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

Nature volume 463, pages 1079–1083 (2010)Cite this article

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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.

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

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Data deposits

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

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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 the Supplementary 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.

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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

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Correspondence to Clifford 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)

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Regier, J., Shultz, J., Zwick, A. et al. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079–1083 (2010). https://doi.org/10.1038/nature08742

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