Near intron pairs and the metazoan tree

Abstract

Gene structure data can substantially advance our understanding of metazoan evolution and deliver an independent approach to resolve conflicts among existing hypotheses. Here, we used changes of spliceosomal intron positions as novel phylogenetic marker to reconstruct the animal tree. This kind of data is inferred from orthologous genes containing mutually exclusive introns at pairs of sequence positions in close proximity, so-called near intron pairs (NIPs). NIP data were collected for 48 species and utilized as binary genome-level characters in maximum parsimony (MP) analyses to reconstruct deep metazoan phylogeny. All groupings that were obtained with more than 80% bootstrap support are consistent with currently supported phylogenetic hypotheses. This includes monophyletic Chordata, Vertebrata, Nematoda, Platyhelminthes and Trochozoa. Several other clades such as Deuterostomia, Protostomia, Arthropoda, Ecdysozoa, Spiralia, and Eumetazoa, however, failed to be recovered due to a few problematic taxa such as the mite Ixodesand the warty comb jelly Mnemiopsis. The corresponding unexpected branchings can be explained by the paucity of synapomorphic changes of intron positions shared between some genomes, by the sensitivity of MP analyses to long-branch attraction (LBA), and by the very unequal evolutionary rates of intron loss and intron gain during evolution of the different subclades of metazoans. In addition, we obtained an assemblage of Cnidaria, Porifera, and Placozoa as sister group of Bilateria+Ctenophora with medium support, a disputable, but remarkable result. We conclude that NIPs can be used as phylogenetic characters also within a broader phylogenetic context, given that they have emerged regularly during evolution irrespective of the large variation of intron density across metazoan genomes.