Cited by 51Genomics and Phylogenetic StudiesInvertebrate Taxonomy and EcologyMarine Invertebrate Physiology and Ecology

Deep Genomic-Scale Analyses of the Metazoa Reject Coelomata: Evidence from Single- and Multigene Families Analyzed Under a Supertree and Supermatrix Paradigm

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Holton, Thérèse A., Pisani, Davide·2010·Genome Biology and Evolution

Abstract

Solving the phylogeny of the animals with bilateral symmetry has proven difficult. Morphological studies have suggested a variety of alternative hypotheses, of which, Hyman's Coelomata hypothesis has become the most established. Studies based on 18S rRNA have failed to endorse Coelomata, supporting instead the rearrangement of the protostomes into two new clades: the Lophotrochozoa (including, e.g., the molluscs and the annelids) and the Ecdysozoa (including the Panarthropoda and most pseudocoelomates, such as the nematodes and priapulids). Support for this new animal phylogeny has been attained from expressed sequence tag studies, although these generally have a limited gene sampling. In contrast, deep genomic-scale analyses have often supported Coelomata. However, these studies are problematic due to their limited taxonomic sampling, which could exacerbate tree reconstruction artifacts. Here, we address both of these sampling limitations; we study the effect of long-branch attraction (LBA) in deep genomic-scale analyses and provide convincing evidence, using both single- and multigene families, that Coelomata is an artifact. We show that optimal outgroup selection is key in avoiding LBA and identify the use of inadequate outgroups as the reason previous deep genomic-scale analyses found strong support for Coelomata.

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  • The increased difficulty in overcoming LBA in the LEAP dataset compared to LEAN is because platyhelminths are more distantly related to arthropods than nematodes, and hence their shared evolutionary history and the internal branch joining these lineages is shorter.

    “This is because although both lineages are fast evolving, platyhelminths (LEAP) are more distantly related to arthropods than nematodes (LEAN), and hence their shared evolutionary history, and the internal branch joining these lineages, is shorter57,58.”

    From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [58]

    The Results (Four-Taxon Data Sets; page unavailable) place a nematode as the sister group of an arthropod and discuss long-branch attraction. The paper does not compare LEAP with LEAN or attribute a shorter shared history or internal branch to platyhelminths’ relationship with arthropods, so it does not support the proposed explanation for the difference between those datasets. (LLM, conf=0.83)

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Research works printed but not linked: 51

