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Spiralian Phylogeny Informs the Evolution of Microscopic Lineages

2015; Elsevier BV; Volume: 25; Issue: 15 Linguagem: Inglês

10.1016/j.cub.2015.06.068

1879-0445

Christopher Laumer, Nicolas Bekkouche, Alexandra Kerbl, Freya Goetz, Ricardo Cardoso Neves, Martin V. Sørensen, Reinhardt M. Kristensen, Andreas Hejnol, Casey W. Dunn, Gonzalo Giribet, Katrine Worsaae,

Marine Sponges and Natural Products

Despite rapid advances in the study of metazoan evolutionary history [1Dunn C.W. Giribet G. Edgecombe G.D. Hejnol A. Animal phylogeny and its evolutionary implications.Annu. Rev. Ecol. Evol. Syst. 2014; 45: 371-395Crossref Scopus (236) Google Scholar], phylogenomic analyses have so far neglected a number of microscopic lineages that possess a unique combination of characters and are thus informative for our understanding of morphological evolution. Chief among these lineages are the recently described animal groups Micrognathozoa and Loricifera, as well as the two interstitial “Problematica” Diurodrilus and Lobatocerebrum [2Haszprunar G. Rieger R.M. Schuchert P. Extant “Problematica” within or near the Metazoa.in: Simonetta A.M. Conway Morris S. The Early evolution of Metazoa and the Significance of Problematic Taxa. Oxford University Press, Cambridge1991: 99-105Google Scholar]. These genera show a certain resemblance to Annelida in their cuticle and gut [3Rieger R.M. A new group of interstitial worms, Lobatocerebridae nov. fam. (Annelida) and its significance for metazoan phylogeny.Zoomorphologie. 1980; 95: 41-84Crossref Scopus (63) Google Scholar, 4Kristensen R.M. Niilonen T. Structural studies on Diurodrilus Remane (Diurodrilidae fam.n.), with description of Diurodrilus westheidei sp.n. from the Arctic interstitial meiobenthos, W. Greenland.Zool. Scr. 1982; 11: 1-12Crossref Scopus (39) Google Scholar]; however, both lack primary annelid characters such as segmentation and chaetae [5Worsaae K. Rouse G.W. Is Diurodrilus an annelid?.J. Morphol. 2008; 269: 1426-1455Crossref PubMed Scopus (46) Google Scholar]. Moreover, they show unique features such as an inverted body-wall musculature or a novel pharyngeal organ. This and their ciliated epidermis have led some to propose relationships with other microscopic spiralians, namely Platyhelminthes, Gastrotricha, and in the case of Diurodrilus, with Micrognathozoa [6Kristensen R.M. Funch P. Micrognathozoa: a new class with complicated jaws like those of Rotifera and Gnathostomulida.J. Morphol. 2000; 246: 1-49Crossref PubMed Google Scholar, 7Bekkouche N. Kristensen R.M. Hejnol A. Sørensen M.V. Worsaae K. Detailed reconstruction of the musculature in Limnognathia maerski (Micrognathozoa) and comparison with other Gnathifera.Front. Zool. 2014; 11: 71Crossref PubMed Scopus (17) Google Scholar]—lineages that are grouped by some analyses into “Platyzoa,” a clade whose status remains uncertain [1Dunn C.W. Giribet G. Edgecombe G.D. Hejnol A. Animal phylogeny and its evolutionary implications.Annu. Rev. Ecol. Evol. Syst. 2014; 45: 371-395Crossref Scopus (236) Google Scholar, 8Cavalier-Smith T. A revised six-kingdom system of life.Biol. Rev. Camb. Philos. Soc. 1998; 73: 203-266Crossref PubMed Scopus (684) Google Scholar, 9Giribet G. Distel D.L. Polz M. Sterrer W. Wheeler W.C. Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology.Syst. Biol. 2000; 49: 539-562Crossref PubMed Scopus (332) Google Scholar, 10Hejnol A. Obst M. Stamatakis A. Ott M. Rouse G.W. Edgecombe G.D. Martinez P. Baguñà J. Bailly X. Jondelius U. et al.Assessing the root of bilaterian animals with scalable phylogenomic methods.Proc. R. Soc. B Biol. Sci. 2009; 276: 4261-4270Crossref PubMed Scopus (583) Google Scholar, 11Struck T.H. Wey-Fabrizius A.R. Golombek A. Hering L. Weigert A. Bleidorn C. Klebow S. Iakovenko N. Hausdorf B. Petersen M. et al.Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of spiralia.Mol. Biol. Evol. 2014; 31: 1833-1849Crossref PubMed Scopus (117) Google Scholar]. Here, we assess the interrelationships among the meiofaunal and macrofaunal members of Spiralia using 402 orthologs mined from genome and transcriptome assemblies of 90 taxa. Lobatocerebrum and Diurodrilus are found to be deeply nested members of Annelida, and unequivocal support is found for Micrognathozoa as the sister group of Rotifera. Analyses using site-heterogeneous substitution models further recover a lophophorate clade and position Loricifera + Priapulida as sister group to the remaining Ecdysozoa. Finally, with several meiofaunal lineages branching off early in the diversification of Spiralia, the emerging concept of a microscopic, acoelomate, direct-developing ancestor of Spiralia is reviewed.