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Arthropod Phylogeny Based on Eight Molecular Loci and Morphology

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Arthropod Phylogeny Based on Eight Molecular Loci and Morphology letters to nature melanogaster (U37541), mosquito Anopheles quadrimaculatus (L04272), mosquito arthropods revealed by the expression pattern of Hox genes in a spider. Proc. Natl Acad. Sci. USA 95, Anopheles gambiae (L20934), med¯y Ceratitis capitata (CCA242872), Cochliomyia homi- 10665±10670 (1998). nivorax (AF260826), locust Locusta migratoria (X80245), honey bee Apis mellifera 24. Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTALW: Improving the sensitivity of progressive (L06178), brine shrimp Artemia franciscana (X69067), water ¯ea Daphnia pulex multiple sequence alignment through sequence weighting, position-speci®c gap penalties and weight (AF117817), shrimp Penaeus monodon (AF217843), hermit crab Pagurus longicarpus matrix choice. Nucleic Acids Res. 22, 4673±4680 (1994). (AF150756), horseshoe crab Limulus polyphemus (AF216203), tick Ixodes hexagonus 25. Foster, P. G. & Hickey, D. A. Compositional bias may affect both DNA-based and protein-based (AF081828), tick Rhipicephalus sanguineus (AF081829). For outgroup comparison, phylogenetic reconstructions. J. Mol. Evol. 48, 284±290 (1999). sequences were retrieved for the annelid Lumbricus terrestris (U24570), the mollusc 26. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic Katharina tunicata (U09810), the nematodes Caenorhabditis elegans (X54252), Ascaris analysis. Mol. Biol. Evol. 17, 540±552 (2000). suum (X54253), Trichinella spiralis (AF293969) and Onchocerca volvulus (AF015193), and 27. Muse, S. V. & Kosakovsky Pond, S. L. Hy-Phy 0.7 b (North Carolina State Univ., Raleigh, 2000). the vertebrate species Homo sapiens (J01415) and Xenopus laevis (M10217). Additional 28. Strimmer, K. & von Haeseler, A. Quartet puzzlingÐa quartet maximum-likelihood method for sequences were analysed for gene arrangements: Boophilus microplus (AF110613), Euhadra reconstructing tree topologies. Mol. Biol. Evol. 13, 964±969 (1996). herklotsi (Z71696), Cepaea nemoralis (U23045) and Pupa strigosa (NC_002176). 29. Adachi, J. & Hasegawa, M. Model of amino acid substitution in proteins encoded by mitochondrial DNA. J. Mol. Evol. 42, 459±468 (1996). Multiple alignments were prepared for all putative protein sequences using Clustal W24 30. Felsenstein, J. PHYLIP (Phylogeny Inference Package). (Univ. Washington, Seattle, 1995). at default settings. Consistent with previous studies25, preliminary analyses revealed obvious tree estimation artefacts due to extremely accelerated substitution rates or protein Supplementary information is available from Nature's World-Wide Website composition bias in the nematode species, the honeybee Apis mellifera and the tick species (http://www.nature.com) or as paper copy from the London editorial of®ce of Nature. Rhipicephalus sanguineus and Ixodes hexagonus. With the exception of Ixodes hexagonus all of these taxa were therefore excluded from further analyses, reducing the total number of Acknowledgements species considered to 18. Sequence alignment was repeated and inspected by eye for suf®cient levels of sequence conservation, which resulted in the exclusion of the ATPase 8 We thank N. Muqim for technical assistance and A. Minelli and T. Burmester for gene (see Supplementary Information for single protein alignments). We used Gblocks26 comments on the manuscript. Most computation was performed on the Biological to extract regions of de®ned sequence conservation from the gene speci®c alignments and Software Server of the Institute Pasteur Paris. This study was in part supported by a DFG generate a single ®le of concatenated conserved regions. Default settings yielded the grant to D.T. and a Brain Korea 21 Project grant to W.K. U.W.H. was supported by 18P2560 alignment. Modi®ed parameter settings for generating the 18P1528 alignment fellowships from Deutscher Akademischer Austauschdienst, Korea Science and were: minimum number of sequences for a conserved position: 15; maximum number of Engineering Foundation, and the Brain Korea 21 Project (Medical Sciences, Yonsei contiguous nonconserved positions: 2; minimum length of a block after gap cleaning: University). 