Coelomata and Not Ecdysozoa: Evidence From Genome-Wide Phylogenetic Analysis

Abstract

Relative positions of nematodes, arthropods, and chordates in animal phylogeny remain uncertain. The traditional tree topology joins arthropods with chordates in a coelomate clade, whereas nematodes, which lack a coelome, occupy a basal position. However, the current leading hypothesis, based on phylogenetic trees for 18S ribosomal RNA and several proteins, joins nematodes with arthropods in a clade of molting animals, Ecdysozoa. We performed a phylogenetic analysis of over 500 sets of orthologous proteins, which are represented in plants, animals, and fungi, using maximum likelihood, maximum parsimony, and distance methods. Additionally, to increase the statistical power of topology tests, the same methods were applied to concatenated alignments of subunits of eight conserved macromolecular complexes. The majority of the methods, when applied to most of the orthologous clusters, both concatenated and individual, grouped the fly with humans to the exclusion of the nematode, in support of the coelomate phylogeny. Trees were also constructed using information on insertions and deletions in orthologous proteins, combinations of domains in multidomain proteins, and presence-absence of species in clusters of orthologs. All of these approaches supported the coelomate clade and showed concordance between evolution of protein sequences and higher-level evolutionary events, such as domain fusion or gene loss.

Resolution of a deep animal divergence by the pattern of intron conservation

“…These results directly contradict the findings of a very recent very large-scale protein sequence tree-building project, which supported the alternative coelomata hypothesis (13). However, whereas the previous results are complicated by the limitations of protein-sequence-based tree-building methods in cases of sparse taxonomic sampling and interlineage rate differences, our results are consistent and robust to such concerns.…”

“…The alternative ''ecdysozoa'' hypothesis joins arthropods and nematodes with deuterostomes as the outgroup. Morphological (7-10) and molecular (1)(2)(3)(4)(5)(6)(11)(12)(13)(14) analyses have lent support to both sides. Molecular many-taxa studies have tended to support ecdysozoa (2-6), whereas many-gene analyses have tended toward coelomata (11)(12)(13).…”

The evolution of the Ecdysozoa

“…Despite these congruent results, there exists a powerful series of papers arguing against the close relationship of nematodes and arthropods and supporting instead the traditional view of the monophyletic Coelomata linking arthropods such as D. melanogaster to humans rather than to nematode worms (Blair et al 2002;Wolf et al 2004;Philip et al 2005;Ciccarelli et al 2006;Rogozin et al 2007). This specific phylogenetic question has the attraction of being approachable with the largest possible molecular datasets, the completely sequenced genomes of flies, worms and humans.…”

Darwin's dilemma: the realities of the Cambrian ‘explosion’

“…This latter field, however, remains fluid, with many unresolved issues. For example, despite strong evidence for the concepts of Ecdysozoa (Aguindaldo et al 1997) and Lophotrochozoa (Rosa et al 1999), respective voices favouring both the older concept of the Coelomata (Almeida et al 2003;Wolf et al 2004;Philip et al 2005; see also Telford 2004) and the directly related theme concerning the expulsion of the Nematoda from the Ecdysozoa (Blair et al 2002) have been raised. In either case, however, the counter-arguments appear more persuasive (e.g.…”