Molecular Biology

, Volume 43, Issue 5, pp 804–818 | Cite as

On the phylogenetic position of insects in the Pancrustacea clade

  • V. V. Aleshin
  • K. V. Mikhailov
  • A. V. Konstantinova
  • M. A. Nikitin
  • L. Yu. Rusin
  • D. A. Buinova
  • O. S. Kedrova
  • N. B. Petrov


The current views on the phylogeny of arthropods are at odds with the traditional system, which recognizes four independent arthropod classes: Chelicerata, Crustacea, Myriapoda, and Insecta. There is compelling evidence that insects comprise a monophyletic lineage with Crustacea within a larger clade named Pancrustacea, or Tetraconata. However, which crustacean group is the closest living relative of insects is still an open question. In recent phylogenetic trees constructed on the basis of large gene sequence data insects are placed together with primitive crustaceans, the Branchiopoda. This topology is often suspected to be a result of the long branch attraction artifact. We analyzed concatenated data on 77 ribosomal proteins, elongation factor 1A (EF1A), initiation factor 5A (eIF5A), and several other nuclear and mitochondrial proteins. Analyses of nuclear genes confirm the monophyly of Hexapoda, the clade uniting entognath and ectognath insects. The hypothesis of the monophyly of Hexapoda and Branchiopoda is supported in the majority of analyses. The Maxillopoda, another clade of Entomostraca, occupies a sister position to the Hexapoda + Branchiopoda group. Higher crustaceans, the Malacostraca, in most analyses appear a more basal lineage within the Pancrustacea. We report molecular synapomorphies in low homoplastic regions, which support the clade Hexapoda + Branchiopoda + Maxillopoda and the monophyletic Malacostraca including Phyllocarida. Thus, the common origin of Hexapoda and Branchiopoda and their position within Entomostraca are suggested to represent bona fide phylogenetic relationships rather than computational artifacts.

