The nematode-arthropod clade revisited: phylogenomic analyses from ribosomal protein genes misled by shared...

Phylogenetic analysis of major groups of Metazoa using genomic data tends to recover the sister relationships of arthropods and chordates, contradicting the proposed Ecdysozoa (the molting animals), which group the arthropods together with nematodes and relatives. Ribosomal protein genes have been a major data source in phylogenomic studies because they are readily detected as Expressed Sequence Tags (ESTs) due to their high transcription rates. Here we address the debate about the recovery of Ecdysozoa in genomic data by building a new matrix of carefully curated EST and genome sequences for 25 ribosomal protein genes of the small subunit, with focus on new insect sequences in addition to the Diptera sequences generally used to represent the arthropods. Individually, each ribosomal protein gene showed low phylogenetic signal, but in simultaneous analysis strong support emerged for many expected groups, with support increasing linearly with increased gene number. In agreement with most studies of metazoan relationships from genomic data, our analyses contradicted the Ecdysozoa (the putative sister relationship of arthropods and nematodes), and instead supported the affinity of arthropods with chordates. In addition, relationships among holometabolan insects resulted in an unlikely basal position for Diptera. To test for biases in the data that might produce an erroneous arthropod-chordate affinity we simulated sequence data on tree topologies with the alternative arthropod-nematode sister relationships, applying a model of amino acid sequence evolution estimated from the real data. Tree searches on these simulated data still revealed an arthropod-chordate grouping, i.e., the topologies used to simulate the data were not recovered correctly. This suggests that the arthropod-chordate relationships may be obtained erroneously also from the real data even if the alternative topology (Ecdysozoa) represents the true phylogeny. Whereas denser taxon sampling in the future may recover the Ecdysozoa, our analyses demonstrate that recent phylogenomic studies may be affected by as yet unspecified biases in amino acid sequence composition in the model organisms with available genomic data.