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Complete mitochondrial genome of bamboo grasshopper, Ceracris fasciata, and the phylogenetic analyses and divergence time estimation of Caelifera (Orthoptera)

Published online by Cambridge University Press:  07 September 2017

S. Gao ,
J.J. Chen  and
G.F. Jiang
S. Gao
Affiliation:
Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, PR China
J.J. Chen
Affiliation:
Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, PR China
G.F. Jiang*
Affiliation:
Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, PR China College of Oceanology and Food Science, Quanzhou Normal University, Quanzhou 362000, PR China
*
*Author for correspondence Phone: +0086 177 5076 1161 Fax: +0086 595 2291 9563 E-mail: [email protected]
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Abstract

The bamboo grasshopper Ceracris fasciata is regarded as a major pest species because of the damage it causes to bamboo, and its classification within the families and subfamilies of the suborder Caelifera remains unclear. Thus, we attempted to resolve these questions using molecular biology methods and analyses. Our results are as follows: (1) the complete mitochondrial genome of C. fasciata is 15,569 bp in length. The mitochondrial genome contains a standard set of 13 protein-coding genes, 22 transfer RNA genes, 2 ribosomal RNA genes and an A + T-rich region in the same order as those of the other analysed Caeliferan species. The putative start codon for the COX1 gene in C. fasciata is ACC, although it is not defined in other genes. The presence of tandem repeats of different sizes in the A + T-rich region may lead to size differences in other mitochondrial genomes. The mitochondrial genome of C. fasciata harbours the typical 37 genes and an A + T-rich region, and it shows similar characteristics to those of other grasshopper species. Characterization of the mitochondrial genome has enriched our knowledge of the mitochondrial genomes of Orthoptera around the world. Therefore, the phylogenetic relationships in Orthoptera can be re-examined. (2) In phylogenetic analyses, the monophyly of Orthoptera and its two suborders (Caelifera and Ensifera) has been consistently recovered based on most of the datasets selected, regardless of the optimal criteria. Our results do not support the monophyly of the subfamily Oedipodinae of Caelifera. We found that Phlaeoba albonema of the Acridinae is sorted into a clade with Ceracris in all our phylogenetic trees, and field experiments show that Phlaeoba always lives with Ceracris in the same ecotopes. Therefore, we suggest that Phlaeoba should be classified as a member of the Oedipodinae. We found that C. fasciata always clustered with Ceracris kiangsu, and both were sisters to Ceracris versicolor. Therefore, the genetic relationship between C. fasciata and C. kiangsu is closer than that between C. fasciata and C. versicolor. (3) The oldest estimated time of divergence of Ensifera in this context was determined to be 146.16 million years ago (Mya), or around the late Jurassic or early Cretaceous. We estimated that katydids (Grylloidea) likely diverged from other groups in the early Cretaceous. According to our divergence time analyses, we concluded that the ancestral Acrididae probably originated in the early Paleogene, and it is likely that the major diversification events happened at the middle Paleogene, well into the next geologic time. We estimated that crickets (Tettigoniidae) likely diverged from other groups in the early Cretaceous. Acrididae and Romaleinae group, Pyrgacrididae and Ommexechidae group, the youngest two clades we observed, were estimated to have diverged 58.79 Mya, between the middle and early Paleogene. C. versicolor is a sister to the group containing C. kiangsu and C. fasciata. First, C. versicolor diverged from the sister group (C. kiangsu + C. fasciata) around 44.81 Mya, and then the C. kiangsu and C. fasciata group separated at 43.04 Mya.

Keywords

OrthopteraCeracris fasciataphylogenetic analysisdivergence time estimation
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 3 , June 2018 , pp. 321 - 336
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Copyright © Cambridge University Press 2017 