Key words

phylogeny molecular evolution cladistics EF1A eIF5A RpS28e Arthropoda Crustacea Insecta 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Ruppert E.E., Fox R.S., Barnes R.D. 2004. Invertebrate Zoology: A Functional Evolutionary Approach, 7th ed. Vol. 3: Arthropods. Belmont, CA: Brooks/Cole-Thomson Learning.Google Scholar
  2. 2.
    Kluge N.Yu. 2000. Sovremennaya sistematika nasekomykh (Modern Insect Taxonomy). St. Petersburg: Lan’.Google Scholar
  3. 3.
    Dogel V.A. 1981. Zoologiya bespozvonochnykh (Invertebrate Zoology). Ed. Polyanskii Yu.I. Moscow: Vysshaya Shkola.Google Scholar
  4. 4.
    Turbeville J.M., Pfeifer D.M., Field K.G., Raff R.A. 1991. The phylogenetic status of arthropods, as inferred from 18S rRNA sequences. Mol. Biol. Evol. 8, 669–686.PubMedGoogle Scholar
  5. 5.
    Ballard J.W.O., Ballard O., Olsen G.J., Faith D.P., Odgers W.A., Rowell D.M., Atkinson P. 1992. Evidence from 12S ribosomal RNA sequences that onychophorans are modified arthropods. Science. 258, 1345–1348.PubMedCrossRefGoogle Scholar
  6. 6.
    Friedrich M., Tautz D. 1995. Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods. Nature. 376, 165–167.PubMedCrossRefGoogle Scholar
  7. 7.
    Averof M., Akam M. 1995. Insect-crustacean relationships: Insights from comparative developmental and molecular studies. Phil. Trans. R. Soc. London B. 256, 183–235.Google Scholar
  8. 8.
    Giribet G., Carranza S., Baguñà J., Riutort M., Ribera C. 1996. First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Mol. Biol. Evol. 13, 76–84.PubMedGoogle Scholar
  9. 9.
    Boore J.L., Lavrov D.V., Brown W.M. 1998. Gene translocation links insects and crustaceans. Nature. 392, 667–668.PubMedCrossRefGoogle Scholar
  10. 10.
    Aleshin V.V., Petrov N.B. 1999. Implicaciones del gen 18S ARNr en la evolución y filogenia de los Arthropoda. In: Evolución y Filogenia de Arthropoda. Boletin de la Sociedad Entomológica Aragonesa, no. 26. Eds. Melic A., de Haro J.J., Méndez M., Ribera I. Zaragoza: SEA, pp. 177–196.Google Scholar
  11. 11.
    Glenner H., Thomsen P.F., Hebsgaard M.B., Sorensen M.V., Willerslev E. 2006. The origin of insects. Science. 314, 1883–1884.PubMedCrossRefGoogle Scholar
  12. 12.
    Budd G.E., Telford M.J. 2009. The origin and evolution of arthropods. Nature. 457, 812–817.PubMedCrossRefGoogle Scholar
  13. 13.
    Regier J.C., Shultz J.W., Kambic R.E. 2005. Pancrustacean phylogeny: Hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc. R. Soc. London B. 272, 395–401.CrossRefGoogle Scholar
  14. 14.
    Giribet G., Richter S., Edgecombe G.D., Wheeler W.C. 2005. The position of crustaceans within Arthropoda: Evidence from nine molecular loci and morphology. Crustacean Issues. 16, 307–330.Google Scholar
  15. 15.
    Zrzav J., Štys P. 1997. The basic body plan of arthropods: Insights from evolutionary morphology and developmental biology. J. Evol. Biol. 10, 353–367.CrossRefGoogle Scholar
  16. 16.
    Dohle W. 2001. Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name Tetraconata for the monophyletic unit Crustacea + Hexapoda. Ann. Soc. Entomol. Fr. (N.S.). 37, 85–103.Google Scholar
  17. 17.
    Schram F.R., Jenner R.A. 2001. The origin of Hexapoda: A crustacean perspective. Ann. Soc. Entomol. Fr. (N.S.). 37, 243–264.Google Scholar
  18. 18.
    Pavlov V.Ya. 2000. Periodicheskaya sistema chlenistykh (The Periodic System of Atriculates). Moscow: VNIRO.Google Scholar
  19. 19.
    Duman-Scheel M., Patel N.H. 1999. Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development. 126, 2327–2334.PubMedGoogle Scholar
  20. 20.
    Richter S. 2002. The Tetraconata concept: Hexapod-crustacean relationships and the phylogeny of Crustacea. Org. Divers. Evol. 2, 217–237.CrossRefGoogle Scholar
