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What genes and chromosomes say about the origin and evolution of insects and other arthropods

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Abstract

At the turn of the 21st century, the use of molecular and molecular cytogenetic methods led to revolutionary advances in systematics of insects and other arthropods. Analysis of nuclear and mitochondrial genes, as well as investigation of structural rearrangements in the mitochondrial chromosome convincingly supported the Pancrustacea hypothesis, according to which insects originated directly from crustaceans, whereas myriapods are not closely related to them. The presence of the specific telomeric motif TTAGG confirmed the monophyletic origin of arthropods (Arthropoda) and the assignment of tongue worms (Pentastomida) to this type. Several different types of telomeric sequences have been found within the class of insects. Investigation of the molecular organization of these sequences may shed light on the relationships between the orders Diptera, Siphonaptera, and Mecoptera and on the origin of such enigmatic groups as the orders Strepsiptera, Zoraptera and suborder Coleorrhyncha.

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References

  1. Kristensen, N.P., Phylogeny of Insect Orders, Ann. Rev. Entomol., 1981, vol. 26, pp. 135–157.

    Article  Google Scholar 

  2. Kluge, N.Yu., Sovremennaya sistematika nasekomykh (Modern Systematics of Insects), part 1: Printsipy sistematiki zhivykh organizmov i obshchaya sistematika nasekomykh s klassifikatsiei pervichnobeskrylykh i drevnekrylykh (Principles of Systematics of Living Organisms and the General System of Insects with Classification of Primary Wingless and Paleopterous Insects), St. Petersburg: Lan’, 2000.

    Google Scholar 

  3. Telford, M.J. and Thomas, R., Demise of the Atelocerata?, Nature, 1995, vol. 376, pp. 123–124.

    Article  CAS  Google Scholar 

  4. Crampton, G.C., Phylogeny and Classification of Insects, J. Ent. Soc., 1924, vol. 5, pp. 153–157.

    Google Scholar 

  5. Turbeville, J.M., Pfeifer D.A., Field, K.G., and Raft, R.A., The Phylogenetic Status of Arthropods, as Inferred from 18S rRNA Sequences, Mol. Biol. Evol., 1991, vol. 8, no. 5, pp. 669–686.

    CAS  PubMed  Google Scholar 

  6. Ballard, J.W.O., Olsen, G.J., Faith, D.P., et al., Evidence from 12S Ribosomal RNA Sequences That Onychophoras Are Modified Arthropods, Science, 1992, vol. 258, pp. 1345–1347.

    Article  CAS  PubMed  Google Scholar 

  7. Friedrich, M. and Tautz, D., Ribosomal DNA Phylogeny of the Major Extant Arthropod Classes and the Evolution of Myriapods, Nature, 1995, vol. 376, pp. 165–167.

    Article  CAS  PubMed  Google Scholar 

  8. Zrzavy, J., The Basic Body Plan of Arthropods: Insights from Evolutionary Morphology and Developmental Biology, J. Evol. Biol., 1997, vol. 10, pp. 353–367.

    Article  Google Scholar 

  9. Pisani, D., Poling, L.L., Lyons-Weiler, M., and Hedges, S.B., The Colonization of Land by Animals: Molecular Phylogeny and Divergence Times among Arthropods, BMC Biol., 2004, vol. 2, pp. 1–10.

    Article  PubMed  Google Scholar 

  10. Wheeler, W.C., Cartwright, P., and Hayashi, C.Y., Arthropod Phylogeny: A Combined Approach, Cladistics, 1993, vol. 9, pp. 1–39.

    Article  Google Scholar 

  11. Bitsch, J., Bitsch, C., Bourgoin, T., and D’Haese, C., The Phylogenetic Position of Early Hexapod Lineages: Morphological Data Contradict Molecular Data, Syst. Entomol., 2004, vol. 29, pp. 433–440.

    Article  Google Scholar 

  12. Zherikhin, V.V., Ponomarenko, A.G., and Rasnitsyn, A.P., Vvedenie v paleoentomologiyu (Introduction to Paleoentomology), Moscow: KMK, 2008.

    Google Scholar 

  13. Hassanin, A., Phylogeny of Arthropoda Inferred from Mitochondrial Sequences: Strategies for Limiting the Misleading Effects of Multiple Changes in Pattern and Rates of Substitution, Mol. Phyl. Evol., 2006, vol. 38, pp. 100–116.

    Article  CAS  Google Scholar 

  14. Mallatt, J.M., Garey, J.R., and Shultzc, 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. Phyl. Evol., 2004, vol. 31, pp. 178–191.

