Movatterモバイル変換

[0]ホーム
URL:

Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Advertisement

Nature
  • Letter
  • Published:

Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences

Naturevolume 463, pages1079–1083 (2010)Cite this article

Subjects

Abstract

The remarkable antiquity, diversity and ecological significance of arthropods have inspired numerous attempts to resolve their deep phylogenetic history, but the results of two decades of intensive molecular phylogenetics have been mixed1,2,3,4,5,6,7. The discovery that terrestrial insects (Hexapoda) are more closely related to aquatic Crustacea than to the terrestrial centipedes and millipedes2,8 (Myriapoda) was an early, if exceptional, success. More typically, analyses based on limited samples of taxa and genes have generated results that are inconsistent, weakly supported and highly sensitive to analytical conditions7,9,10. Here we present strongly supported results from likelihood, Bayesian and parsimony analyses of over 41 kilobases of aligned DNA sequence from 62 single-copy nuclear protein-coding genes from 75 arthropod species. These species represent every major arthropod lineage, plus five species of tardigrades and onychophorans as outgroups. Our results strongly support Pancrustacea (Hexapoda plus Crustacea) but also strongly favour the traditional morphology-based Mandibulata11 (Myriapoda plus Pancrustacea) over the molecule-based Paradoxopoda (Myriapoda plus Chelicerata)2,5,12. In addition to Hexapoda, Pancrustacea includes three major extant lineages of ‘crustaceans’, each spanning a significant range of morphological disparity. These are Oligostraca (ostracods, mystacocarids, branchiurans and pentastomids), Vericrustacea (malacostracans, thecostracans, copepods and branchiopods) and Xenocarida (cephalocarids and remipedes). Finally, within Pancrustacea we identify Xenocarida as the long-sought sister group to the Hexapoda, a result confirming that ‘crustaceans’ are not monophyletic. These results provide a statistically well-supported phylogenetic framework for the largest animal phylum and represent a step towards ending the often-heated, century-long debate on arthropod relationships.

This is a preview of subscription content,access via your institution

Access options

Access through your institution

Subscription info for Japanese customers

We have a dedicated website for our Japanese customers. Please go tonatureasia.com to subscribe to this journal.

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

￥ 4,980

Prices may be subject to local taxes which are calculated during checkout

Figure 1:Phylogenetic relationships of 75 arthropod and five outgroup species.
Figure 2:Phylogram of relationships for 75 arthropod and five outgroup species.

Similar content being viewed by others

Accession codes

Data deposits

All sequences generated for this publication have been deposited in GenBank under the accession numbers given inSupplementary Tables 4 and 5. Full data matrices are available inSupplementary Information.

References

  1. Abele, L. G., Kim, W. & Felgenhauer, B. E. Molecular evidence for inclusion of the phylum Pentastomida in the Crustacea.Mol. Biol. Evol.6, 685–691 (1989)

    Google Scholar 

  2. Friedrich, M. & Tautz, D. Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods.Nature376, 165–167 (1995)

    Article ADS CAS  Google Scholar 

  3. Regier, J. C. & Shultz, J. W. Molecular phylogeny of the major arthropod groups indicates polyphyly of crustaceans and a new hypothesis for the origin of hexapods.Mol. Biol. Evol.14, 902–913 (1997)

    Article CAS  Google Scholar 

  4. Giribet, G., Edgecombe, G. D. & Wheeler, W. C. Arthropod phylogeny based on eight molecular loci and morphology.Nature413, 157–161 (2001)

    Article ADS CAS  Google Scholar 

  5. Hwang, U. W., Friedrich, M., Tautz, D., Park, C. J. & Kim, W. Mitochondrial protein phylogeny joins myriapods with chelicerates.Nature413, 154–157 (2001)

    Article ADS CAS  Google Scholar 

  6. 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)

    Article CAS  Google Scholar 

  7. Budd, G. E. & Telford, M. J. The origin and evolution of arthropods.Nature457, 812–817 (2009)

    Article ADS CAS  Google Scholar 

  8. Boore, J. L., Lavrov, D. V. & Brown, W. M. Gene translocation links insects and crustaceans.Nature392, 667–668 (1998)

    Article ADS CAS  Google Scholar 

  9. Phillips, M. J., Delsuc, F. & Penny, D. Genome-scale phylogeny and the detection of systematic biases.Mol. Biol. Evol.21, 1455–1458 (2004)

    Article CAS  Google Scholar 

  10. 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)

    Article CAS  Google Scholar 

  11. Snodgrass, R. E.Evolution of the Annelida, Onychophora and Arthropoda (Smithsonian Inst. Press, 1938)

    Google Scholar 

  12. 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)

    Article CAS  Google Scholar 

  13. Dunn, C. W. et al. Broad phylogenomic sampling improves resolution of the animal tree of life.Nature452, 745–749 (2008)

    Article ADS CAS  Google Scholar 

  14. Timmermans, M. J. T. N., Roelofs, D., Mariën, J. & Van Straalen, N. M. Revealing pancrustacean relationships: phylogenetic analysis of ribosomal protein genes places Collembola (springtails) in a monophyletic Hexapoda and reinforces the discrepancy between mitochondrial and nuclear DNA markers.BMC Evol. Biol.8, 83 (2008)