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References

Alexander, R.D. (1968) Life cycle origins, speciation, and related phenomena in crickets. Quarterly Review of Biology 43, 1–41.Google Scholar
Amedegnato, C. (1974) Les genres d'acridiens neotropicaux, leur classification par familles, sous-familles et tribus. Acrida 3, 193–203.Google Scholar
Amédégnato, C., Chapco, W. & Litzenberger, G. (2003) Out of South America? Additional evidence for a southern origin of melanopline grasshoppers. Molecular Phylogenetics and Evolution 29, 115–119.Google Scholar
Ander, K. (1939) Vergleichend-Anatomische und Phylogenetische Studien €uber die Ensifera (Saltatoria). Opuscula Entomological Supplement 2, 1–306.Google Scholar
Baccetti, B.M. (1987) Evolutionary Biology of Orthopteroid Insects. Chichester, Ellis Horwood Limited.Google Scholar
Blackith, R.E. & Blackith, R.M. (1968) A numerical taxonomy of orthopteroid insects. Australian Journal of Zoology 16, 111–131.Google Scholar
Boore, J.L. (1999) Animal mitochndrial genomes. Nucleic Acids Research 27, 1767–1780.CrossRefGoogle Scholar
Boore, J.L. & Brown, W.M. (2000) Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Molecular Biology and Evolution 17, 87–106.CrossRefGoogle Scholar
Cameron, S.L., Miller, K.B., D'Haese, C.A., Whiting, M.F. & Barker, S.C. (2004) Mitochondrial genome data alone are not enough to unambiguously resolve the relationships of Entognatha, Insecta and Crustacea sensu lato (Arthropoda). Cladistics 20, 534–557.Google Scholar
Carapelli, A., Liò, 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 Evolutionary Biology 7 (Suppl 2), S8.CrossRefGoogle ScholarPubMed
Caterino, M.S., Cho, S. & Sperling, F.A.H. (2000) The current state of insect molecular systematics: a thriving tower of Babel. Annual Review of Entomology 45, 1–54.Google Scholar
Chapco, W. & Litzenberger, G. (2002) A molecular phylogenetic study of two relict species of melanopline grasshoppers. Genome 45, 313–318.Google Scholar
Chapco, W., Litzenberger, G. & Kuperus, W.R. (2001) A molecular biogeographic analysis of the relationship between North American melanoploid grasshoppers and their Eurasian and South American relatives. Molecular Phylogenetics and Evolution 18, 460–466.Google Scholar
Chapman, R.F. & Joern, A. (Eds) (1990) Biology of Grasshoppers. New York, John Wiley & Sons.Google Scholar
Chintauan-Marquier, I., Legendre, F., Hugel, S., Robillard, T., Grandcolas, P., Nel, A., Zuccon, D. & Desutter-Grandcolas, L. (2016) Laying the foundations of evolutionary and systematic studies in crickets (Insecta, Orthoptera): a multilocus phylogenetic analysis. Cladistics 32, 54–81.CrossRefGoogle ScholarPubMed
Chopard, L. (1920). Recherches sur la conformation et le développement des derniers segmentes abdominaux chez les orthoptères. Thèse de la Faculté des Sciences de Paris. Rennes: Imprimerie Oberthur.CrossRefGoogle Scholar
Chopard, L. (1949) Ordres des Orthopteres. pp. 617–722 in Grasse, P.P. (Ed.) Traite de Zoologie. Paris, Masson.Google Scholar
Cigliano, M.M., Braun, H., Eades, D.C. & Otte, D. (2017) Orthoptera Species File. Version 5.0/5.0. Available online at http://Orthoptera.SpeciesFile.org.Google Scholar
Desutter-Grandcolas, L. (2003) Phylogeny and the evolution of acoustic communication in extant Ensifera (Insecta, Orthoptera). Zoologica Scripta 32, 525–561.Google Scholar
Dirsh, V.M. (1973) Genital organs in Acridomorphoidea (Insecta) as taxonomic character. Journal of Zoological Systematics and Evolutionary Research 11, 133.Google Scholar
Dirsh, V.M. (1975) Classification of the Acridomorphoid Insects. Faringdon, Classey EW. Ltd.Google Scholar
Dixon, A.P., Faber-Langendoen, D., Josse, C., Morrison, J. & Loucks, C.J. (2014) Distribution mapping of world grassland types. Journal of Biogeography 41, 2003–2019.Google Scholar
Drummond, A.J., Ho, S.Y.W., Phillips, M.J. & Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. Plos Biology 4, 699–710.Google Scholar
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.CrossRefGoogle ScholarPubMed
Eades, D.C. (2000) Evolutionary relationships of phallic structures of Acridomorpha (Orthoptera). Journal of Orthoptera Research 9, 181–210.Google Scholar
