Evidence for a clade of nematodes, arthropods and other moulting animals
Abstract
The arthropods constitute the most diverse animal group, but, despite their rich fossil record and a century of study, their phylogenetic relationships remain unclear. Taxa previously proposed to be sister groups to the arthropods include Annelida, Onychophora, Tardigrada and others, but hypotheses of phylogenetic relationships have been conflicting. For example, onychophorans, like arthropods, moult periodically, have an arthropod arrangement of haemocoel, and have been related to arthropods in morphological and mitochondrial DNA sequence analyses. Like annelids, they possess segmental nephridia and muscles that are a combination of smooth and obliquely striated fibres. 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, kinorhynchs 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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Analyses of nuclear SSU rRNA sequences have limitations including nucleotide compositional bias, among site rate variation, and heterogeneous rates of evolution across lineages.
“Among the limitations noted are nucleotide compositional bias, among site rate variation, and heterogeneous rates of evolution across lineages (12–16).”
From Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA (2001) · cites this paper as [13]
Cites
The fossil record and the early evolution of the Metazoa
Morris, S. C. (1993) · Nature · doi:10.1038/361219a0 · Cited by 389 · see citing works
Evidence from 12 <i>S</i> Ribosomal RNA Sequences that Onychophorans Are Modified Arthropods
Ballard, J. W. O., Olsen, G. J., Faith, D. P., Odgers, W. A., Rowell, D. M., & Atkinson, P. W. (1992) · Science · doi:10.1126/science.1455227 · Cited by 248 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Broad phylogenomic sampling improves resolution of the animal tree of life
Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., Seaver, E., Rouse, G. W., Obst, M., Edgecombe, G. D., et al. (2008) · Nature · doi:10.1038/nature06614 · Cited by 1,921 · see citing works
Genome-scale approaches to resolving incongruence in molecular phylogenies.
Rokas, A., Williams, B. L., King, N., & Carroll, S. B. (2003) · Nature · doi:10.1038/nature02053 · Cited by 1,512 · see citing works
A review of long-branch attraction
Bergsten, J. (2005) · Cladistics · doi:10.1111/j.1096-0031.2005.00059.x · Cited by 1,162 · see citing works
Early animal evolution: emerging views from comparative biology and geology
Knoll, A. H., & Carroll, S. B. (1999) · Science · doi:10.1126/science.284.5423.2129 · Cited by 821 · see citing works
The origin and evolution of model organisms
Hedges, S. B. (2002) · Nature Reviews Genetics · doi:10.1038/nrg929 · Cited by 806 · see citing works
Lartillot, N., Brinkmann, H., & Philippe, H. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-s1-s4 · Cited by 705 · see citing works
WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra
Hobmayer, B., Rentzsch, F., Kuhn, K., Happel, C. M., von Laue, C. C., Snyder, P., Rothbächer, U., & Holstein, T. W. (2000) · Nature · doi:10.1038/35025063 · Cited by 599 · see citing works
Comparative genomics and evolution of proteins involved in RNA metabolism
Anantharaman, V. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.7.1427 · Cited by 541 · see citing works
Peterson, K. J., & Eernisse, D. J. (2001) · Evolution & Development · doi:10.1046/j.1525-142x.2001.003003170.x · Cited by 529 · see citing works
Control and biochemical nature of the ecdysteroidogenic pathway
Gilbert, L. I., Rybczynski, R., & Warren, J. T. (2002) · Annual Review of Entomology · doi:10.1146/annurev.ento.47.091201.145302 · Cited by 532 · see citing works
The new animal phylogeny: Reliability and implications
Adoutte, A., Balavoine, G., Lartillot, N., Lespinet, O., Prud'homme, B., & de Rosa, R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4453 · Cited by 512 · see citing works
Wang, D. Y.-C., Kumar, S., & Hedges, S. B. (1999) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.1999.0617 · Cited by 493 · see citing works
The evolution of signalling pathways in animal development
Pires-daSilva, A., & Sommer, R. J. (2003) · Nature Reviews Genetics · doi:10.1038/nrg977 · Cited by 466 · see citing works
The New View of Animal Phylogeny
Halanych, K. M. (2004) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.35.112202.130124 · Cited by 489 · see citing works
Rogozin, I. B., Wolf, Y. I., Sorokin, A. V., Mirkin, B. G., & Koonin, E. V. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00558-x · Cited by 445 · see citing works
A critical reappraisal of the fossil record of the bilaterian phyla
BUDD, G. E., & JENSEN, S. (2000) · Biological Reviews of the Cambridge Philosophical Society · doi:10.1017/s000632310000548x · Cited by 428 · see citing works
Medina, M., Collins, A. G., Silberman, J. D., & Sogin, M. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171316998 · Cited by 395 · see citing works
Kortschak, R. D., Samuel, G., Saint, R., & Miller, D. J. (2003) · Current Biology · doi:10.1016/j.cub.2003.11.030 · Cited by 353 · see citing works
The last common bilaterian ancestor
Erwin, D. H., & Davidson, E. H. (2002) · Development · doi:10.1242/dev.129.13.3021 · Cited by 320 · see citing works
How good are deep phylogenetic trees?
