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The origin and evolution of arthropods

Nature volume 457, pages 812–817 (2009)Cite this article

Abstract

The past two decades have witnessed profound changes in our understanding of the evolution of arthropods. Many of these insights derive from the adoption of molecular methods by systematists and developmental biologists, prompting a radical reordering of the relationships among extant arthropod classes and their closest non-arthropod relatives, and shedding light on the developmental basis for the origins of key characteristics. A complementary source of data is the discovery of fossils from several spectacular Cambrian faunas. These fossils form well-characterized groupings, making the broad pattern of Cambrian arthropod systematics increasingly consensual.

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Figure 1: Progress and problems in arthropod phylogeny.
Figure 2: Putative stem-group mandibulates and chelicerates.
Figure 3: Stem-group arthropods.
Figure 4: Possible anterior-appendage homologies and mouth rotation in arthropods.

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References

  1. Darwin, C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (John Murray, 1859).

    Google Scholar 

  2. Bowler, P. J. Life's Splendid Drama: Evolutionary Biology and the Reconstruction of Life's Ancestry (Chicago Univ. Press, 1996).

    Google Scholar 

  3. Ballard, J. W. O. et al. Evidence from 12S ribosomal-RNA sequences that onychophorans are modified arthropods. Science 258, 1345–1348 (1992).

    CAS  ADS  PubMed  Google Scholar 

  4. Telford, M. J., Bourlat, S. J., Economou, A., Papillon, D. & Rota-Stabelli, O. The evolution of the Ecdysozoa. Phil. Trans. R. Soc. Lond. B 363, 1529–1537 (2008).

    Google Scholar 

  5. Dunn, C. W. et al. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745–749 (2008). This paper provides the most recent analysis of the relationships of the Metazoa, using a broadly sampled phylogenomic-scale data set.

    CAS  ADS  PubMed  Google Scholar 

  6. Dzik, J. & Krumbiegel, G. The oldest 'onychophoran' Xenusion: a link connecting phyla? Lethaia 22, 169–182 (1989).

    Google Scholar 

  7. 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).

    Google Scholar 

  8. Aguinaldo, A. M. A. et al. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489–493 (1997). This classic paper provided the first strong evidence for the clade Ecdysozoa.

    CAS  PubMed  Google Scholar 

  9. Wagele, J. W., Erikson, T., Lockhart, P. & Misof, B. The Ecdysozoa: artifact or monophylum? J. Zoolog. Syst. Evol. Res. 37, 211–223 (1999).

    Google Scholar 

  10. Philip, G. K., Creevey, C. J. & McInerney, J. O. 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. Mol. Biol. Evol. 22, 1175–1184 (2005).

    CAS  PubMed  Google Scholar 

  11. Rogozin, I. B., Thomson, K., Csueroes, M., Carmel, L. & Koonin, E. V. Homoplasy in genome-wide analysis of rare amino acid replacements: the molecular-evolutionary basis for Vavilov's law of homologous series. Biol. Direct 3, 7 (2008).

    PubMed Central  PubMed  Google Scholar 

  12. Rogozin, I. B., Wolf, Y. I., Carmel, L. & Koonin, E. V. Analysis of rare amino acid replacements supports the Coelomata clade. Mol. Biol. Evol. 24, 2594–2597 (2007).

    CAS  PubMed  Google Scholar 

  13. Rogozin, I. B., Wolf, Y. I., Carmel, L. & Koonin, E. V. Ecdysozoan clade rejected by genome-wide analysis of rare amino acid replacements. Mol. Biol. Evol. 24, 1080–1090 (2007).

    CAS  PubMed  Google Scholar 

  14. Zheng, J., Rogozin, I. B., Koonin, E. V. & Przytycka, T. M. Support for the Coelomata clade of animals from a rigorous analysis of the pattern of intron conservation. Mol. Biol. Evol. 24, 2583–2592 (2007).

    CAS  PubMed  Google Scholar 

  15. Copley, R. R., Aloy, P., Russell, R. B. & Telford, M. J. Systematic searches for molecular synapomorphies in model metazoan genomes give some support for Ecdysozoa after accounting for the idiosyncrasies of Caenorhabditis elegans . Evol. Dev. 6, 164–169 (2004).

    CAS  PubMed  Google Scholar 

  16. Philippe, H., Lartillot, N. & Brinkmann, H. Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Mol. Biol. Evol. 22, 1246–1253 (2005).

    CAS  PubMed  Google Scholar 

  17. Webster, B. L. et al. Mitogenomics and phylogenomics reveal priapulid worms as extant models of the ancestral Ecdysozoan. Evol. Dev. 8, 502–510 (2006).

