A Rigorous Analysis of the Pattern of Intron Conservation Supports the Coelomata Clade of Animals

Many intron positions are conserved in varying subsets of eukaryotic genomes and, consequently, comprise a potentially informative class of phylogenetic characters. Roy and Gilbert developed a method of phylogenetic reconstruction using the patterns of intron presence-absence in eukaryotic genes and, applying this method to the analysis of animal phylogeny, obtained support for an Ecdysozoa clade ([1]). The critical assumption in the method was the independence of the rates of intron loss in different branches of the phylogenetic. Here, this assumption is refuted by showing that the branch-specific intron loss rates are strongly correlated. We show that different tree topologies are obtained, in each case with a significant statistical support, when different subsets of intron positions are analyzed. The analysis of the conserved intron positions supports the Coelomata topology, i.e., a clade comprised of arthropods and chordates, whereas the analysis of more variable intron positions favors the Ecdysozoa topology, i.e., a clade of arthropods and nematodes. We show, however, that the support for Ecdysozoa is fully explained by parallel loss of introns in nematodes and arthropods, a factor that does not contribute to the analysis of the conserved introns. The developed procedure for the identification and analysis of conserved introns and other characters with minimal or no homoplasy is expected to be useful for resolving many hard phylogenetic problems.

[1]  Katharine,et al.  The phylogenetic status of arthropods, as inferred from 18S rRNA sequences. , 1991, Molecular biology and evolution.

[2]  Ernst Haeckel Generelle Morphologie der Organismen , 1866 .

[3]  Peer Bork,et al.  Consistency of genome‐based methods in measuring Metazoan evolution , 2005, FEBS letters.

[4]  N. Grishin,et al.  Genome trees and the tree of life. , 2002, Trends in genetics : TIG.

[5]  B. Snel,et al.  Toward Automatic Reconstruction of a Highly Resolved Tree of Life , 2006, Science.

[6]  D. Penny,et al.  Smoke without fire: most reported cases of intron gain in nematodes instead reflect intron losses. , 2006, Molecular biology and evolution.

[7]  M. Blaxter,et al.  Evolutionary biology: Animal roots and shoots , 2005, Nature.

[8]  N. Lartillot,et al.  The new animal phylogeny: reliability and implications. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[9]  W. Gilbert,et al.  Resolution of a deep animal divergence by the pattern of intron conservation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[10]  P. Holland,et al.  Rare genomic changes as a tool for phylogenetics. , 2000, Trends in ecology & evolution.

[11]  Hervé Philippe,et al.  An empirical assessment of long-branch attraction artefacts in deep eukaryotic phylogenomics. , 2005, Systematic biology.

[12]  Sean B. Carroll,et al.  Hox genes in brachiopods and priapulids and protostome evolution , 1999, Nature.

[13]  N. Grishin,et al.  Genome trees constructed using five different approaches suggest new major bacterial clades , 2001, BMC Evolutionary Biology.

[14]  E. Koonin,et al.  Remarkable Interkingdom Conservation of Intron Positions and Massive, Lineage-Specific Intron Loss and Gain in Eukaryotic Evolution , 2003, Current Biology.

[15]  J. Mallatt,et al.  Testing the new animal phylogeny: first use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. , 2002, Molecular biology and evolution.

[16]  T. Gojobori,et al.  Bmc Evolutionary Biology the Evolutionary Position of Nematodes , 2022 .

[17]  E. Koonin,et al.  Coelomata and not Ecdysozoa: evidence from genome-wide phylogenetic analysis. , 2003, Genome research.

[18]  J. Boore,et al.  The use of genome-level characters for phylogenetic reconstruction. , 2006, Trends in ecology & evolution.

[19]  Patrick Aloy,et al.  Systematic searches for molecular synapomorphies in model metazoan genomes give some support for Ecdysozoa after accounting for the idiosyncrasies of Caenorhabditis elegans , 2004, Evolution & development.

[20]  Ernst Haeckel,et al.  Generelle Morphologie der Organismen: Allgemeine Grundzüge der organischen Formen-Wissenschaft, mechanisch begründet durch die von Charles Darwin reformierte Descendenz-Theorie. Band 1: Allgemeine Anatomie. Band 2: Allgemeine Entwicklungsgeschichte , 1866 .

[21]  E. Koonin,et al.  Conservation versus parallel gains in intron evolution , 2005, Nucleic acids research.

[22]  E. Koonin,et al.  Three distinct modes of intron dynamics in the evolution of eukaryotes. , 2007, Genome research.

[23]  M. Telford Animal Phylogeny: Back to the Coelomata? , 2004, Current Biology.

[24]  Richard R. Copley,et al.  Animal Phylogeny: Fatal Attraction , 2005, Current Biology.

