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Mitochondrial protein phylogeny joins myriapods with chelicerates

Abstract

The animal phylum Arthropoda is very useful for the study of body plan evolution given its abundance of morphologically diverse species and our profound understanding of Drosophila development1. However, there is a lack of consistently resolved phylogenetic relationships between the four extant arthropod subphyla, Hexapoda, Myriapoda, Chelicerata and Crustacea. Recent molecular studies2,3,4 have strongly supported a sister group relationship between Hexapoda and Crustacea, but have not resolved the phylogenetic position of Chelicerata and Myriapoda. Here we sequence the mitochondrial genome of the centipede species Lithobius forficatus and investigate its phylogenetic information content. Molecular phylogenetic analysis of conserved regions from the arthropod mitochondrial proteome yields highly resolved and congruent trees. We also find that a sister group relationship between Myriapoda and Chelicerata is strongly supported. We propose a model to explain the apparently parallel evolution of similar head morphologies in insects and myriapods.

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Figure 1: Phylogenetic distribution of tRNACys arrangements in arthropod mitochondrial genomes.
Figure 2: Visualization of phylogenetic information content by maximum likelihood mapping.
Figure 3: Phylogram of best maximum-likelihood tree with 18P2560 alignment (ln(likelihood) = -42925.32 ).

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References

  1. Akam, M. Arthropods: developmental diversity within a (super) phylum. Proc. Natl Acad. Sci. USA 97, 4438–4441 (2000).

    Article  ADS  CAS  Google Scholar 

  2. Boore, J. L., Labrov, D. V. & Brown, W. M. Gene translocation links insects and crustaceans. Nature 392, 667–668 (1998).

    Article  ADS  CAS  Google Scholar 

  3. Shultz, J. W. & Regier, J. C. Phylogenetic analysis of arthropods using two nuclear protein-encoding genes supports a crustacean + hexapod clade. Proc. R. Soc. Lond. B 267, 1011–1019 (2000).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  5. Snodgrass, R. E. Evolution of Annelida, Onychophora and Arthropoda. Smithson. Misc. Coll. 138, 1–77 (1938).

    Google Scholar 

  6. Cisne, J. L. Trilobites and the evolution of arthropods. Science 186, 13–18 (1974).

    Article  ADS  CAS  Google Scholar 

  7. Giribet, G. & Ribera, C. A review of arthropod phylogeny: new data based on ribosomal DNA sequences and direct character optimization. Cladistics 16, 204–231 (2000).

    Article  Google Scholar 

  8. Boore, J. L., Collins, T. M., Stanton, D., Daehler, L. L. & Brown, W. M. Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature 376, 163–165 (1995).

    Article  ADS  CAS  Google Scholar 

  9. Curole, J. P. & Kocher, T. D. Mitogenomics: digging deeper with complete mitochondrial genomes. Trends Ecol. Evol. 14, 394–203 (1999).

    Article  CAS  Google Scholar 

  10. Boore, J. L. Animal mitochondrial genomes. Nucleic Acids Res. 27, 1767–1780 (1999).

    Article  CAS  Google Scholar 

  11. Wilson, K., Cahill, V., Ballment, E. & Benzie, J. The complete sequence of the mitochondrial genome of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to branchiopods? Mol. Biol. Evol. 17, 863–874 (2000).

    Article  CAS  Google Scholar 

  12. Garcia-Machado, E. et al. Mitochondrial genes collectively suggest the paraphyly of Crustacea with respect to Insecta. J. Mol. Evol. 49, 142–149 (1999).

    Article  ADS  CAS  Google Scholar 

  13. Aguinaldo, A. et al. Evidence for a clade of nematodes, arthropods and other molting animals. Nature 387, 489–493 (1997).

    Article  CAS  Google Scholar 

  14. Sidow, A. & Thomas, W. K. A molecular evolutionary framework for eukaryotic model organisms. Curr. Biol. 4, 596–603 (1994).

    Article  CAS  Google Scholar 

  15. Hausdorf, B. Early evolution of the Bilateria. Syst. Biol. 49, 130–142 (2000).

    Article  CAS  Google Scholar 

  16. Strimmer, K. & von Haeseler, A. Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc. Natl Acad. Sci. USA 94, 6815–6819 (1997).

    Article  ADS  CAS  Google Scholar 

  17. Peterson, K. J. & Eernisse, D. J. Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA sequences. Evol. Dev. 3, 170–205 (2001).

    Article  CAS  Google Scholar 

  18. Cook, C. E., Smith, M. L., Telford, M. J., Bastianello, A. & Akam, M. Hox genes and the phylogeny of the arthropods. Curr. Biol. 11, 759–763 (2001).

    Article  CAS  Google Scholar 

  19. Kusche, K. & Burmester, T. Diplopod hemocyanin sequence and the evolution of the Myriapoda. Mol. Biol. Evol. 18, 1566–1573 (2001).

