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Type: Article
Published: 2017-02-20
Page range: 523–534
Abstract views: 63
PDF downloaded: 1

Molecular Phylogenetic Analysis of the Orthoptera (Arthropoda, Insecta) based on Hexamerin Sequences

College of Life Sciences, The Key Laboratory of Zoological Systematics and Application, , Hebei University, 071002 Baoding, P. R. China
College of Life Sciences, The Key Laboratory of Zoological Systematics and Application, , Hebei University, 071002 Baoding, P. R. China
College of Life Sciences, The Key Laboratory of Zoological Systematics and Application, , Hebei University, 071002 Baoding, P. R. China
College of Life Sciences, The Key Laboratory of Zoological Systematics and Application, , Hebei University, 071002 Baoding, P. R. China
College of Life Sciences, The Key Laboratory of Zoological Systematics and Application, , Hebei University, 071002 Baoding, P. R. China
College of Life Sciences, The Key Laboratory of Zoological Systematics and Application, , Hebei University, 071002 Baoding, P. R. China
Orthoptera Insect Hexamerin sequences Molecular phylogeny

Abstract

The higher taxa classification and phylogeny of the insect order Orthoptera have long been controversial. Hexamerin, as a member of the highly conserved arthropod hemocyanin superfamily, has been shown to be a good marker for the phylogenetic study of insects. However, few studies have used hexamerins on the phylogeny of Orthoptera. In this study, we determined twenty-seven different hexamerin subunit type sequences in seventeen speices of Orthoptera. In order to infer the phylogenetic relationships among the superfamilies within Orthoptera and test the monophyly of Orthoptera, phylogenic trees were reconstructed using Neighbor-Joining (NJ) and Bayesian inference (BI) methods with two dipluran and three hymenopteran hexamerin sequences as outgroups. The result supported the monophyly of Orthoptera, which includes two monophyletic suborders Caelifera and Ensifera. The Caelifera includes Acridoidea, Eumastacoidea, Tetrigoidea and Tridactyloidea, and the Ensifera includes Tettigonioidea, Grylloidea and Gryllotalpoidea. Our study is basically consistent with the study of morphological classification. In addition, our study indicates that a relatively comprehensive taxa sampling is essential to solve some problems in phylogenetic reconstruction.

 

References

  1. Abascal, F., Zardoya, R. & Posada, D. (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics, 21 (9), 2104–2105.
    https://doi.org/10.1093/bioinformatics/bti263

    Ander, K. (1931) Orthopterologische Beitrage 1– 2. Entomologisk tidskrift, 52, 245–257.

    Beintema, J.J., Stam, W.T., Hazes, B. & Smidt, M.P. (1994) Evolution of arthropod hemocyanins and insect storage proteins (hexamerins). Molecular Biology and Evolution, 11 (3), 493–503.

    Burmester, T. & Scheller, K. (1996) Common origin of arthropod tyrosinase, arthropod hemocyanin, insect hexamerin, and dipteran arylphorin receptor. Journal of Molecular Evolution, 42 (6), 713–728.
    https://doi.org/10.1007/BF02338804

    Burmester, T., Massey, Jr. H.C., Zakharkin, S.O. & Benes, H. (1998) The evolution of hexamerins and the phylogeny of insects. Journal of Molecular Evolution, 47 (47), 93–108.
    https://doi.org/10.1007/PL00006366

    Burmester, T. (1999) Evolution and function of insect hexamerins. European Journal of Entomology, 96 (3), 213–225.

