Improvement of molecular phylogenetic inference and the phylogeny of Bilateria

Abstract

Inferring the relationships among Bilateria has been an active and controversial research area since Haeckel. The lack of a sufficient number of phylogenetically reliable characters was the main limitation of traditional phylogenies based on morphology. With the advent of molecular data, this problem has been replaced by another one, statistical inconsistency, which stems from an erroneous interpretation of convergences induced by multiple changes. The analysis of alignments rich in both genes and species, combined with a probabilistic method (maximum likelihood or Bayesian) using sophisticated models of sequence evolution, should alleviate these two major limitations. We applied this approach to a dataset of 94 genes and 79 species using CAT, a previously developed model accounting for site-specific amino acid replacement patterns. The resulting tree is in good agreement with current knowledge: the monophyly of most major groups (e.g. Chordata, Arthropoda, Lophotrochozoa, Ecdysozoa, Protostomia) was recovered with high support. Two results are surprising and are discussed in an evo-devo framework: the sister-group relationship of Platyhelminthes and Annelida to the exclusion of Mollusca, contradicting the Neotrochozoa hypothesis, and, with a lower statistical support, the paraphyly of Deuterostomia. These results, in particular the status of deuterostomes, need further confirmation, both through increased taxonomic sampling, and future improvements of probabilistic models.

Additional molecular support for the new chordate phylogeny

“…The Bayesian inference under the CAT mixture model suggests deuterostome paraphyly by supporting a basal position of chordates within Bilateria (Fig. 2b) as previously reported (Lartillot and Philippe, 2008). However, ML retrieved the monophyly of deuterostomes, but with BP WAG1F1G8 of only 50%, leaving the monophyly of deuterostomes unresolved by our data.…”

“…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).…”

“…We built upon previous phylogenomic datasets assembled in the Philippe lab Jimenez-Guri et al, 2007;Lartillot and Philippe, 2008;Philippe et al, 2004Philippe et al, , 2005b to select a set of 179 orthologous markers showing sufficient conservation across metazoans to be useful for inferring the phylogeny of metazoans. Alignments were built and updated with available sequences downloaded from the Trace Archive (http://www.ncbi.nlm.nih.gov/Traces/) and the EST Database (http://www.ncbi.nlm.nih.gov/dbEST/) of GenBank at the National Center for Biotechnology Information (http://www.ncbi.nlm.nih.gov/) using the program ED from the MUST package (Philippe, 1993).…”

“…Models accounting for site-specific modulations of the amino-acid replacement process, such as the CAT mixture model (Lartillot and Philippe, 2004), seem to offer a significantly better fit to real data than empirical substitution matrices currently used in standard models of amino-acid sequence evolution. Accounting for sitespecific amino-acid propensities has also been shown to induce a significant improvement of phylogenetic reconstruction in difficult cases such as long-branch attraction (Baurain et al, 2007;Lartillot et al, 2007;Lartillot and Philippe, 2008). This improvement essentially lays in the ability of the CAT model to detect multiple conservative substitutions more efficiently than standard amino-acid models .…”

“…The possible pitfalls associated with phylogenomic studies include systematic errors that can be traced back to some kind of model misspecifications (Philippe et al, 2005a) and caused mainly by heterogeneity of evolutionary rates among taxa Philippe et al, 2005b) and compositional bias (Blanquart and Lartillot, 2008;Jeffroy et al, 2006;Lartillot and Philippe, 2008;Phillips et al, 2004). Empirical protocols have been designed to detect and reduce the impact of systematic error in genome-scale studies (Rodríguez-Ezpeleta et al, 2007) but the ultimate solution lies in the development of improved models of sequence evolution (Felsenstein, 2004;Philippe et al, 2005a;Steel, 2005).…”