  21. 21.
    Harzsch S., Hafner G. 2006. Evolution of eye development in arthropods: Phylogenetic aspects. Arthropod Struct. Dev. 35, 319–340.PubMedCrossRefGoogle Scholar
  22. 22.
    Regier J.C., Shultz J.W., Ganley A.R., Hussey A., Shi D., Ball B., Zwick A., Stajich J.E., Cummings M.P., Martin J.W., Cunningham C.W. 2008. Resolving arthropod phylogeny: Exploring phylogenetic signal within 41 kb of protein-coding nuclear gene sequence. Syst. Biol. 57, 920–938.PubMedCrossRefGoogle Scholar
  23. 23.
    Stollewerk A., Chipman A.D. 2006. Neurogenesis in myriapods and chelicerates and its importance for understanding arthropod relationships. Integr. Comp. Biol. 46, 195–206.CrossRefGoogle Scholar
  24. 24.
    Backer H., Fanenbruck M., Wagele J.W. 2008. A forgotten homology supporting the monophyly of Tracheata: The subcoxa of insects and myriapods re-visited. Zool. Anz. 247, 185–207.CrossRefGoogle Scholar
  25. 25.
    Zherikhin V.V., Ponomarenko A.G., Rasnitsyn A.P., 2008. Vvedenie v paleoentomologiyu (Introduction to Paleoentomology). Moscow: KMK.Google Scholar
  26. 26.
    Baurain D., Brinkmann H., Philippe H. 2007. Lack of resolution in the animal phylogeny: Closely spaced cladogeneses or undetected systematic errors? Mol. Biol. Evol. 24, 6–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Parkinson J., Whitton C., Schmid R., Thomson M., Blaxter M. 2004. NEMBASE: A resource for parasitic nematode ESTs. Nucleic Acids Res. 32, D427–D430.PubMedCrossRefGoogle Scholar
  28. 28.
    Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389–33402.PubMedCrossRefGoogle Scholar
  29. 29.
    Edgar R.C. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797.PubMedCrossRefGoogle Scholar
  30. 30.
    Hall T.A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98.Google Scholar
  31. 31.
    Jobb G., von Haeseler A., Strimmer K. 2004. TREEFINDER: A powerful graphical analysis environment for molecular phylogenetics. BMC Evol. Biol. 4, 18.PubMedCrossRefGoogle Scholar
  32. 32.
    Friedman N., Ninio M., Pe’er I., Pupko T. 2002. A structural EM algorithm for phylogenetic inference. J. Comput. Biol. 9, 331–353.PubMedCrossRefGoogle Scholar
  33. 33.
    Roure B., Rodriguez-Ezpeleta N., Philippe H. 2007. SCaFoS: A tool for selection, concatenation, and fusion of sequences for phylogenomics. BMC Evol. Biol. 7, Suppl. 1, S2.PubMedCrossRefGoogle Scholar
  34. 34.
    Jameson D., Gibson A.P., Hudelot C., Higgs, P.G. 2003. OGRe: A relational database for comparative analysis of mitochondrial genomes. Nucleic Acids Res. 31, 202–206.PubMedCrossRefGoogle Scholar
  35. 35.
    Talavera G., Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56, 564–577.PubMedCrossRefGoogle Scholar
  36. 36.
    Guindon S., Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704.PubMedCrossRefGoogle Scholar
  37. 37.
    Huelsenbeck J.P., Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 17, 754–755.PubMedCrossRefGoogle Scholar
  38. 38.
    Keane T.M., Creevey C.J., Pentony M.M., Naughton T.J., Mclnerney J.O. 2006. Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol. Biol. 6, 29.PubMedCrossRefGoogle Scholar
  39. 39.
    Keane T.M., Naughton T.J., McInerney J.O. 2007. MultiPhyl: A high-throughput phylogenomics webserver using distributed computing. Nucleic Acids Res. 35, W33–W37.PubMedCrossRefGoogle Scholar
  40. 40.
    Felsenstein J. 2005. PHYLIP (Phylogeny Inference Package) Version 3.6. Distributed by the Author. Seattle, WA: Department of Genome Sciences, University of Washington.Google Scholar
  41. 41.