    PubMed  Google Scholar 

  18. Irimia, M., Maeso, I., Penny, D., Garcia-Fernàndez, J. & Roy, S. Rare coding sequence changes are consistent with Ecdysozoa, not Coelomata. Mol. Biol. Evol. 24, 1604–1607 (2007).

    CAS  PubMed  Google Scholar 

  19. Papillon, D., Perez, Y., Caubit, X. & Le Parco, Y. Identification of chaetognaths as protostomes is supported by the analysis of their mitochondrial genome. Mol. Biol. Evol. 21, 2122–2129 (2004).

    CAS  PubMed  Google Scholar 

  20. Schmidt-Rhaesa, A., Bartolomaeus, T., Lemburg, C., Ehlers, U. & Garey, J. R. The position of the Arthropoda in the phylogenetic system. J. Morphol. 238, 263–285 (1998).

    PubMed  Google Scholar 

  21. Budd, G. E. The morphology and phylogenetic significance of Kerygmachela kierkegaardi Budd (Buen Formation, Lower Cambrian, N Greenland). Trans. R. Soc. Edinb. 89, 249–290 (1999).

    Google Scholar 

  22. Eriksson, B. J. & Budd, G. E. Onychophoran cephalic nerves and their bearing on our understanding of head segmentation and stem-group evolution of Arthropoda. Arthropod Struct. Dev. 29, 197–209 (2000).

    CAS  PubMed  Google Scholar 

  23. Nielsen, C. Animal Evolution: Interrelationships of the Animal Phyla (Oxford Univ. Press, 2001).

    Google Scholar 

  24. Mallatt, J. & Giribet, G. Further use of nearly complete, 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol. Phylogenet. Evol. 40, 772–794 (2006).

    CAS  PubMed  Google Scholar 

  25. Bourlat, S. J., Nielsen, C., Economou, A. D. & Telford, M. J. Testing the new animal phylogeny: a phylum level analysis of the animal kingdom. Mol. Phylogenet. Evol. 49, 23–31 (2008).

    CAS  PubMed  Google Scholar 

  26. Manton, S. M. The Arthropoda: Habits, Functional Morphology and Evolution (Clarendon, 1977).

    Google Scholar 

  27. Fortey, R. A., Briggs, D. E. G. & Wills, M. A. The Cambrian evolutionary 'explosion': decoupling cladogenesis from morphological disparity. Biol. J. Linn. Soc. 57, 13–33 (1996).

    Google Scholar 

  28. Boore, J. L., Lavrov, D. V. & Brown, W. M. Gene translocation links insects and crustaceans. Nature 392, 667–668 (1998). This paper details a rare genomic change supporting Pancrustacea rather than Atelocerata.

    CAS  ADS  PubMed  Google Scholar 

  29. Giribet, G., Edgecombe, G. D. & Wheeler, W. C. Arthropod phylogeny based on eight molecular loci and morphology. Nature 413, 157–161 (2001).

    CAS  ADS  PubMed  Google Scholar 

  30. Mallatt, J. M., Garey, J. R. & Shultz, J. W. Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Mol. Phylogenet. Evol. 31, 178–191 (2004).

    CAS  PubMed  Google Scholar 

  31. Richter, S. The Tetraconata concept: hexapod–crustacean relationships and the phylogeny of Crustacea. Org. Divers. Evol. 2, 217–237 (2002).

    Google Scholar 

  32. Ungerer, P. & Scholtz, G. Filling the gap between identified neuroblasts and neurons in crustaceans adds new support for Tetraconata. Proc. R. Soc. B 275, 369–376 (2008). This paper presents data typical of the high-quality morphological techniques now being used to address arthropod phylogeny.

    PubMed  Google Scholar 

  33. Harzsch, S. & Hafner, G. Evolution of eye development in arthropods: phylogenetic aspects. Arthropod Struct. Dev. 35, 319–340 (2006).

    PubMed  Google Scholar 

  34. Fanenbruck, M. & Harzsch, S. A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia, Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager, 1987 (Remipedia, Speleonectidae): implications for arthropod relationships. Arthropod Struct. Dev. 34, 343–378 (2005).

    Google Scholar 

  35. Sanders, H. L. The Cephalocarida and crustacean phylogeny. Syst. Zool. 6, 112–128 (1957).

    Google Scholar 

  36. Cook, C. E., Yue, Q. Y. & Akam, M. Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Proc. R. Soc. B 272, 1295–1304 (2005).

    CAS  PubMed Central  PubMed  Google Scholar 

  37. Carapelli, A., Liò, P., Nardi, F., van der Wath, E. & Frati, F. Phylogenetic analysis of mitochondrial protein coding genes confirms the reciprocal paraphyly of Hexapoda and Crustacea. BMC Evol. Biol. 7 (suppl. 2), S8 (2007).