Philippe, H., & Laurent, J. (1998) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(98)80028-2 · Cited by 324 · see citing works
Philippe, H., Delsuc, F., Brinkmann, H., & Lartillot, N. (2005) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.35.112202.130205 · Cited by 306 · see citing works
Fossils, molecules and embryos: new perspectives on the Cambrian explosion
Valentine, J. W., Jablonski, D., & Erwin, D. H. (1999) · Development · doi:10.1242/dev.126.5.851 · Cited by 300 · see citing works
Small Bilaterian Fossils from 40 to 55 Million Years Before the Cambrian
Chen, J.-Y., Bottjer, D. J., Oliveri, P., Dornbos, S. Q., Gao, F., Ruffins, S., Chi, H., Li, C.-W., & Davidson, E. H. (2004) · Science · doi:10.1126/science.1099213 · Cited by 284 · see citing works
Spiralian Phylogeny Informs the Evolution of Microscopic Lineages
Laumer, C. E., Bekkouche, N., Kerbl, A., Goetz, F., Neves, R. C., Sørensen, M. V., Kristensen, R. M., Hejnol, A., Dunn, C. W., Giribet, G., et al. (2015) · Current Biology · doi:10.1016/j.cub.2015.06.068 · Cited by 278 · see citing works
Vertebrate-Type Intron-Rich Genes in the Marine Annelid <i>Platynereis dumerilii</i>
Raible, F., Tessmar-Raible, K., Osoegawa, K., Wincker, P., Jubin, C., Balavoine, G., Ferrier, D., Benes, V., de Jong, P., Weissenbach, J., et al. (2005) · Science · doi:10.1126/science.1119089 · Cited by 257 · see citing works
Phylogenomic Insights into Animal Evolution
Telford, M. J., Budd, G. E., & Philippe, H. (2015) · Current Biology · doi:10.1016/j.cub.2015.07.060 · Cited by 213 · see citing works
Dating the Time of Origin of Major Clades: Molecular Clocks and the Fossil Record
Smith, A. B., & Peterson, K. J. (2002) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.30.091201.140057 · Cited by 193 · see citing works
The phylogenetic position of ctenophores and the origin(s) of nervous systems
Jákely, G., Paps, J., & Nielsen, C. (2015) · EvoDevo · doi:10.1186/2041-9139-6-1 · Cited by 189 · see citing works
Precambrian animal diversity: Putative phosphatized embryos from the Doushantuo Formation of China
Chen, J.-Y., Oliveri, P., Li, C.-W., Zhou, G.-Q., Gao, F., Hagadorn, J. W., Peterson, K. J., & Davidson, E. H. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4457 · Cited by 187 · see citing works
A Molecular Phylogenetic Framework for the Phylum Ctenophora Using 18S rRNA Genes
Podar, M., Haddock, S. H. D., Sogin, M. L., & Harbison, G. R. (2001) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.2001.1036 · Cited by 175 · see citing works
Darwin's dilemma: the realities of the Cambrian ‘explosion’
Conway Morris, S. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1846 · Cited by 179 · see citing works
Torruella, G., Derelle, R., Paps, J., Lang, B. F., Roger, A. J., Shalchian-Tabrizi, K., & Ruiz-Trillo, I. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/msr185 · Cited by 169 · see citing works
On Reduced Amino Acid Alphabets for Phylogenetic Inference
Susko, E., & Roger, A. J. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm144 · Cited by 177 · see citing works
Mushegian, A. R., Garey, J. R., Martin, J., & Liu, L. X. (1998) · Genome Research · doi:10.1101/gr.8.6.590 · Cited by 164 · see citing works
Self-citationThe Evolution of Early Neurogenesis
Hartenstein, V., & Stollewerk, A. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.02.004 · Cited by 161 · see citing works
Philippe, H., Poustka, A. J., Chiodin, M., Hoff, K. J., Dessimoz, C., Tomiczek, B., Schiffer, P. H., Müller, S., Domman, D., Horn, M., et al. (2019) · Current Biology · doi:10.1016/j.cub.2019.04.009 · Cited by 152 · see citing works
A critical reappraisal of the fossil record of the bilaterian phyla
BUDD, G. E., & JENSEN, S. (2000) · Biological Reviews · doi:10.1111/j.1469-185x.1999.tb00046.x · Cited by 145 · see citing works
A new perspective on lower metazoan relationships from 18S rDNA sequences
Kim, J., Kim, W., & Cunningham, C. W. (1999) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026124 · Cited by 143 · see citing works
Bilaterian Origins: Significance of New Experimental Observations
Peterson, K. J., Cameron, R. A., & Davidson, E. H. (2000) · Developmental Biology · doi:10.1006/dbio.1999.9475 · Cited by 133 · see citing works
Phytoecdysteroids: A novel defense against plant-parasitic nematodes