    Page R.D.M. 1996. TREEVIEW: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357–358.PubMedGoogle Scholar
  42. 42.
    Schmidt H.A., Strimmer K., Vingron M., von Haeseler A. 2002. TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics. 18, 502–504.PubMedCrossRefGoogle Scholar
  43. 43.
    Shimodaira H. 2002. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51, 492–508.PubMedCrossRefGoogle Scholar
  44. 44.
    Shimodaira H., Hasegawa M. 2001. CONSEL: For assessing the confidence of phylogenetic tree selection. Bioinformatics. 17, 1246–1247.PubMedCrossRefGoogle Scholar
  45. 45.
    Van de Peer Y., De Wachter R. 1993. TREECON: A software package for the construction and drawing of evolutionary trees. Comput. Appl. Biosci. 9, 177–182.PubMedGoogle Scholar
  46. 46.
    Dimmic M.W., Rest J.S., Mindell D.P., Goldstein R.A. 2002. rtREV: An amino acid substitution matrix for inference of retrovirus and reverse transcriptase phylogeny. J. Mol. Evol. 55, 65–73.PubMedCrossRefGoogle Scholar
  47. 47.
    Whelan S., Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691–699.PubMedGoogle Scholar
  48. 48.
    Jones D.T., Taylor W.R., Thornton J.M. 1992. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275–282.PubMedGoogle Scholar
  49. 49.
    Mallatt J., Giribet G. 2006. 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.PubMedCrossRefGoogle Scholar
  50. 50.
    Kashiyama K., Seki T., Numata H., Goto S.G. 2009. Molecular characterization of visual pigments in Branchiopoda and the evolution of opsins in Arthropoda. Mol. Biol. Evol. 26, 299–311.PubMedCrossRefGoogle Scholar
  51. 51.
    Kishino H., Hasegawa M. 1989. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J. Mol. Evol. 29, 170–179.PubMedCrossRefGoogle Scholar
  52. 52.
    Rota-Stabelli O., Telford M.J. 2008. 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.PubMedCrossRefGoogle Scholar
  53. 53.
    Pavlinov I.Ya., 2005. Vvedenie v sovremennuyu filogenetiku (Introduction to Modern Phylogenetics). Moscow: KMK.Google Scholar
  54. 54.
    Aleshin V.V., Konstantinova A.V., Mikhailov K.V., Nikitin M.A., Petrov N.B. 2007. Do we need many genes for phylogenetic inference? Biokhimiya. 72, 1610–1623.Google Scholar
  55. 55.
    Zanelli C.F., Valentini S.R. 2007. Is there a role for eIF5A in translation? Amino Acids. 33, 351–358.PubMedCrossRefGoogle Scholar
  56. 56.
    Regier J.C., Shultz J.W. 1998. Molecular phylogeny of arthropods and the significance of the Cambrian ‘explosion’ for molecular systematics. Am. Zool. 38, 918–928.Google Scholar
  57. 57.
    Keeling P.J., Inagaki Y. 2004. A class of eukaryotic GTPase with a punctate distribution suggesting multiple functional replacements of translation elongation factor 1alpha. Proc. Natl. Acad. Sci. USA. 101, 15380–15385.PubMedCrossRefGoogle Scholar
  58. 58.
    Zarenkov N.A., 1983. Chlenistonogie. Rakoobraznye (Arthropods and Crustaceans), part 2. Moscow: Mosk. Gos. Univ.Google Scholar
  59. 59.
    Spears T., Abele L.G. 1998. Crustacean phylogeny inferred from 18S rDNA. In: Arthropod Relationship. The Systematics Association Special Volume Series 55. Eds. Fortey R.A., Thomas R.H. London: Chapman & Hall, pp. 169–187.Google Scholar
  60. 60.
    Savard J., Tautz D., Lercher M.J. 2006. Genome-wide acceleration of protein evolution in flies (Diptera). BMC Evol. Biol. 6, 7.PubMedCrossRefGoogle Scholar
  61. 61.
    Nardi F., Spinsanti G., Boore J.L., Carapelli A., Dallai R., Frati F. 2003. Hexapod origins: Monophyletic or paraphyletic? Science. 299, 1887–1889.PubMedCrossRefGoogle Scholar
  62. 62.
    Carapelli A., Lio P., Nardi F., van der Wath E., Frati F. 2007. Phylogenetic analysis of mitochondrial protein coding genes confirms the reciprocal paraphyly of Hexapoda and Crustacea. BMC Evol. Biol. 7, Suppl. 2, S8.PubMedCrossRefGoogle Scholar