    Article CAS  Google Scholar 

  15. Philippe, H. et al. Phylogenomics revives traditional views on deep animal relationships.Curr. Biol.19, 706–712 (2009)

    Article CAS  Google Scholar 

  16. Regier, J. C. et al. Resolving arthropod phylogeny: exploring phylogenetic signal within 41 kb of protein-coding nuclear gene sequence.Syst. Biol.57, 920–938 (2008)

    Article CAS  Google Scholar 

  17. Holder, M. T., Zwickl, D. J. & Dessimoz, C. Evaluating the robustness of phylogenetic methods to among-site variability in substitution processes.Phil. Trans. R. Soc. B363, 4013–4021 (2008)

    Article CAS  Google Scholar 

  18. Seo, T. & Kishino, H. Statistical comparison of nucleotide, amino acid, and codon substitution models for evolutionary analysis of protein-coding sequences.Syst. Biol.58, 199–210 (2009)

    Article CAS  Google Scholar 

  19. Podsiadlowski, L., Braband, A. & Mayer, G. The complete mitochondrial genome of the onychophoranEpiperipatus biolleyi reveals a unique transfer RNA set and provides further support for the Ecdysozoa hypothesis.Mol. Biol. Evol.25, 42–51 (2008)

    Article CAS  Google Scholar 

  20. Shultz, J. W. A phylogenetic analysis of the arachnid orders based on morphological characters.Zool. J. Linn. Soc.150, 221–265 (2007)

    Article  Google Scholar 

  21. Schram, F. R. ed.Crustacean Phylogeny (Balkema, 1983)

    Google Scholar 

  22. Fanenbruck, M., Harzsch, S. & Wagele, J. The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships.Proc. Natl Acad. Sci. USA101, 3868–3873 (2004)

    Article ADS CAS  Google Scholar 

  23. Harzsch, S. Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phyologeny.Integr. Comp. Biol.46, 162–194 (2006)

    Article  Google Scholar 

  24. Boxshall, G. A. Crustacean classification: on-going controversies and unresolved problems.Zootaxa1668, 313–325 (2007)

    Google Scholar 

  25. 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)

    Article  Google Scholar 

  26. Hennig, W.Insect Phylogeny (Wiley, 1981)

    Google Scholar 

  27. Zrzavy, J., Hypsa, V. & Vlaskova, M. inArthropod Relationships (eds Fortey, R. A. & Thomas, R. H.) 97–107 (Chapman and Hall, 1997)

    Google Scholar 

  28. Gai, Y.-H., Song, D., Sun, H. & Zhou, K. Myriapod monophyly and relationships among myriapod classes based on nearly complete 28S and 18S rDNA sequences.Zool. Sci.23, 1101–1108 (2006)

    Article CAS  Google Scholar 

  29. Zwickl, D. J.Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological Sequence Datasets under the Maximum Likelihood Criterion. PhD thesis, Univ. Texas Austin (2006)

    Google Scholar 

  30. Goldman, N., Thorne, J. L. & Jones, D. T. Using evolutionary trees in protein secondary structure prediction and other comparative sequence analyses.J. Mol. Biol.263, 196–208 (1996)

    Article CAS  Google Scholar 

  31. Remm, M., Storm, C. E. & Sonnhammer, E. L. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons.J. Mol. Biol.314, 1041–1052 (2001)

    Article CAS  Google Scholar 

  32. Regier, J. C. & Shi, D. Increased yield of PCR product from degenerate primers with nondegenerate, nonhomologous 5′ tails.Biotechniques38, 34–38 (2005)

    Article CAS  Google Scholar 

  33. Staden, R., Judge, D. & Bonfield, J. Sequence assembly and finishing methods.Methods Biochem. Anal.43, 303–322 (2001)

    CAS PubMed  Google Scholar 

  34. Smith, S. W., Overbeck, R., Woese, C. R., Gilbert, W. & Gillevet, P. M. The genetic data environment and expandable GUI for multiple sequence analysis.Comp. Appl. Biosci.10, 671–675 (1994)

    CAS PubMed  Google Scholar 

  35. Katoh, K., Kuma, K., Toh, H. & Miyata, T. MAFFT version 5: improvement in accuracy of multiple sequence alignment.Nucleic Acids Res.33, 511–518 (2005)

    Article CAS  Google Scholar 

  36. PAUP*. v.4.0 (Sinauer Associates, Sunderland, Massachusetts, 2002)

  37. Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogeny.Bioinformatics17, 754–755 (2001)

    Article CAS  Google Scholar 

  38. Ronquist, F. & Huelsenbeck, J. P. MRBAYES 3: Bayesian phylogenetic inference under mixed models.Bioinformatics19, 1572–1574 (2003)

    Article CAS  Google Scholar 

  39. Altekar, G., Dwarkadas, S., Huelsenbeck, J. P. & Ronquist, F. Parallel Metropolis-coupled Markov chain Monte Carlo for Bayesian phylogenetic inference.Bioinformatics20, 407–415 (2004)