[25]  K. Peterson,et al.  Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences , 2001, Evolution & development.

[26]  M. Telford,et al.  The place of phylogeny and cladistics in Evo-Devo research. , 2003, The International journal of developmental biology.

[27]  Leo X. Liu,et al.  Large-scale taxonomic profiling of eukaryotic model organisms: a comparison of orthologous proteins encoded by the human, fly, nematode, and yeast genomes. , 1998, Genome research.

[28]  B. Snel,et al.  Genome phylogeny based on gene content , 1999, Nature Genetics.

[29]  Hung D. Nguyen,et al.  New Maximum Likelihood Estimators for Eukaryotic Intron Evolution , 2005, PLoS Comput. Biol..

[30]  Michael W. Berry,et al.  An SVD-based comparison of nine whole eukaryotic genomes supports a coelomate rather than ecdysozoan lineage , 2004, BMC Bioinformatics.

[31]  J. Farris Phylogenetic Analysis Under Dollo's Law , 1977 .

[32]  W. Wheeler,et al.  Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology. , 2000, Systematic biology.

[33]  J. Felsenstein Cases in which Parsimony or Compatibility Methods will be Positively Misleading , 1978 .

[34]  R. Raff,et al.  Molecular phylogeny of the animal kingdom. , 1988, Science.

[35]  J. Felsenstein Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. , 1996, Methods in enzymology.

[36]  H. Philippe,et al.  Archaea sister group of Bacteria? Indications from tree reconstruction artifacts in ancient phylogenies. , 1999, Molecular biology and evolution.

[37]  J. W. Valentine,et al.  The significance of moulting in Ecdysozoan evolution , 2000, Evolution & development.

[38]  J. W. Valentine,et al.  Defining phyla: evolutionary pathways to metazoan body plans , 2001, Evolution & development.

[39]  B. Snel,et al.  Genome trees and the nature of genome evolution. , 2005, Annual review of microbiology.

[40]  G. Pesole,et al.  Long-branch attraction phenomenon and the impact of among-site rate variation on rodent phylogeny. , 2000, Gene.

[41]  A. Wilson,et al.  Ancient origin of lactalbumin from lysozyme: Analysis of DNA and amino acid sequences , 2005, Journal of Molecular Evolution.

[42]  Alexei Fedorov,et al.  Large-scale comparison of intron positions among animal, plant, and fungal genes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Victor A. Albert,et al.  Parsimony, phylogeny, and genomics , 2006 .

[44]  Teresa M. Przytycka,et al.  An Important Connection Between Network Motifs and Parsimony Models , 2006, RECOMB.

[45]  R. Raff,et al.  Evidence for a clade of nematodes, arthropods and other moulting animals , 1997, Nature.

[46]  M. Telford The multimeric β‐thymosin found in nematodes and arthropods is not a synapomorphy of the Ecdysozoa , 2004, Evolution & development.

[47]  Liran Carmel,et al.  Ecdysozoan clade rejected by genome-wide analysis of rare amino acid replacements. , 2007, Molecular biology and evolution.

[48]  S. Blair Hedges,et al.  The origin and evolution of model organisms , 2002, Nature Reviews Genetics.

[49]  M. Nei,et al.  Molecular Evolution and Phylogenetics , 2000 .

[50]  H. Philippe,et al.  The new phylogeny of eukaryotes. , 2000, Current opinion in genetics & development.

[51]  F. Delsuc,et al.  Phylogenomics and the reconstruction of the tree of life , 2005, Nature Reviews Genetics.

[52]  Hervé Philippe,et al.  Phylogeny: A non-hyperthermophilic ancestor for Bacteria , 2002, Nature.

[53]  J. Dopazo,et al.  Genome-scale evidence of the nematode-arthropod clade , 2005, Genome Biology.

[54]  M. Manuel,et al.  The Comparison of β-Thymosin Homologues Among Metazoa Supports an Arthropod-Nematode Clade , 2000, Journal of Molecular Evolution.

[55]  H. Philippe,et al.  Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. , 2005, Molecular biology and evolution.

[56]  J. McInerney,et al.  The Opisthokonta and the Ecdysozoa may not be clades: stronger support for the grouping of plant and animal than for animal and fungi and stronger support for the Coelomata than Ecdysozoa. , 2005, Molecular biology and evolution.

[57]  Alexei Fedorov,et al.  Mystery of intron gain. , 2003, Genome research.

[58]  H. Philippe,et al.  Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model , 2007, BMC Evolutionary Biology.

[59]  R. Raff Understanding Evolution: The Next Step. (Book Reviews: The Shape of Life. Genes, Development, and the Evolution of Animal Form.) , 1996 .