  63. 63.
    Luan Y.X., Mallatt J.M., Xie R.D., Yang Y.M., Yin W.Y. 2005. The phylogenetic positions of three basal-hexapod groups (Protura, Diplura, and Collembola) based on ribosomal RNA gene sequences. Mol. Biol. Evol. 22, 1579–1592.PubMedCrossRefGoogle Scholar
  64. 64.
    Timmermans M.J., Roelofs D., Marién J., van Straalen N.M. 2008. 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.PubMedCrossRefGoogle Scholar
  65. 65.
    Adachi J., Hasegawa M. 1996. Model of amino acid substitution in proteins encoded by mitochondrial DNA. J. Mol. Evol. 42, 459–468.PubMedCrossRefGoogle Scholar
  66. 66.
    Abascal F., Posada D., Zardoya R. 2007. MtArt: A new model of amino acid replacement for Arthropoda. Mol. Biol. Evol. 24, 1–5.PubMedCrossRefGoogle Scholar
  67. 67.
    Rosenberg M.S., Kumar S. 2003. Taxon sampling, bioinformatics, and phylogenomics. Syst. Biol. 52, 119–124.PubMedCrossRefGoogle Scholar
  68. 68.
    Heath T.A., Zwickl D.J., Kim J., Hillis D.M. 2008. Taxon sampling affects inferences of macroevolutionary processes from phylogenetic trees. Syst. Biol. 57, 160–166.PubMedCrossRefGoogle Scholar
  69. 69.
    Goremykin V., Moser C. 2009. Classification of the Arabidopsis ERF gene family based on Bayesian analysis. Mol. Biol. 43, 729–734.CrossRefGoogle Scholar
  70. 70.
    Fenn J.D., Song H., Cameron S.L., Whiting M.F. 2008. A preliminary mitochondrial genome phylogeny of Orthoptera (Insecta) and approaches to maximizing phylogenetic signal found within mitochondrial genome data. Mol. Phylogenet. Evol. 49, 59–68.PubMedCrossRefGoogle Scholar
  71. 71.
    DeSalle R., Freedman T., Prager E.M., Wilson A.C. 1987. Tempo and mode of sequence evolution in mito chondrial DNA of Hawaiian Drosophila. J. Mol. Evol. 26, 157–164.PubMedCrossRefGoogle Scholar
  72. 72.
    Istoricheskoe razvitie klassa nasekomykh (Historical Development of the Class of Insects). 1980. Eds. Rodendorf B.B., Rasnitsyn A.P. Moscow: Nauka. Tr. Paleontol. Inst. Akad. Nauk SSSR, vol. 175.Google Scholar
  73. 73.
    Walossek D., Müller K.J. 1998. Cambrian “Orsten”-type arthropods and the phylogeny of Crustacea. In: Arthropod Relationship. The Systematics Association Special Volume Series 55. Eds. Fortey R.A., Thomas R.H. London: Chapman & Hall, pp. 139–153.Google Scholar
  74. 74.
    Miller B.R., Crabtree M.B., Savage H.M. 1997. Phylogenetic relationships of the Culicomorpha inferred from 18S and 5.8S ribosomal DNA sequences (Diptera: Nematocera). Insect Mol. Biol. 6, 105–114.PubMedCrossRefGoogle Scholar
  75. 75.
    Pawlowski J., Szadziewski R., Kmieciak D., Fahrni J., Bittar G. 2003. Phylogeny of the infraorder Culicomorpha (Diptera: Nematocera) based on 28S RNA gene sequences. Syst. Entomol. 21, 167–178.CrossRefGoogle Scholar
  76. 76.
    Schram F.R. 1986. Crustacea. Oxford: Oxford Univ. Press.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2009

Authors and Affiliations

  • V. V. Aleshin
    • 1
  • K. V. Mikhailov
    • 2
  • A. V. Konstantinova
    • 1
  • M. A. Nikitin
    • 1
  • L. Yu. Rusin
    • 3
    • 4
  • D. A. Buinova
    • 5
  • O. S. Kedrova
    • 4
  • N. B. Petrov
    • 1
  1. 1.Belozersky Institute of Physicochemical BiologyMoscow State UniversityMoscowRussia
  2. 2.Faculty of Bioengineering and BioinformaticsMoscow State UniversityMoscowRussia
  3. 3.Kharkevich Institute for Information Transmission ProblemsRussian Academy of SciencesMoscowRussia
  4. 4.Biological FacultyMoscow State UniversityMoscowRussia
  5. 5.Russian Scientific Center of RoentgenoradiologyMoscowRussia

Personalised recommendations