Soriano, I. R., Riley, I. T., Potter, M. J., & Bowers, W. S. (2004) · Journal of Chemical Ecology · doi:10.1023/b:joec.0000045584.56515.11 · Cited by 126 · see citing works
Copley, R. R., Aloy, P., Russell, R. B., & Telford, M. J. (2004) · Evolution & Development · doi:10.1111/j.1525-142x.2004.04021.x · Cited by 108 · see citing works
Rooting the tree of life: the phylogenetic jury is still out
Gouy, R., Baurain, D., & Philippe, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0329 · Cited by 96 · see citing works
PETERSON, K. J., SUMMONS, R. E., & DONOGHUE, P. C. J. (2007) · Palaeontology · doi:10.1111/j.1475-4983.2007.00692.x · Cited by 93 · see citing works
Van Auken, K., Weaver, D. C., Edgar, L. G., & Wood, W. B. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4499 · Cited by 89 · see citing works
The LAP family: a phylogenetic point of view
Santoni, M.-J., Pontarotti, P., Birnbaum, D., & Borg, J.-P. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(02)02738-5 · Cited by 88 · see citing works
Organization of an echinoderm <i>Hox</i> gene cluster
Martinez, P., Rast, J. P., Arenas-Mena, C., & Davidson, E. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1469 · Cited by 85 · see citing works
Kocot, K. M. (2016) · Organisms Diversity & Evolution · doi:10.1007/s13127-015-0261-3 · Cited by 59 · see citing works
Finnerty, J. R. (2005) · BioEssays · doi:10.1002/bies.20299 · Cited by 59 · see citing works
THE AGE AND RELATIONSHIPS OF THE MAJOR ANIMAL PHYLA
Lynch, M. (1999) · Evolution · doi:10.1111/j.1558-5646.1999.tb03768.x · Cited by 64 · see citing works
Zhao, H., & Nonet, M. L. (2000) · Development · doi:10.1242/dev.127.6.1253 · Cited by 57 · see citing works
The mouth, the anus, and the blastopore—open questions about questionable openings
Hejnol, A., & Martindale, M. Q. (2009) · Animal Evolution · doi:10.1093/acprof:oso/9780199549429.003.0004 · Cited by 37 · see citing works
Models for Gut-Mediated Horizontal Gene Transfer by Bacterial Plasmid Conjugation
Ott, L. C., & Mellata, M. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.891548 · Cited by 32 · see citing works
She Shapes Events as they Come: Plasticity in Female Insect Reproduction
Hodin, J. (2009) · Phenotypic Plasticity of Insects · doi:10.1201/b10201-12 · Cited by 28 · see citing works
Origin of Metazoan Developmental Toolkits and Their Expression in the Fossil Record
Tweedt, S. M., & Erwin, D. H. (2015) · Advances in Marine Genomics · doi:10.1007/978-94-017-9642-2_3 · Cited by 27 · see citing works
Genomic, phylogenetic, and cell biological insights into metazoan origins
Nichols, S. A., Dayel, M. J., & King, N. (2009) · Animal Evolution · doi:10.1093/acprof:oso/9780199549429.003.0003 · Cited by 24 · see citing works
Near intron pairs and the metazoan tree
Lehmann, J., Stadler, P. F., & Krauss, V. (2013) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2012.11.012 · Cited by 11 · see citing works
When Chinese Masks Meet Phylogenetics
Russo, C. A. M., Aguiar, B., Voloch, C. M., & Selvatti, A. P. (2016) · The American Biology Teacher · doi:10.1525/abt.2016.78.3.241 · Cited by 3 · see citing works
- Authors
- Aguinaldo, A. M. A., Turbeville, J. M., Linford, L. S., Rivera, M. C., Garey, J. R., Raff, R. A., & Lake, J. A.
- Affiliations
- University of California, Los Angeles (US)
- University of Arkansas at Fayetteville (US)
- Duquesne University (US)
- Indiana University Bloomington (US)
- ORCID
- Garey, James R.
- Venue
- Nature
- Published
- 1997-05
- Volume
- 387
- Issue
- 6632
- Pages
- 489-493
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2029482176
- Cited by
- 1,609
- References
- 2
- Citations by year
- 2026: 23 · 2025: 20 · 2024: 39 · 2023: 14 · 2022: 37 · 2021: 43 · 2020: 36 · 2019: 21 · 2018: 23 · 2017: 30 · 2016: 46 · 2015: 42 · 2014: 43 · 2013: 37 · 2012: 54
- FWCI
- 136.47
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Invertebrate Taxonomy and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Tardigrade Biology and Ecology
- Keywords
- arthropod phylogeny, nematodes, Ecdysozoa, molting, Onychophora, tardigrades, nematomorphs, Kinorhyncha, priapulids, Articulata, 18S rDNA phylogeny, Caenorhabditis elegans, Drosophila melanogaster, developmental genetics, hemocoel
- MeSH terms
- Animals, Arthropods, Biological Evolution, Molecular Sequence Data, Nematoda, Phylogeny, RNA, Ribosomal, 18S
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