  1. Aguinaldo AMA Evidence for a clade of nematodes, arthropods and other moulting animals Nature 1997 387 489 493 9168109
  2. Belinky F Cohen O Huchon D Large-scale parsimony analysis of metazoan indels in protein-coding genes Mol Biol Evol. 2010 27 441 451 19864469
  3. Blair JE Ikeo K Gojobori T Hedges SB The evolutionary position of nematodes BMC Evol Biol. 2002 2 7 11985779 PMC102755
  4. Bourlat SJ Nielsen C Economou AE Telford MJ Testing the new animal phylogeny: a phylum level molecular analysis of the animal kingdom Mol Phylogenet Evol. 2008 49 23 31 18692145
  5. Brinkmann H Philippe H Archaea sister group of Bacteria? Indications from tree reconstruction artefacts in ancient phylogenies Mol Biol Evol. 1999 16 817 825 10368959
  6. Burleigh JG Driskell AC Sanderson MJ Supertree bootstrapping methods for assessing phylogenetic variation among genes in genome-scale data sets Syst Biol. 2006 55 426 440 16861207
  7. Castresana J Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis Mol Biol Evol. 2000 17 540 552 10742046
  8. Copley RR Aloy P Russell RB Telford MJ Systematic searches for molecular synapomorphies in model metazoan genomes give some support for Ecdysozoa after accounting for the idiosyncrasies of Caenorhabditis elegans Evol Dev. 2004 6 164 169 15099303
  9. Creevy CJ McInerney JO Clann: investigating phylogenetic information through supertree analyses Bioinformatics 2005 21 390 392 15374874
  10. Delsuc F Brinkmann H Philippe H Phylogenomics and the reconstruction of the tree of life Nat Rev Genet. 2005 6 361 375 15861208
  11. Dopazo H Dopazo J Genome-scale evidence of the nematode-arthropod clade Genome Biol. 2005 6 R41 15892869 PMC1175953
  12. Dopazo H Santoyo J Dopazo J Phylogenomics and the number of characters required for obtaining an accurate phylogeny of eukaryote model species Bioinformatics 2004 20 i116 i121 15262789
  13. Enright AJ Van Dongen S Ouzounis CA An efficient algorithm for large-scale detection of protein families Nucleic Acids Res. 2002 30 1575 1584 11917018 PMC101833
  14. Fitzpatrick DA Logue ME Stajich JE Butler G A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis BMC Evol Biol. 2006 6 99 17121679 PMC1679813
  15. Guindon S Gascuel O A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood Syst Biol. 2003 52 696 704 14530136
  16. Halanych KM Evidence from 18S ribosomal DNA that the lophophorates are protostome animals Science 1995 267 1641 1643 7886451
  17. Hyman LH The invertebrates. Vol. 1: Protozoa through Ctenophora 1940 New York McGraw-Hill
  18. Irimia M Maeso I Penny D Garcia-Fernàndez J Roy SW Rare coding sequence changes are consistent with Ecdysozoa, not Coelomata Mol Biol Evol. 2007 24 1604 1607 17525471
  19. Keane TM Creevy CJ Pentony MM Naughton TJ McInerney JO Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified BMC Evol Biol. 2006 6 29 16563161 PMC1435933
  20. Lartillot N Philippe H A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process Mol Biol Evol. 2004 21 1095 1109 15014145
  21. Lartillot N Philippe H Improvement of molecular phylogenetic inference and the phylogeny of the Bilateria Philos Trans R Soc Lond B. 2008 363 1463 1472 18192187 PMC2615818
  22. Littlewood DT Olsen PD Telford MJ Herniou EA Riutort M Elongation factor 1-alpha sequences alone do not assist in resolving the position of the acoela within the metazoa Mol Biol Evol. 2001 18 437 442 11230546
  23. Löytynoja A Goldman N Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis Science 2008 320 1632 1635 18566285
  24. McInerney JO Cotton JA Pisani D The prokaryotic tree of life: past, present… and future? Trends Ecol Evol. 2008 23 276 281 18367290
  25. Moore BR Smith SA Donoghue MJ Increasing data transparency and estimating phylogenetic uncertainty in supertrees: approaches using nonparametric bootstrapping Syst Biol. 2006 55 662 676 16969942
  26. Nielsen C Animal evolution, interrelationships of the living phyla 2001 Oxford Oxford University Press
  27. Philip GK Creevy CJ McInerney JO 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 got the Coelomata than Ecdysozoa Mol Biol Evol. 2005 22 1175 1184 15703245
  28. Philippe H Brinkmann H Martinez P Riutort M Baguñà J Acoel flatworms are not platyhelminthes: evidence from phylogenomics PLoS One 2007 2 e717 17684563 PMC1933604
  29. Philippe H Phylogenomics revives traditional views on deep animal relationships Curr Biol. 2009 19 706 712 19345102
  30. Philippe H Lartillot N Brinkmann H Multi gene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia Mol Biol Evol. 2005 22 1246 1253 15703236
  31. Pisani D Cotton JA McInerney JO Supertrees disentangle the chimerical origin of eukaryotic genomes Mol Biol Evol. 2007 24 1752 1760 17504772
  32. Pisani D Wilkinson M Matrix representation with parsimony, taxonomic congruence, and total evidence Syst Biol. 2002 51 151 155 11943097
  33. Ragan MA Phylogenetic inference based on matrix representation of trees Mol Phylogenet Evol. 1992 1 53 58 1342924
  34. Robinson M Gouy M Gautier C Mouchiroud D Sensitivity of the relative-rate test to taxonomic sampling Mol Biol Evol. 1998 15 1091 1098 9729873
  35. Rogozin IB Thomson K Csürös M Carmel L Koonin EV Homoplasy in genome-wide analysis of rare amino acid replacements: the molecular-evolutionary basis for Vavilov's law of homologous series Biol Direct. 2008 3 7 18346278 PMC2292158
  36. Rogozin IB Wolf YI Carmel L Koonin EV Analysis of rare amino acid replacements supports the Coelomata clade Mol Biol Evol. 2007 24 2594 2597 17921482
  37. Rokas A Carroll SB More genes or more taxa? The relative contribution of gene number and taxon number to phylogenetic accuracy Mol Biol Evol. 2005 22 1337 1344 15746014
  38. Ronquist F Huelsenbeck JP MrBayes 3: Bayesian phylogenetic inference under mixed models Bioinformatics 2003 19 1572 1574 12912839
  39. Rosenberg MS Kumar S Incomplete taxon sampling is not a problem for phylogenetic inference Proc Natl Acad Sci U S A. 2001 98 10751 10756 11526218 PMC58547
  40. Rota-Stabelli O Telford MJ A multi criterion approach for the selection of optimal outgroups in phylogeny: recovering some support for the Mandibulata over Myriochelata using mitogenomics Mol Phylogenet Evol. 2008 48 103 111 18501642
  41. Roy SW Irimia M Rare genomic characters do not support Coelomata: intron loss/gain Mol Biol Evol. 2008 25 620 623 18281272
  42. Ruiz-Trillo I Riutort M Littlewood DTJ Herniou EA Baguna J Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes Science 1999 283 1919 1923 10082465
  43. Semple C Steel M Phylogenetics 2003 New York Oxford University Press
  44. Telford MJ Bourlat SJ Economou A Papillon D Rota-Stabelli O The evolution of the Ecdysozoa Philos Trans R Soc Lond B Biol Sci. 2008 363 1529 1537 18192181 PMC2614232
  45. Thompson JD Higgins DG Gibson TJ CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 1994 22 4673 4680 7984417 PMC308517
  46. Wehe A Bansal MS Burleigh JG Eulenstein O DupTree: a program for large-scale phylogenetic analyses using gene tree parsimony Bioinformatics 2008 24 1540 1541 18474508
  47. Wilkinson M Cotton JA Hodkinson T Parnell J Waldren S Supertree methods for building the tree of life: divide-and-conquer approaches to large phylogenetic problems Towards the tree of life: taxonomy and systematics of large and species rich taxa 2006 Systematic Association special volume. CRC Press 61 75
  48. Wolf YI Rogozin IB Koonin EV Coelomata and not Ecdysozoa: evidence from genome-wide phylogenetic analysis Genome Res. 2004 14 29 36 14707168 PMC314272
  49. Yang Z Computational molecular evolution. Oxford series in ecology and evolution 2006 New York Oxford University Press
  50. Zheng J Rogozin IB Koonin EV Przytycka TM Support for the Coelomata clade of animals from a rigorous analysis of the pattern of intron conservation Mol Biol Evol. 2007 24 2583 2592 17893400
  51. Zilversmit M O'Grady P Desalle R Shallow genomics, phylogenetics, and evolution in the family Drosophilidae Pac Symp Biocomput. 2002 7 512 523 11928503