    Article  CAS  Google Scholar 

  15. Gat, Y.-H., Song, D.-X., Sun, H.-Y., and Zhoul, K.-Y., Myriapod Monophyly and Relationships among Myriapod Classes Based on Nearly Complete 28S and 18S rDNA Sequences, Zool. Sci., 2006, vol. 23, pp. 1101–1108.

    Article  Google Scholar 

  16. Nardi, F., Spinsanti, G., Boore, J.L., et al., Hexapod Origins: Monophyletic or Paraphyletic?, Science, 2003, vol. 299, pp. 1887–1889.

    Article  CAS  PubMed  Google Scholar 

  17. Dunn, C.W., Hejnol, A., Matus, D.Q., et al., Broad Phylogenomic Sampling Improves Resolution of the Animal Tree of Life, Nature, 2008, vol. 452, pp. 745–749.

    Article  CAS  PubMed  Google Scholar 

  18. Giribet, G., Edgecombe, G.D., and Wheeler, W.C., Arthropod Phylogeny Based on Eight Molecular Loci and Morphology, Nature, 2001, vol. 413, pp. 157–161.

    Article  CAS  PubMed  Google Scholar 

  19. Giribet, G., Edgecombe, G.D., Carpenter, J.M., et al., Is Ellipura Monophyletic? A Combined Analysis of Basal Hexapod Relationships with Emphasis on the Origin of Insects, Org. Div. Evol., 2004, vol. 4, pp. 319–340.

    Article  Google Scholar 

  20. Shultz, J.W. and Regier, J.C., Phylogenetic Analysis of Arthropods Using Two Nuclear Protein-Encoding Genes Supports a Crustacean+Hexapod Clade, Proc. R. Soc. London, Ser. B, 2000, vol. 267, pp. 1011–1019.

    Article  CAS  Google Scholar 

  21. Lukhtanov, V.A. and Kuznetsova, V.G., Molecular and Cytogenetic Approaches to Species Diagnostics, Systematics, and Phylogenetics, Zh. Obshch. Biol., 2009, vol. 70, no. 5, pp. 415–437.

    CAS  PubMed  Google Scholar 

  22. Hickson, R.E., Simon, R.E., Cooper, A., et al., Conserved Sequence Motifs, Alignment, and Secondary Structure for the Third Domain of Animal 12S rRNA, Mol. Biol. Evol., 1996, vol. 13, pp. 150–169.

    CAS  PubMed  Google Scholar 

  23. Xie, Q., Tian, X., Qin, Y., and Bu, W., Phylogenetic Comparison of Local Length Plasticity of the Small Subunit of Nuclear rDNAs among All Hexapoda Orders and the Impact of Hyper-Length-Variation on Alignment, Mol. Phyl. Evol., 2009, vol. 50, pp. 310–316.

    Article  CAS  Google Scholar 

  24. Ronquist, F. and Huelsenbeck, J.P., MrBayes 3: Bayesian Phylogenetic Inference under Mixed Models, Bioinformatics, 2003, vol. 19, pp. 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  25. Misof, B., Niehuis, O., Bischoff, I., et al., Towards to 18S Phylogeny of Hexapods: Accounting for Group-Specific Character Covariance in Optimized Mixed Nucleotide/Doublet Models, Zoology, 2007, vol. 110, pp. 409–429.

    Article  CAS  PubMed  Google Scholar 

  26. Kjer, K.M., Aligned 18S and Insect Phylogeny, Syst. Biol., 2004, vol. 53, pp. 506–514.

    Article  PubMed  Google Scholar 

  27. Regier, J.C., Shultz, J.W., Ganley, A.R.D., et al., Resolving Arthropod Phylogeny: Exploring Phylogenetic Signal within 41 Kb of Protein-Coding Nuclear Gene Sequence, Syst. Biol., 2008, vol. 57, no. 6, pp. 920–938.

    Article  CAS  PubMed  Google Scholar 

  28. Felsenstein, J., Inferring Phylogenies, Sunderland, Massachusetts Sinauer Ass., 2004.

    Google Scholar 

  29. Shcherbakov, D.E., Controversies over the Insect Origin Revisited: AMBA Projects AM/PFICM98/1.99, in Proceedings of the First International Paleontological Conference, Moscow, 1998, pp. 141–148.

  30. Boore, J.L., Collins, T.M., Stanton, D., et al., Deducing the Pattern of Arthropod Phylogeny from Mitochondrial DNA Rearrangements, Nature, 1995, vol. 376, pp. 163–165.