    PubMed Central  PubMed  Google Scholar 

  38. Siveter, D. J., Williams, M. & Waloszek, D. A phosphatocopid crustacean with appendages from the Lower Cambrian. Science 293, 479–481 (2001).

    CAS  PubMed  Google Scholar 

  39. Zhang, X. G., Siveter, D. J., Waloszek, D. & Maas, A. An epipodite-bearing crown-group crustacean from the Lower Cambrian. Nature 449, 595–598 (2007).

    CAS  ADS  PubMed  Google Scholar 

  40. Siveter, D. J., Sutton, M. D., Briggs, D. E. G. & Siveter, D. J. A new probable stem lineage crustacean with three-dimensionally preserved soft parts from the Herefordshire (Silurian) Lagerstatte, UK. Proc. R. Soc. B 274, 2099–2107 (2007). This paper provides valuable new data on a crustacean-like taxon considerably younger than the Cambrian faunas.

    PubMed Central  PubMed  Google Scholar 

  41. Wilson, H. M. Juliformian millipedes from the Lower Devonian of Euramerica: implications for the timing of millipede cladogenesis in the Paleozoic. J. Paleontol. 80, 638–649 (2006).

    Google Scholar 

  42. Fayers, S. R. & Trewin, N. H. A hexapod from the Early Devonian Windyfield chert, Rhynie, Scotland. Palaeontology 48, 1117–1130 (2005).

    Google Scholar 

  43. Boxshall, G. A. Crustacean classification: on-going controversies and unresolved problems. Zootaxa 1668, 313–325 (2007).

    Google Scholar 

  44. Friedrich, M. & Tautz, D. Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods. Nature 376, 165–167 (1995).

    CAS  ADS  PubMed  Google Scholar 

  45. Pisani, D., Poling, L., Lyons-Weiler, M. & Hedges, S. The colonization of land by animals: molecular phylogeny and divergence times among arthropods. BMC Biol. 2, 1 (2004).

    PubMed Central  PubMed  Google Scholar 

  46. Edgecombe, G. D. Morphological data, extant Myriapoda, and the myriapod stem-group. Contrib. Zool. 73, 207–252 (2004).

    Google Scholar 

  47. Rota-Stabelli, O. & Telford, M. J. A multi criterion approach for the selection of optimal outgroups in phylogeny: recovering some support for Mandibulata over Myriochelata using mitogenomics. Mol. Phylogenet. Evol. 48, 103–111 (2008).

    CAS  PubMed  Google Scholar 

  48. Dunlop, J. A. New ideas about the euchelicerate stem-lineage. Acta Zool. Bulg. (Suppl. 1) 9–23 (2005).

  49. Budd, G. E. The Cambrian fossil record and the origin of the phyla. Integr. Comp. Biol. 43, 157–165 (2003).

    PubMed  Google Scholar 

  50. Gehling, J. G. The case for Ediacaran fossil roots to the metazoan tree. Mem. Geol. Soc. India 20, 181–223 (1991).

    Google Scholar 

  51. Waggoner, B. M. Phylogenetic hypotheses of the relationships of arthropods to Precambrian and Cambrian problematic fossil taxa. Syst. Biol. 45, 190–222 (1996).

    Google Scholar 

  52. Ivantsov, A. Y. Vendia and other Precambrian 'arthropods'. Paleontol. J. 35, 335–343 (2001).

    Google Scholar 

  53. Jensen, S. The Proterozoic and earliest Cambrian trace fossil record; patterns, problems and perspectives. Integr. Comp. Biol. 43, 219–228 (2003).

    PubMed  Google Scholar 

  54. Hou, X.-G., Aldridge, R. J., Bergström, J., Siveter, D. J. & Feng, X.-H. The Cambrian Fossils of Chengjiang, China (Blackwell Science, 2004).

    Google Scholar 

  55. Conway Morris, S., Peel, J. S., Higgins, A. K., Soper, N. J. & Davis, N. C. A Burgess Shale-like fauna from the Lower Cambrian of North Greenland. Nature 326, 181–183 (1987).

    ADS  Google Scholar 

  56. Briggs, D. E. G. & Collins, D. The arthropod Alalcomenaeus cambricus Simonetta, from the Middle Cambrian Burgess Shale of British Columbia. Palaeontology 42, 953–977 (1999).

    Google Scholar 

  57. Whittington, H. B. The lobopod animal Aysheaia pedunculata Walcott, Middle Cambrian, Burgess Shale, British Columbia. Phil. Trans. R. Soc. Lond. B 284, 165–197 (1978).

    ADS  Google Scholar 

  58. Budd, G. A Cambrian gilled lobopod from Greenland. Nature 364, 709–711 (1993).

    ADS  Google Scholar 

  59. Budd, G. E. Arthropod body-plan evolution in the Cambrian with an example from anomalocaridid muscle. Lethaia 31, 197–210 (1998).

