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

Hervé Philippe,Nicolas Lartillot,Henner Brinkmann

doi:10.1093/molbev/msi111

Hervé Philippe, Nicolas Lartillot + Show 1 more

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https://doi.org/10.1093/molbev/msi111

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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.

Highlights

The traditional view of bilaterian animal evolution based on morphological and embryological characters proposed that the phylogeny correlates with a gradual increase in complexity (Adoutte et al 2000)
The most simple organisms emerged first, i.e., acoelomates followed by the pseudocoelomates and by the true coelomates. This view was challenged by a careful analysis of small-subunit ribosomal RNA sequences, sampled from a selected set of animals with slowly evolving rRNAs (Aguinaldo et al 1997). In this so-called new animal phylogeny, some pseudocoelomates, in particular nematodes, were grouped with some coelomates in the clade Ecdysozoa, whereas other pseudocoelomates and acoelomates were grouped with the remaining protostomian coelomates in the clade Lophotrochozoa
Often taken for granted (Adoutte et al 2000; Graham 2000; Giribet 2002), the new animal phylogeny has only been confirmed by the analyses of Hox genes, horse radish peroxidase (HRP) antibody staining (Haase et al 2001), large-subunit rRNA (Mallatt and Winchell 2002), and Na/K adenosine triphosphatase (ATPase) (Anderson, Cordoba, and Thollesson 2004)

Summary

Introduction

The traditional view of bilaterian animal evolution based on morphological and embryological characters proposed that the phylogeny correlates with a gradual increase in complexity (Adoutte et al 2000). The most simple organisms emerged first, i.e., acoelomates (e.g., platyhelminths) followed by the pseudocoelomates (e.g., nematodes) and by the true coelomates (e.g., arthropods and chordates) This view was challenged by a careful analysis of small-subunit ribosomal RNA (rRNA) sequences, sampled from a selected set of animals with slowly evolving rRNAs (Aguinaldo et al 1997). In this so-called new animal phylogeny, some pseudocoelomates, in particular nematodes, were grouped with some coelomates (e.g., arthropods and tardigrades) in the clade Ecdysozoa, whereas other pseudocoelomates (e.g., rotifers) and acoelomates were grouped with the remaining protostomian coelomates (e.g., annelids and molluscs) in the clade Lophotrochozoa. Dopazo 2004; Hugues and Friedman 2004; Wolf, Rogozin, and Koonin 2004) pro-

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