    Burmester, T. & Scheller, K. (1999) Ligands and receptors: common theme in insect storage protein transport. Die Naturwissenschaften, 86 (10), 468–474.
    https://doi.org/10.1007/s001140050656

    Burmester, T. (2002) Origin and evolution of arthropod hemocyanins and related proteins. Journal of Comparative Physiology B, 172 (2), 95–107.
    https://doi.org/10.1007/s00360-001-0247-7

    Burmester, T. & Hankeln, T. (2007) The respiratory proteins of insects. Journal of Insect Physiology, 53 (4), 285–294.
    https://doi.org/10.1016/j.jinsphys.2006.12.006

    Burmester, T. (2014) Expression and evolution of hexamerins from the tobacco hornworm, Manduca sexta, and other Lepidoptera. Insect Biochemistry and Molecular Biology, 62, 226–234.
    https://doi.org/10.1016/j.ibmb.2014.11.009

    Dong, L.J, Shi, J.P., Zhang, X.H., Zhang, Y.L., Li, X.J. & Yin, H. (2015) Molecular phylogenetic analysis of Acridoidea (Orthoptera: Caelifera) based on mitochondrial cytochrome oxidase subunit sequences. Zootaxa, 4018 (3), 411–425.
    https://doi.org/10.11646/zootaxa.4018.3.5

    Dong, L.J., Zhang, X.H., Li, Y.L., Lu, S.S. & Yin, H. (2015) Cloning and Expression Analysis of the Hexamerin Gene from Acrida cinerea (Acridoidea: Acrididae). Journal of Agricultural Science and Technology, 17 (4), 78–84.

    Dirsh, V.M. (1975) Classification of the Acridomorphoid Insects. E. W. Classey Ltd., Farringdon, 171 pp., 74 figs.

    Ertas, B., von Reumont, B.M., Wägele, J.W., Misof, B. & Burmester, T. (2009) Hemocyanin suggests a close relationship of Remipedia and Hexapoda. Molecular Biology and Evolution, 26 (2), 711–2718.
    https://doi.org/10.1093/molbev/msp186

    Enderle, U., Käuser, G., Renn, L., Scheller, K. & Koolman, J. (1983) Ecdysteroids in the hemolymph of blowfly are bound to calliphorin. In: Scheller, K. (Ed.), The Larval Serum Proteins of Insects: Function, Biosynthesis, Genetic. Georg Thieme Verlag, Stuttgart, New York, pp. 40–49.

    Flook, P.K. & Rowell, C.H.F. (1997) The effectiveness of mitochondrial rRNA gene sequences for the reconstruction of the phylogeny of an insect order, Orthoptera. Molecular Phylogenetics & Evolution, 8 (2), 177–192.
    https://doi.org/10.1006/mpev.1997.0425

    Flook, P.K. & Rowell, C.H.F. (1998) Inferences about Orthopteroid phylogeny and molecular evolution from small subunit nuclear ribosomal DNA sequences. Insect Molecular Biology, 7 (2), 163–178.
    https://doi.org/10.1046/j.1365-2583.1998.72060.x

    Flook, P.K., Klee. S. & Rowell, C.H.F. (1999) Combined molecular Phylogenetic analysis of the Orthoptera and implications for their higher systematics. Systematic Biology, 48 (2), 233–253.
    https://doi.org/10.1080/106351599260274

    Flook, P.K., Klee, S. & Rowell, C.H.F. (2000) Molecular Phylogenetic Analysis of the Pneumoroidea (Orthoptera, Caelifera): Molecular Data Resolve Morphological Character Conflicts in the Basal Acridomorpha. Molecular Phylogenetics & Evolution, 15 (3), 345–354.
    https://doi.org/10.1006/mpev.1999.0759

    Fujii, T., Sakurai, H., Izumi, S. & Tomino, S. (1989) Structure of the gene for the arylphorin-type storage protein SP 2 of Bombyx mori. Journal of Biological Chemistry, 264 (19), 11020–11025.

    Handlirsch, A. (1910) Canadian fossil insects. Insects from the tertiary lake deposits of the southern interior of British Columbia, collected by Mr. Lawrence M. Lambe in 1906. Contributions Canadian Survey. Contributions to Canadian palaeontology, Pal. 2, 93–129 + viii.

    Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics, 17 (8), 754–755.
    https://doi.org/10.1093/bioinformatics/17.8.754

    Hagner-Holler, S., Schoen, A., Erker, W., Marden, J.H., Rupprecht, R., Decker, H. & Burmester, T. (2004) A respiratory hemocyanin from an insect. Proceedings of the National Academy of Sciences of the United States of America, 101 (3), 871–874.
    https://doi.org/10.1073/pnas.0305872101

    Hagner-Holler, S., Pick, C., Girgenrath, S., Marden, J.H. & Burmester, T. (2007) Diversity of stonefly hexamerins and implication for the evolution of insect storage proteins. Insect Biochemistry & Molecular Biology, 37 (10), 1064–1074.
    https://doi.org/10.1016/j.ibmb.2007.06.001

    Kevan, D.K. McE. (1982) Orthoptrea. In: McGraw Hill synopsis and classification of Living Organisms. McGraw Hill Book Company, New York, pp. 352–838.

    Kusche, K. & Burmester, T. (2001) Molecular cloning and evolution of lobster hemocyanin. Biochemical and Biophysical Research Communications, 282 (4), 887–892.
    https://doi.org/10.1006/bbrc.2001.4660

    Kusche, K. & Burmester, T. (2001) Diplopod hemocyanin sequence and the phylogenetic position of the Myriapoda. Molecular Biology & Evolution, 18 (8), 1566–1573.
    https://doi.org/10.1093/oxfordjournals.molbev.a003943

    Liu, D.F. & Jiang, G.F. (2005) Molecular phylogenetic analysis of Acridoidea based on 18S rDNA with a discussion on its taxonomic system. Acta Entomologica Sinica, 48 (2), 232–241.

    Lartillot, N., Lepage, T. & Blanquart, S. (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics, 25 (17), 2286–2288.
    https://doi.org/10.1093/bioinformatics/btp368

    Le, S.Q. & Gascuel, O. (2008) An improved general amino acid replacement matrix. Molecular Biology and Evolution, 25 (7), 1307–1320.
    https://doi.org/10.1093/molbev/msn067

    Ma, C., Yang, P.C., Jiang, F., Chapuis, M.P., Shali, Y., Sword, G.A. & Kang, L. (2012) Mitochondrial genomes reveal the global phylogeography and dispersal routes of the migratory locust. Molecular Ecology, 21 (17), 4344–4358.
    https://doi.org/10.1111/j.1365-294X.2012.05684.x

    Martins, J.R., Nunes, F.M.F., Cristino, A.S., Simões, Z.L.P. & Bitondi, M.M.G. (2010) The four hexamerin genes in the honey bee: structure, molecular evolution and function deduced from expression patterns in queens, workers and drones. Bmc Molecular Biology, 11 (23), 1–20.
    https://doi.org/10.1186/1471-2199-11-23

    Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, pp. 1–8.
    https://doi.org/10.1109/GCE.2010.5676129

    Nicholas, K.B. & Nicholas, H.B. Jr. (1997) GeneDoc: Analysis and Visualization of Genetic Variation. Available from: http://www.psc.edu/biomed/genedoc/ (accessed 20 Decembe 2016)

    Nagamanju, P., Hansen, I.A., Burmester, T., Meyer, S.R., Scheller, K. & Dutta-Gupta, A. (2003) Complete sequence, expression and evolution of two members of the hexamerin protein family during the larval development of the rice moth, Corcyra cephalonica. Insect Biochemistry & Molecular Biology, 33 (1), 73–80.
    https://doi.org/10.1016/S0965-1748(02)00178-9

    Pick, C., Hagner-Holler, S. & Burmester, T. (2008) Molecular characterization of hemocyanin and hexamerin from the firebrat Thermobia domestica (Zygentoma). Insect Biochemistry and Molecular Biology, 38 (11), 977–983.
    https://doi.org/10.1016/j.ibmb.2008.08.001

    Scheller, K., Fischer, B. & Schenkel, H. (1990) Molecular properties, functions and developmentally regulated biosynthesis of arylphorin in Calliphora vicina. In: Hagedorn, H.H. (Ed.), Molecular Insect Science. Plenum, New York, pp. 155–162.
    https://doi.org/10.1007/978-1-4899-3668-4_19

    Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28 (10), 2731–2739.
    https://doi.org/10.1093/molbev/msr121