    Article CAS  Google Scholar 

  40. MRMODELTEST. v.2 (Evolutionary Biology Centre, Uppsala University, 2004)

  41. Regier, J. C. & Shultz, J. W. Elongation factor-2: a useful gene for arthropod phylogenetics.Mol. Phylogenet. Evol.20, 136–148 (2001)

    Article CAS  Google Scholar 

  42. Cummings, M. & Huskamp, J. Grid computing.EDUCAUSE Rev.40, 116–117 (2005)

    Google Scholar 

  43. Bazinet, A. L. & Cummings, M. C. inDistributed & Grid Computing–Science Made Transparent for Everyone. Principles, Applications and Supporting Communities (ed. Weber, M. H. W.) 2–13 (Tectum, 2009)

    Google Scholar 

Download references

Acknowledgements

C.W.C. thanks W. Hartman for early insight into questions of arthropod phylogeny and D. Percy for sequencing. J.W.M. and R.W. thank N. Tait, G. Hampson and R. Hessler for help collecting samples. J.C.R. and A.Z. thank M. Cummings and A. Bazinet for making available grid computing, and the DNA Sequencing Facility at the Center for Biosystems Research, University of Maryland Biotechnology Institute. J.W.S. was supported by the Maryland Agricultural Experiment Station. C.W.C. was supported by the Whiteley Center. This work was funded by two programmes at the US National Science Foundation, namely Biocomplexity in the Environment: Genome-Enabled Environmental Science and Engineering, and Assembling the Tree of Life.

Author Contributions C.W.C., J.C.R., J.W.S., A.Z. and J.W.M. designed the project. J.W.S., J.W.M., R.W. and J.C.R. designed and carried out taxon sampling and collection. J.C.R. and C.W.C. supervised DNA sequencing and editing, with PCR templates generated by J.C.R., B.B. and others. J.C.R., A.Z., C.W.C. and J.W.S. decided on the strategy for data analysis and its implementation, with the degen1 coding method developed and implemented by J.C.R., A.H. and A.Z. J.C.R. and A.Z. assembled theSupplementary Information and submitted sequences to GenBank. J.W.S. and J.W.M. proposed the names for the new, strongly supported clades in the Pancrustacea. C.W.C. wrote the first draft of the manuscript, with major additions by J.C.R. and J.W.S. and additional contributions by J.W.M. and A.Z. All authors commented on the manuscript.

Author information

Authors and Affiliations

  1. Center for Biosystems Research, University of Maryland Biotechnology Institute,,

    Jerome C. Regier, Jeffrey W. Shultz, Andreas Zwick & April Hussey

  2. Department of Entomology,,

    Jeffrey W. Shultz

  3. Institute for Bioscience and Biotechnology Research, University of Maryland, College Park, Maryland 20742, USA ,

    Jeffrey W. Shultz

  4. Department of Biology, Duke University, Durham, North Carolina 27708, USA,

    Bernard Ball & Clifford W. Cunningham

  5. Natural History Museum of Los Angeles County, Los Angeles, California 90007, USA ,

    Regina Wetzer & Joel W. Martin

Authors
  1. Jerome C. Regier
  2. Jeffrey W. Shultz
  3. Andreas Zwick
  4. April Hussey
  5. Bernard Ball
  6. Regina Wetzer
  7. Joel W. Martin
  8. Clifford W. Cunningham

Corresponding author

Correspondence toClifford W. Cunningham.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-7 with Legends and Supplementary Tables 1-5. (PDF 918 kb)

Supplementary Data

This file contains the nucleotide data matrix, 80 taxa. (TXT 4150 kb)

Supplementary Data

This file contains the degen1 data matrix, 80 taxa. (TXT 4072 kb)

Supplementary Data

This file contains the amino acid data matrix, 85 taxa. (TXT 1087 kb)

Supplementary Data

This file contains the perl script to generate degen1 data matrices. (TXT 9 kb)

Supplementary Information

This file contains explanation of the Degen1_v1_2.pl script. (PDF 29 kb)

Rights and permissions

About this article

Cite this article

Regier, J., Shultz, J., Zwick, A.et al. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences.Nature463, 1079–1083 (2010). https://doi.org/10.1038/nature08742

Download citation

This article is cited by

Access through your institution
Buy or subscribe

Editorial Summary

The complex world of arthropods

The evolutionary interrelationship of arthropods (jointed-legged animals) has long been a matter of dispute. A new phylogeny based on an analysis of over 41,000 base pairs of DNA from 75 species, including representatives of every major arthropod lineage, should ease the way towards a consensus on the matter. The data support the idea that insects are land-living crustaceans, that crustaceans comprise a diverse assemblage of at last three distinct arthropod types, and that myriapods (millipedes and centipedes) are the closest relatives of this great 'pancrustacean' group.

Advertisement

Search

Advanced search

Quick links

Nature Briefing

Sign up for theNature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox.Sign up for Nature Briefing
[8]ページ先頭
©2009-2025 Movatter.jp