5. Alignments can be retrieved from the EBI webserver (ftp://ftp.ebi.ac.uk/pub/databases/ Correspondence and requests for materials should be addressed to U.W.H. embl/align) under accession numbers ALIGN_000111 and ALIGN_000112. Maximum- (e-mail: [email protected]) or M.F. (e-mail: [email protected]). likelihood mapping was carried out as described in ref. 16. Pairwise relative rate tests were carried out with the Hy-Phy program package27. Protein composition homogeneity test and maximum likelihood tree estimation was carried out using the TREE-PUZZLE program28 applying the mtREV24 sequence evolution model for mitochondrial proteins29 and a four rate approximated gamma distribution of among-site rate heterogeneity. Maximum-likelihood trees were determined by likelihood ratio tests between competing ................................................................. topologies. Maximum-parsimony tree reconstruction and neighbour-joining analysis with Dayhoff PAM matrix distances were performed using the respective algorithms Arthropod phylogeny based on eight implemented in Phylip 3.5 (ref. 30). Non-parametric bootstrapping analyses were based on 100 replicate data sets. molecular loci and morphology Received 22 February; accepted 13 July 2001. 1. Akam, M. Arthropods: developmental diversity within a (super) phylum. Proc. Natl Acad. Sci. USA Gonzalo Giribet*, Gregory D. Edgecombe² & Ward C. Wheeler³ 97, 4438±4441 (2000). 2. Boore, J. L., Labrov, D. V. & Brown, W. M. Gene translocation links insects and crustaceans. Nature * Department of Organismic and Evolutionary Biology, Harvard University, 392, 667±668 (1998). 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA 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). ² Australian Museum, 6 College Street, Sydney, New South Wales 2010, Australia 4. Friedrich, M. & Tautz, D. Ribosomal DNA phylogeny of the major extant arthropod classes and the ³ Division of Invertebrate Zoology, American Museum of Natural History, evolution of myriapods. Nature 376, 165±167 (1995). Central Park West at 79th Street, New York, New York 10024, USA 5. Snodgrass, R. E. Evolution of Annelida, Onychophora and Arthropoda. Smithson. Misc. Coll. 138, 1± 77 (1938). .............................................................................................................................................. 6. Cisne, J. L. Trilobites and the evolution of arthropods. Science 186, 13±18 (1974). The interrelationships of major clades within the Arthropoda 7. Giribet, G. & Ribera, C. A review of arthropod phylogeny: new data based on ribosomal DNA remain one of the most contentious issues in systematics, which sequences and direct character optimization. Cladistics 16, 204±231 (2000). 1,2 8. Boore, J. L., Collins, T. M., Stanton, D., Daehler, L. L. & Brown, W. M. Deducing the pattern of has traditionally been the domain of morphologists . A growing arthropod phylogeny from mitochondrial DNA rearrangements. Nature 376, 163±165 (1995). body of DNA sequences and other types of molecular data has 9. Curole, J. P. & Kocher, T. D. Mitogenomics: digging deeper with complete mitochondrial genomes. revitalized study of arthropod phylogeny3±7 and has inspired new Trends Ecol. Evol. 14, 394±203 (1999). considerations of character evolution8,9. Novel hypotheses such as 10. Boore, J. L. Animal mitochondrial genomes. Nucleic Acids Res. 27, 1767±1780 (1999). 4,10±12 11. Wilson, K., Cahill, V., Ballment, E. & Benzie, J. The complete sequence of the mitochondrial genome of a crustacean±hexapod af®nity were based on analyses of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to single or few genes and limited taxon sampling, but have received branchiopods? Mol. Biol. Evol. 17, 863±874 (2000). recent support from mitochondrial gene order13, and eye and 12. Garcia-Machado, E. et al. Mitochondrial genes collectively suggest the paraphyly of Crustacea with 14,15 respect to Insecta. J. Mol. Evol. 49, 142±149 (1999). brain ultrastructure and neurogenesis . Here we assess rela- 13. Aguinaldo, A. et al. Evidence for a clade of nematodes, arthropods and other molting animals. Nature tionships within Arthropoda based on a synthesis of all well 387, 489±493 (1997). sampled molecular loci together with a comprehensive data set 14. Sidow, A. & Thomas, W. K. A molecular evolutionary framework for eukaryotic model organisms. of morphological, developmental, ultrastructural and gene-order Curr. Biol. 4, 596±603 (1994). 15. Hausdorf, B. Early evolution of the Bilateria. Syst. Biol. 49, 130±142 (2000). characters. The molecular data include sequences of three nuclear 16. Strimmer, K. & von Haeseler, A. Likelihood-mapping: a simple method to visualize phylogenetic ribosomal genes, three nuclear protein-coding genes, and two content of a sequence alignment. Proc. Natl Acad. Sci. USA 94, 6815±6819 (1997). mitochondrial genes (one protein coding, one ribosomal). We 17. Peterson, K. J. & Eernisse, D. J. Animal phylogeny and the ancestry of bilaterians: inferences from 16,17 morphology and 18S rDNA sequences. Evol. Dev. 3, 170±205 (2001). devised new optimization procedures and constructed a parallel 18 18. Cook, C. E., Smith, M. L., Telford, M. J., Bastianello, A. & Akam,
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