Multigene Analyses of Bilaterian Animals Corroborate the Monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia

Abstract

Almost a decade ago, a new phylogeny of bilaterian animals was inferred from small-subunit ribosomal RNA (rRNA) that claimed the monophyly of two major groups of protostome animals: Ecdysozoa (e.g., arthropods, nematodes, onychophorans, and tardigrades) and Lophotrochozoa (e.g., annelids, molluscs, platyhelminths, brachiopods, and rotifers). However, it received little additional support. In fact, several multigene analyses strongly argued against this new phylogeny. These latter studies were based on a large amount of sequence data and therefore showed an apparently strong statistical support. Yet, they covered only a few taxa (those for which complete genomes were available), making systematic artifacts of tree reconstruction more probable. Here we expand this sparse taxonomic sampling and analyze a large data set (146 genes, 35,371 positions) from a diverse sample of animals (35 species). Our study demonstrates that the incongruences observed between rRNA and multigene analyses were indeed due to long-branch attraction artifacts, illustrating the enormous impact of systematic biases on phylogenomic studies. A refined analysis of our data set excluding the most biased genes provides strong support in favor of the new animal phylogeny and in addition suggests that urochordates are more closely related to vertebrates than are cephalochordates. These findings have important implications for the interpretation of morphological and genomic data.

Additional molecular support for the new chordate phylogeny

“…Some hints of this unexpected result had been observed in previous large-scale phylogenetic studies including a single tunicate representative (Blair and Hedges, 2005;Philippe et al, 2005b;Vienne and Pontarotti, 2006). However, a substantial increase in taxon sampling turned out to be required for recovering convincing support in favor of such an unorthodox relationship.…”

“…Despite some troubled beginnings due to the shortcomings of using only a restricted set of taxa (Philippe et al, 2005a), phylogenomics has provided strong corroborating support for the new animal phylogeny, essentially confirming the monophyly of Protostomia, Ecdysozoa, and Lophotrochozoa (Baurain et al, 2007;Dunn et al, 2008;Lartillot and Philippe, 2008;Philippe et al, 2005b). Phylogenomics has also helped solving some longstanding mysteries such as the position of chaetognaths, which finally appear to belong to Protostomia (Marletaz et al, 2006;Matus et al, 2006) and also proposed unexpected phylogenetic affinities for enigmatic taxa such as Buddenbrockia plumatellae recently unmasked as a cnidarian worm (Jimenez-Guri et al, 2007), or Xenoturbella bocki, representing a fourth deuterostome phylum on its own (Bourlat et al, 2006).…”

Phylogenomic analyses reveal subclass Scuticociliatia as the sister group of subclass Hymenostomatia within class Oligohymenophorea

“…Therefore, in order to resolve these relationships more clearly, an analysis based on genomic data was carried out. Phylogenomic analyses that used omics data have generally improved the robustness of molecular phylogenetic reconstructions and untangled many previously debated phylogenies among major eukaryotic lineages (Chiari et al, 2012;Hampl et al, 2009;Liang et al, 2013;Philippe et al, 2009;Philippe et al, 2005;Philippe and Telford, 2006;Ryan et al, 2013;Struck and Fisse, 2008). With respect to the phylum Ciliophora, the first phylogenomic analysis was carried out to explore the phylogenetic position of the ambiguous taxon Protocruzia (Gentekaki et al, 2014).…”

Phylogeny of the families Pyuridae and Styelidae (Stolidobranchiata, Ascidiacea) inferred from mitochondrial and nuclear DNA sequences

“…New phylogenomic approaches have recently overturned conventional thinking about the relationships within chordates (Philippe et al, 2005;Bourlat et al, 2006;Delsuc et al, 2006;Dunn et al, 2008;Blair and Hedges, 2005). One of the most recent molecular phylogenies has suggested that the Subphylum Urochordata (Tunicata), represented by three different classes, Ascidiacea, Thaliacea and Larvacea, should be raised to the phylum level (Zeng and Swalla, 2005) but the subject is still under discussion since there are discrepancies between phylogenomic analyses and results from mitochondrial and rRNA data.…”