    Terwilliger, N.B., Dangott, L.J. & Ryan, M.C. (1999) Cryptocyanin, a crustacean molting protein: evolutionary links to arthropod hemocyanin and insect hexamerins. Proceedings of the National Academy of Sciences, 96 (5), 2013–2018.
    https://doi.org/10.1073/pnas.96.5.2013

    Terwilliger, N.B., Ryan, M.C. & Towle, D. (2005) Evolution of novel functions: crypto-cyanin helps build new exoskeleton in Cancer magister. Journal of Experimental Biology, 208 (13), 2467–2474.
    https://doi.org/10.1242/jeb.01667

    Telfer, W.H. & Kunkel, J.G. (1991) The function and evolution of insect storage hexamerins. Annual Review of Entomology, 36 (1), 205–228.
    https://doi.org/10.1146/annurev.en.36.010191.001225

    Von, Heijne, G. (1986) A simple method for predicting signal peptide cleavage sequences. Nucleic Acids Res, 14, 4683–4690.
    https://doi.org/10.1093/nar/14.11.4683

    Willott, E., Wang, X.Y. & Wells, M.A. (1989) cDNA and gene sequence of Manduca sexta arylphorin, an aromatic amino acid-rich larval serum protein. Homology to arthropod hemocyanins. Journal of Biological Chemistry, 264 (32), 19052–19059.

    Whelan, S. & Goldman, N. (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Molecular Biology and Evolution, 18 (18), 691–699.
    https://doi.org/10.1093/oxfordjournals.molbev.a003851

    Xia, K.L. (1958) Taxonomic essentials of Acrididae from China. Science Press, Biejing, 239 pp. [in Chinese]

    Xie, W. & Luan, Y.X. (2014) Evolutionary implications of dipluran hexamerins. Insect Biochemistry and Molecular Biology, 46 (1), 17–24.
    https://doi.org/10.1016/j.ibmb.2014.01.003

    Yang, J., Ren, Q. & Huang, Y. (2016) Complete mitochondrial genomes of three crickets (Orthoptera: Gryllidae) and comparative analyses within Ensifera mitogenomes. Zootaxa, 4092 (4), 529–47.
    https://doi.org/10.11646/zootaxa.4092.4.4

    Yuan, F. (1996) Insect taxonomy. China Agriculture Press, Beijing, 46 pp.

    Yin, H., Li, X.J., Wang, W.Q. & Yin, X.C. (2004) Inferences about Acridoidea phylogenetic relationships from small subunit nuclear ribosomal DNA sequence. Acta Entomologica Sinica, 47 (6), 809–814.

    Yin, X.C., Li, X.J., Wang, W.Q., Yin, H., Cao, C.Q., Ye, B.H. & Yin, Z. (2008) Phylogenetic analyses of some genera in Oedipodidae (Orthoptera: Acridoidea) based on 16S mitochondrial partial gene sequences. Insect Science, 15, 471–476.
    https://doi.org/10.1111/j.1744-7917.2008.00235.x

    Zhou, X., Tarver, M.R. & Scharf, M.E. (2007) Hexamerin-based regulation of juvenile hormone-dependent gene expression underlies phenotypic plasticity in a social insect. Development, 134 (3), 601–610.
    https://doi.org/10.1242/dev.02755

    Zhang, D.C., Li, X.J., Wang, W.Q., Yin, H., Yin, Z. & Yin, X.C. (2005) Molecular phylogeny of Ssme genera of Pamphagidae (Acridoidea, Orthoptera) from China based on mitochondrial 16S rDNA sequences. Zootaxa, 1103, 41–49.

    Zhang, X.H., Li, X.L., Zhang, K.J., Hou, J. & Yin, H. (2016) Cloning and expression analysis of the Hexamerin subunit type 2 (Hex2) from the grasshopper, Calliptamus italicus (Orthoptera:Catantopidae). Acta Entomologica sinica, 59 (2), 156–163.

    Zhou, Y. (1963) Some viewpoints about insect taxonomy. Acta Entomologica Sinica, 12, 586596.