Evidence for a clade of nematodes, arthropods and other moulting animals - Nature
- ️Lake, James A.
- ️Thu May 29 1997
Abstract
The arthropods constitute the most diverse animal group, but, despite their rich fossil record and a century of study, their phylogenetic relationships remain unclear1. Taxa previously proposed to be sister groups to the arthropods include Annelida, Onychophora, Tardigrada and others, but hypotheses of phylogenetic relationships have been conflicting2,3. For example, onychophorans, like arthropods, moult periodically, have an arthropod arrangement of haemocoel1,4, and have been related to arthropods in morphological and mitochondrial DNA sequence analyses4,5. Like annelids, they possess segmental nephridia and muscles that are a combination of smooth and obliquely striated fibres6. Our phylogenetic analysis of 18S ribosomal DNA sequences indicates a close relationship between arthropods, nematodes and all other moulting phyla. The results suggest that ecdysis (moulting) arose once and support the idea of a new clade, Ecdysozoa, containing moulting animals: arthropods, tardigrades, onychophorans, nematodes, nematomorphs, kinor-hynchs and priapulids. No support is found for a clade of segmented animals, the Articulata, uniting annelids with arthropods. The hypothesis that nematodes are related to arthropods has important implications for developmental genetic studies using as model systems the nematode Caenorhabditis elegans and the arthropod Drosophila melanogaster, which are generally held to be phylogenetically distant from each other.
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References
Boudreaux, H. B. Arthropod Phylogeny with Special Reference to Insects (Wiley, New York, 1979).
Raff, R. A., Marshall, C. R. & Turbeville, J. M. Using DNA sequences to unravel the Cambrian radiation of the animal phyla. Annu. Rev. Ecol. Syst. 25, 351–375 (1994).
Eernisse, D. J., Albert, J. S. & Anderson, F. E. Annelida and Arthropoda are not sister taxa: a phylogenetic analysis of spiralian metazoan morphology. Syst. Biol. 41, 305–330 (1992).
Ballard, J. W. et al. Evidence from 12S ribosomal RNA sequences that onychophorans are modified arthropods. Science 258, 1345–1348 (1992).
Weygoldt, P. Arthropod relationships: the phylogenetic-systematic approach. Z. Zool. Syst. Evolut.-forsch. 24, 19–35 (1986).
Brusca, R. C. & Brusca, G. J. Invertebrates (Sinauer, Sunderland, MA, 1990).
Halanych, K. M. et al. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267, 1641–1632 (1995).
Lake, J. A. The order of sequence alignment can bias the selection of tree topology. Biol. Evol. 8, 378–385 (1991).
Stewart, C.-B. The powers and pitfalls of parsimony. Nature 361, 603–607 (1993).
Winnepenninckx, B. et al. 18S rRNA data indicate that aschelminthes are polyphyletic in origin and consist of at least three distinct clades. Mol. Biol. Evol. 12, 1132–1137 (1995).
Wright, K. in Microscopic Anatomy of Invertebrates Vol. 4 (eds Harrison, F. W. & Ruppert, E. E.) 111–195 (Wiley-Liss, New York, 1991).
Lake, J. A. Reconstructing evolutionary trees from DNA and protein sequences: Paralinear distances. Proc. Natl Acad. Sci. USA 91, 1455–1459 (1994).
Lockhart, P. J., Steel, M. A., Hendy, M. D. & Penny, D. Recovering evolutionary trees under a more realistic model of sequence evolution. Mol. Biol. Evol. 11, 605–612 (1994).
Field, K. G. et al. Molecular phylogeny of the animal kingdom. Science 239, 748–753 (1988).
Hillis, D. M. & Bull, J. J. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42, 182–192 (1993).
Nielsen, C. Animal Evolution: Interrelationships of the Living Phyla (Oxford University Press, 1995).
Gee, H. Before the Backbone: Views on the Origin of the Vertebrates (Chapman & Hall, London, 1996).
Balavoine, G. The early emergence of plaryhelminths is contradicted by the agreement between 18S rRNA and Hox data C. R. Acad. Sci. Paris Life Sci. 320, 83–94 (1997).
Valentine, J. W. Bilaterians of the Precambrian–Cambrian transition and the annelid–arthropod relationship. Proc. Natl Acad. Sci. USA 86, 2272–2275 (1989).
petterson, C. The Hierarchy of Life (eds Fernholm, B., Bremer, K. & Jornvall, H.) 471–488 (Elsevier, Amsterdam, 1989).
Lake, J. A. Origin of the Metazoa. Proc. Natl Acad. Sci. USA 87, 763–766 (1990).
Ruppert, E. E. in Microscopic Anatomy of Invertebrates Vol. 4, (eds Harrison, R. W. & Ruppert, E. E.) 1–17 (Wiley-Liss, New York, 1991).
de Queiroz, K. & Gauthier, J. Phylogeny as a central principle in taxonomy: Phylogenetic definitions of taxon names. Syst. Zool. 39, 307–322 (1990).
Boore, J. L., Collins, T. M., Stanton, S., Daehier, L. L. & Brown, W. M. Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature 376 163–165 (1995).
Conway Morris, S. The fossil record and the early evolution of the Metazoa. Nature 361, 219–225 (1993).
Lake, J. A. Calculating the probability of multitaxon evolutionary trees: Bootstrappers Gambit Proc. Natl Acad. Sci. USA 92, 9662–9666 (1995).
Goldman, N. Simple diagnostic statistical tests of models for DNA substitution. J. Mol. Evol. 37, 650–661 (1993).
Felsenstein, J. & Churchill, G. A. A hidden Markov model approach to variation among sites in rate of evolution. Mol. Biol. Evol. 13, 93–104 (1996).
Wallace, R. L., Ricci, C. & Malone, G. A cladistic analysis of pseudoceolomate (aschelminth) morphology. Invert. Biol. 115, 104–112 (1996).
Garey, J. R., Krotec, M., Nelson, D. R. & Brooks, J. Molecular analysis supports a Tardigrade–Arthropod association. Invert. Biol. 115, 79–88 (1996).
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Authors and Affiliations
Molecular Biology Institute and MCD Biology, University of California, Los Angeles, California, 90095, USA
Anna Marie A. Aguinaldo, Lawrence S. Linford, Maria C. Rivera & James A. Lake
Department of Biological Sciences, University of Arkansas, Fayetteville, Arkansas, 72701, USA
James M. Turbeville
Department of Biological Sciences, Duquesne University, Pittsburgh, Pennsylvania, 15282
James R. Garey
Department of Biology, University of South Florida, Tampa, Florida, 33620, USA
James R. Garey
Department of Biology and Indiana Molecular Biology Institute, Indiana University, Bloomington, Indiana, 47405, USA
Rudolf A. Raff
Authors
- Anna Marie A. Aguinaldo
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- James M. Turbeville
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- Lawrence S. Linford
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- Maria C. Rivera
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- James R. Garey
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- Rudolf A. Raff
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- James A. Lake
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Aguinaldo, A., Turbeville, J., Linford, L. et al. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489–493 (1997). https://doi.org/10.1038/387489a0
Received: 07 November 1996
Accepted: 03 April 1997
Issue Date: 29 May 1997
DOI: https://doi.org/10.1038/387489a0