Intoshia variabili (Orthonectida).Acta Zool. 2000; 81: 1-8Crossref Scopus (8) Google Scholar] may be segmental in origin.