    Google Scholar 

  60. Liu, J. N., Shu, D. G., Han, J., Zhang, Z. F. & Zhang, X. L. Morpho-anatomy of the lobopod Magadictyon cf. haikouensis from the Early Cambrian Chengjiang Lagerstatte, South China. Acta Zool. 88, 279–288 (2007).

    Google Scholar 

  61. Bergstrom, J. Opabinia and Anomalocaris, unique Cambrian arthropods. Lethaia 19, 241–246 (1986).

    Google Scholar 

  62. Budd, G. E. The morphology of Opabinia regalis and the reconstruction of the arthropod stem-group. Lethaia 29, 1–14 (1996).

    Google Scholar 

  63. Hou, X.-G. & Bergström, J. Fossils and Strata Vol. 45 (Wiley, 1997).

    Google Scholar 

  64. Størmer, L. On the relationship and phylogeny of fossil and recent Arachnomorpha. A comparative study in Arachnida, Xiphosura, Eurypterida, Trilobita and other fossil Arthropoda. Skr. Norske Vidensk-Akad. 5, 1–158 (1944).

    Google Scholar 

  65. Chen, J. Y., Waloszek, D. & Maas, A. A new 'great-appendage' arthropod from the Lower Cambrian of China and homology of chelicerate chelicerae and raptorial antero-ventral appendages. Lethaia 37, 3–20 (2004).

    Google Scholar 

  66. Budd, G. E. A palaeontological solution to the arthropod head problem. Nature 417, 271–275 (2002).

    CAS  ADS  PubMed  Google Scholar 

  67. Chen, J. Y., Edgecombe, G. D., Ramskold, L. & Zhou, G. Q. Head segmentation in Early Cambrian Fuxianhuia — implications for arthropod evolution. Science 268, 1339–1343 (1995).

    CAS  ADS  PubMed  Google Scholar 

  68. Waloszek, D., Chen, J. Y., Maas, A. & Wang, X. Q. Early Cambrian arthropods — new insights into arthropod head and structural evolution. Arthropod Struct. Dev. 34, 189–205 (2005).

    Google Scholar 

  69. Budd, G. E. Head structure in upper stem-group euarthropods. Palaeontology 51, 561–573 (2008).

    Google Scholar 

  70. Scholtz, G. & Edgecombe, G. D. The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Dev. Genes Evol. 216, 395–415 (2006).

    PubMed  Google Scholar 

  71. Cotton, T. J. & Braddy, S. J. The phylogeny of arachnomorph arthropods and the origin of the Chelicerata. Trans. R. Soc. Edinb. 94, 169–193 (2004).

    Google Scholar 

  72. Eriksson, B. J., Tait, N. N. & Budd, G. E. Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system. J. Morphol. 255, 1–23 (2003).

    PubMed  Google Scholar 

  73. Walossek, D. & Muller, K. J. Upper Cambrian stem-lineage crustaceans and their bearing upon the monophyletic origin of Crustacea and the position of Agnostus . Lethaia 23, 409–427 (1990).

    Google Scholar 

  74. Telford, M. J. & Thomas, R. H. Demise of the Atelocerata? Nature 376, 123–124 (1995).

    CAS  ADS  Google Scholar 

  75. Damen, W. G. M., Saridaki, T. & Averof, M. Diverse adaptations of an ancestral gill: a common evolutionary origin for wings, breathing organs, and spinnerets. Curr. Biol. 12, 1711–1716 (2002). The fascinating gene-expression data in this paper support the likely homology of insect wings and tracheae with crustacean gills.

    CAS  PubMed  Google Scholar 

  76. Philippe, H. & Telford, M. J. Large-scale sequencing and the new animal phylogeny. Trends Ecol. Evol. 21, 614–620 (2006).

    PubMed  Google Scholar 

  77. Thomas, R. H. & Telford, M. J. Appendage development in embryos of the oribatid mite Archegozetes longisetosus (Acari, Oribatei, Trhypochthoniidae). Acta Zool. 80, 193–200 (1999).

    Google Scholar 

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Acknowledgements

We thank A. Daley for assistance with photography and R. Copley for critically reading an earlier draft. Our research is supported by the Marie Curie Research Training Network ZOONET (grant number MRTN-CT-2004-005624).

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Authors and Affiliations

  1. Department of Earth Sciences, Uppsala University, Villavägen 16, Uppsala, SE-752 36, Sweden

    Graham E. Budd

  2. Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK

    Maximilian J. Telford

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Budd, G., Telford, M. The origin and evolution of arthropods. Nature 457, 812–817 (2009). https://doi.org/10.1038/nature07890

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