    Article  CAS  PubMed  Google Scholar 

  31. Ballard, J.W.O. and Whitlock, M.C., The Incomplete Natural History of Mitochondria, Mol. Ecol., 2004, vol. 13, pp. 729–744.

    Article  PubMed  Google Scholar 

  32. Lavrov, D.V. and Lang, B.F., Poriferan mtDNA and Animal Phylogeny Based on Mitochondrial Gene Arrangements, Syst. Biol., 2005, vol. 54, pp. 651–659.

    Article  PubMed  Google Scholar 

  33. Sturtevant, A.H., Dobzhansky, T., Inversions in the Third Chromosome of Wild Races of Drosophila pseudoobscura, and Their Use in the Study of the History of the Species, Proc. Natl. Acad. Sci. USA, 1936, vol. 22, pp. 448–450.

    Article  CAS  PubMed  Google Scholar 

  34. Boore, J.L., Lavrov, D.V., and Brown, W.M., Gene Translocation Links Insects and Crustaceans, Nature, 1998, vol. 392, pp. 667–668.

    Article  CAS  PubMed  Google Scholar 

  35. Aleshin, V.V., Mikhailov, K.V., Konstantinova, A.V., et al., On the Phylogenetic Position of Hexapoda within the Clade Pancrustacea, Mol. Biol., 2009, vol. 43, no. 5, pp. 866–881.

    CAS  Google Scholar 

  36. Glenner, H., Thomsen, P.F., Hebsgaard, M.B., et al., The Origin of Insects, Science, 2006, vol. 314, pp. 1883–1884.

    Article  CAS  PubMed  Google Scholar 

  37. Shao, R., Kirkness, E.F., and Barker, S.C., The Single Mitochondrial Chromosome Typical of Animals Has Evolved into 18 Minichromosomes in the Human Body Louse, Pediculus humanus, Genet. Res., 2009, vol. 19, pp. 904–912.

    Article  CAS  Google Scholar 

  38. Rand, D.M., ’Why Genomes in Pieces?’ Revisited: Sucking Lice Do Their Own Thing in mtDNA Circle Game, Genet. Res., 2009, vol. 19, pp. 700–702.

    Article  CAS  Google Scholar 

  39. Zakian, V.A., Telomeres: Beginning to Understand the End, Science, 1995, vol. 270, pp. 1601–1607.

    Article  CAS  PubMed  Google Scholar 

  40. Traut, W., Szczepanowski, M., Vitková, M., et al., The Telomere Repeat Motif of Basal Metazoa, Chromosome Res., 2007, vol. 15, no. 3, pp. 371–382.

    CAS  PubMed  Google Scholar 

  41. Vitková, M., Král, J., Traut, W., et al., The Evolutionary Origin of Insect Telomeric Repeats, (TTAGG)n, Chromosome Res., 2005, vol. 13, pp. 145–156.

    Article  PubMed  Google Scholar 

  42. Chesunov, A.V., Pentastomida Casus: Special Problem in the Context of Modern Phylogenetics, Zh. Obshch. Biol., 2002, vol. 63, no. 3, pp. 209–226.

    CAS  PubMed  Google Scholar 

  43. Lavrov, D.V., Brown, W.M., and Boore, J.L., Phylogenetic Position of the Pentastomida and (Pan)Crustacean Relationships, Proc. R. Soc. London, Ser. B, 2004, vol. 271, pp. 537–544.

    Article  Google Scholar 

  44. Pelliccia, F., Volpi, E.V., Lanza, V., et al., Telomeric Sequences of Asellus aquaticus (Crustacea, Isopoda), Heredity, 1994, vol. 72, pp. 78–80.

    Article  Google Scholar 

  45. Frydrychová, R., Grossmann, P., Truba, P., et al., Phylogenetic Distribution of TTAGG Telomeric Repeats in Insects, Genome, 2004, vol. 47, pp. 163–178.

    Article  PubMed  Google Scholar 

  46. Ouvrard, D., Campbell, B.C., and Chan, K.L., I8S rRNA Secondary Structure and Phylogenetic Position of Peloridiidae (Insecta, Hemiptera), Mol. Phyl. Evol., 2000, vol. 16, no. 3, pp. 403–417.