    Article  CAS  Google Scholar 

  20. Casares, F. & Mann, R. S. Control of antennal versus leg development in Drosophila. Nature 392, 723–726 (1998).

    Article  ADS  CAS  Google Scholar 

  21. Delle Cave, L. & Simonetta, A. M. in The Early Evolution of Metazoa and the Significance of Problematic Taxa (eds Simonetta, A. M. & Conway Morris, S.) 189–244 (Cambridge Univ. Press, Cambridge, 1991).

    Google Scholar 

  22. Telford, M. J. & Thomas, R. H. Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc. Natl Acad. Sci. USA 95, 10671–10675 (1998).

    Article  ADS  CAS  Google Scholar 

  23. Damen, W. G., Hausdorf, M., Seyfarth, E. A. & Tautz, D. A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc. Natl Acad. Sci. USA 95, 10665–10670 (1998).

    Article  ADS  CAS  Google Scholar 

  24. Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).

    Article  CAS  Google Scholar 

  25. Foster, P. G. & Hickey, D. A. Compositional bias may affect both DNA-based and protein-based phylogenetic reconstructions. J. Mol. Evol. 48, 284–290 (1999).

    Article  ADS  CAS  Google Scholar 

  26. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000).

    Article  CAS  Google Scholar 

  27. Muse, S. V. & Kosakovsky Pond, S. L. Hy-Phy 0.7 β (North Carolina State Univ., Raleigh, 2000).

    Google Scholar 

  28. Strimmer, K. & von Haeseler, A. Quartet puzzling—a quartet maximum-likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13, 964–969 (1996).

    Article  CAS  Google Scholar 

  29. Adachi, J. & Hasegawa, M. Model of amino acid substitution in proteins encoded by mitochondrial DNA. J. Mol. Evol. 42, 459–468 (1996).

    Article  ADS  CAS  Google Scholar 

  30. Felsenstein, J. PHYLIP (Phylogeny Inference Package). (Univ. Washington, Seattle, 1995).

Download references

Acknowledgements

We thank N. Muqim for technical assistance and A. Minelli and T. Burmester for comments on the manuscript. Most computation was performed on the Biological Software Server of the Institute Pasteur Paris. This study was in part supported by a DFG grant to D.T. and a Brain Korea 21 Project grant to W.K. U.W.H. was supported by fellowships from Deutscher Akademischer Austauschdienst, Korea Science and Engineering Foundation, and the Brain Korea 21 Project (Medical Sciences, Yonsei University).

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Correspondence to Ui Wook Hwang or Markus Friedrich.

Supplementary information

Supplement Figure 1

(GIF 12.6 KB)

Consistent support for a chelicerate/myriapod sister clade when nematode taxa are included. Single protein alignments (23PND1.PHYLIP, 23PND2_PHYLIP, 23PND3.PHYLIP, 23PND4.PHYLIP, 23PND4l.PHYLIP, 23PND5.PHYLIP, 23PND6.PHYLIP, 23PCOI-1.PHYLIP, 23PCOII-1.PHYLIP, 23PCOIII-1.PHYLIP, 23PCytB.PHYLIP and 23Patpase6-1.PHYLIP) were generated for same set of species included in the original analysis plus the four nematode species and deposited with supplementary materials. Mitochondrial protein quartet puzzling trees shown as unrooted phylograms of were estimated with a 2055 site long alignment (23P2055, EBI WWW server accession number ALIGN_000113) produced with the Gblocks program at default settings as described in Material and Methods. Bars represent 0.1 substitutions per site. a, Taxon choice as with 18P2560 and 18P1528. Myriapod/chelicerate clade supported with BP = 95. b, Taxon choice same as in a with four nematode taxa added (Caenorhabditis, Ascaris, Onchocerca, Trichinella) and the fast evolving chelicerate Ixodes removed. All four nematode taxa form extremely long branches consistent with accelerated substitution rates indicated in distance matrix (Supplement Table 1). Myriapod/chelicerate clade supported with BP = 98. c, Taxon choice same as in b with fast evolving chelicerate taxa added (Rhipicephalus, Ixodes). The latter are drawn away from the chelicerate Limulus most likely due to long branch attraction. Myriapod (Lithobius) /chelicerate (Limulus) clade supported with BP = 88.

Single protein alignments (ZIP 37.3 KB)

Supplement Table 1 Maximum likelihood distance matrix for alignment 23P2055 used to estimate trees in Supplement Figure 1. Nematode taxa (Caenorhabditis, Ascaris, Onchocerca, Trichinella) exhibit at least three times higher sequence divergence than most other taxa included.

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Hwang, U., Friedrich, M., Tautz, D. et al. Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413, 154–157 (2001). https://doi.org/10.1038/35093090

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