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Authors
Holton, T. A., & Pisani, D.
Affiliations
National University of Ireland, Maynooth (IE)
Corresponding author
Holton, Thérèse A.
Venue
Genome Biology and Evolution
Published
2010-01-01
Volume
2
Pages
310-324
ISSN
1759-6653 (ISSN-L)
OpenAlex
W2162552502
Cited by
51
References
9
Citations by year
2023: 1 · 2022: 5 · 2021: 2 · 2020: 3 · 2017: 1 · 2016: 2 · 2015: 2 · 2014: 4 · 2013: 10 · 2012: 13
FWCI
4.04
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Genome Biology and Evolution (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Explore Bristol Research (publishedVersion)
  • Bristol Research (University of Bristol) (submittedVersion)
Funders
  • Irish Research Council for Science, Engineering and Technology
  • Science Foundation Ireland
  • Irish Centre for High-End Computing
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Invertebrate Taxonomy and Ecology
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Keywords
animal phylogeny, animals, long-branch attraction, outgroup selection, Lophotrochozoa, Ecdysozoa, gene family, supertree, supermatrix, taxon sampling, 18S rRNA phylogeny
MeSH terms
Animals, Bayes Theorem, Multigene Family, Invertebrates, Models, Genetic, Phylogeny, Proteins, Evolution, Molecular, Genomics, Databases, Genetic, Eukaryota

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