    Article  CAS  Google Scholar 

  47. Forero, D., The Systematics of the Hemiptera, Rev. Colombiana Entomol., 2008, vol. 34, no. 1, pp. 1–21.

    Google Scholar 

  48. Rosen, M., and Edström, J., DNA Structures Common for Chironomid Telomeres Terminating with Complex Repeats, Insect Mol. Biol., 2000, vol. 9, pp. 341–347.

    Article  CAS  PubMed  Google Scholar 

  49. Walter, M.F., Bozorgnia, L., Maheshwari, A., and Biessmann, H., The Rate of Terminal Nucleotide Loss from a Telomere of the Mosquito Anopheles gambiae, Insect Mol. Biol., 2001, vol. 10, pp. 105–110.

    Article  CAS  PubMed  Google Scholar 

  50. Biessmann, H. and Mason, J.M., Telomerase-Independent Mechanisms of Telomere Maintenance, Cell Mol. Life Sci., 2003, vol. 60, pp. 2325–2333.

    Article  CAS  PubMed  Google Scholar 

  51. Whiting, M.F., Phylogeny of the Holometabolous Insect Orders: Molecular Evidence, Zool. Scripta, 2002, vol. 31, pp. 3–15.

    Article  Google Scholar 

  52. Bonneton, F., Brunei, F.G., Kathirithamby, J., and Laudet, V., The Rapid Divergence of the Ecdysone Receptor Is a Synapomorphy for Mecopterida That Clarifies the Strepsiptera Problem, Insect Mol. Biol., 2006, vol. 15, no. 3, pp. 351–362.

    Article  CAS  PubMed  Google Scholar 

  53. Rodendorf, B.B., Osnovy paleontologii: Chlenistonogie—trakheinye i khelitserovye (Fundamentals of Paleontology: Artropoda—Tracheids and Chelicerids), Moscow: Nauka, 1962.

    Google Scholar 

  54. Kristensen, N.P., Forthy Years’ Insect Phylogenetic Systematics, Zool. Beitrage N.F., 1995, vol. 36, pp. 83–124.

    Google Scholar 

  55. Engel, M.S. and Grimaldi, D.A., A Winged Zorotypus in Miocene Amber from the Dominican Republic (Zoraptera: Zorotypidae), with Discussion on Relationships of and within the Order, Acta Geol. Hisp., 2000, vol. 35, pp. 149–164.

    Google Scholar 

  56. Kuznetsova, V.G., Nokkala, S., and Shcherbakov, D.E., Karyotype, Reproductive Organs, and Pattern of Gametogenesis in Zorotypus hubbardi Caudell (Insecta: Zoraptera, Zorotypidae), with Discussion on Relationships of the Order, Can. J. Zool., 2002, vol. 80, pp. 1047–1054.

    Article  Google Scholar 

  57. Kuznetsova, V.G., The Chromosomes of the Holokinetic Type and Their Distribution among Insects and Other Invertebrate Animals, in Kariosistematika bespozvonochnykh zhivotnykh (Karyosystematics of Invertebrates), Leningrad: Zool. Inst. Akad. Nauk SSSR, 1979, pp. 5–19.

    Google Scholar 

  58. Yoshizava, K. and Johson, K.P., Aligned 18S for Zoraptera (Insecta): Phylogenetic Position and Molecular Evolution, Mol. Phyl. Evol., 2005, vol. 37, pp. 572–580.

    Article  Google Scholar 

  59. Yoshizawa, K., The Zoraptera Problem: Evidence for Zoraptera and Embiodea from the Wing Base, Syst. Entomol., 2007, vol. 32, pp. 197–204.

    Article  Google Scholar 

  60. Terry, M.D. and Whiting, M.F., Mantophasmatodea and Phylogeny of the Lower Neopterous Insects, Cladistics, 2005, vol. 21, pp. 240–257.

    Article  Google Scholar 

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Authors and Affiliations

  1. Zoological Institute, Russian Academy of Sciences, St. Petersburg, 199034, Russia

    V. A. Lukhtanov & V. G. Kuznetsova

  2. Department of Entomology, St. Petersburg State University, St. Petersburg, 199034, Russia

    V. A. Lukhtanov

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  1. V. A. Lukhtanov
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  2. V. G. Kuznetsova
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Original Russian Text © V.A. Lukhtanov, V.G. Kuznetsova, 2010, published in Genetika, 2010, Vol. 46, No. 9, pp. 1258–1265.

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Lukhtanov, V.A., Kuznetsova, V.G. What genes and chromosomes say about the origin and evolution of insects and other arthropods. Russ J Genet 46, 1115–1121 (2010). https://doi.org/10.1134/S1022795410090279

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