Eades, D.C., Otte, D., Cigliano, M.M. & Braun, H. (2014) Orthoptera Species File. Version 5.0/5.0. [8/1/2014]. Available online at http://Orthoptera.SpeciesFile.org.Google Scholar
Faircloth, B.C., McCormac, J.E., Crawford, N.G., Harvey, M.G., Brumfield, R.T. & Glenn, T.C. (2012) Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Systematic Biology 61, 717–726.Google Scholar
Fenn, J.D., Cameron, S.L. & Whiting, M.F. (2007) The complete mitochondrial genome sequence of the Mormon cricket (Anabrus simplex: Tettigoniidae: Orthoptera) and an analysis of control region variability. Insect Molecular Biology 16, 239–252.CrossRefGoogle Scholar
Flook, P., Rowell, H. & Gellissen, G. (1995 a) Homoplastic rearrangements of insect mitochondrial tRNA genes. Science of Nature 82, 336–337.Google Scholar
Flook, P.K. & Rowell, C.H.F. (1997) The phylogeny of the Caelifera (Insecta, Orthoptera) as deduced from mitochondrial rRNA gene sequences. Molecular Phylogenetics Evolution 8, 89–103.CrossRefGoogle Scholar
Flook, P.K. & Rowell, C.H. (1998) Inferences about orthopteroid phylogeny and molecular evolution from small subunit nuclear ribosomal DNA sequences. Insect Molecular Biology 7, 163–178.Google Scholar
Flook, P.K., Rowell, C.H.F. & Gellissen, G. (1995 b) The sequence, organization, and evolution of the Locusta migratoria mitochondrial genome. Journal Molecular Evolution 41, 928–941.Google Scholar
Flook, P.K., Klee, S. & Rowell, C.H.F. (1999) Combined molecular phylogenetic analysis of the Orthoptera (Arthropoda, Insecta) and implications for their higher systematics. Systematic Biology 48, 233–253.CrossRefGoogle ScholarPubMed
Gangwere, S.K., Muralirangan, M.C. & Muralirangan, M. (Eds) (1997) The Bionomics of Grasshoppers, Katydids, and Their Kin. New York, CAB International.Google Scholar
Gorochov, A.V. (1995 a) Contribution to the system and evolution of the order Orthoptera. Zoologichesky Zhurnal 74, 39–45.Google Scholar
Gorochov, A.V. (1995 b) System and evolution of the suborder Ensifera (Orthoptera). Proceedings of the Zoological Institute, Russian Academy of Sciences 260, 3–224.Google Scholar
Gorochov, A.V. (2001) The higher classification, phylogeny and evolution of the superfamily Stenopelmatoidea. pp. 3–33 in Field, L.H. (Ed.) Biology of Wetas, King Crickets and Their Allies. Cambridge, MA, CABI Publishing.Google Scholar
Greenfield, M.D. (1997) Acoustic communication in Orthoptera. pp. 197–230 in Gangwere, S.K., Muralirangan, M.C. & Muralirangan, M. (Eds) The Bionomics of Grasshoppers, Katydids and Their Kin. Wallingford, CAB International.Google Scholar
Gregory, T.R. (2014) Animal Genome Size Database. Available online at http://www.genomesize.com.Google Scholar
Grimaldi, D. & Engel, M.S. (2005) Evolution of the Insects. New York: Cambridge University Press.Google Scholar
Gwynne, D.T. (1995) Phylogeny of the Ensifera (Orthoptera): a hypothesis supporting multiple origins of acoustical signalling, complex spermatophores and maternal care in crickets, katydids, and weta. Journal of Orthoptera Research 4, 203–218.Google Scholar
Gwynne, D.T. (2001) Katydids and Bush-Crickets: Reproductive Behavior and Evolution of the Tettigoniidae. Ithaca, NY, Cornell University Press.Google Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hanrahan, S.J. & Johnston, J.S. (2011) New genome size estimates of 134 species of arthropods. Chromosome Research 19, 809–823.Google Scholar
Heads, M. (2005) Dating nodes on molecular phylogenies: a critique of molecular biogeography. Cladistics 21, 62–78.Google Scholar
Ho, S.Y.W. (2007) Calibrating molecular estimates of substitution rates and divergence times in birds. Journal of Avian Biology 38, 409–414.Google Scholar
Ho, S.Y.W., Saarma, U., Barnett, R., Haile, J. & Shapiro, B. (2008) The effect of inappropriate calibration: three case studies in molecular ecology. PLos ONE 3, e1615.Google Scholar
Hugel, S. (2005) Red ecouverte du genre Pygacris a l^ıle de la Reunion: description du m^ale de P. descampi Kevan, 1975 (Orthoptera, Caelifera). Bulletin de la Société entomologique de France 110, 153–159.Google Scholar
Jost, M.C. & Shaw, K.L. (2006) Phylogeny of Ensifera (Hexapoda: Orthoptera) using three ribosomal loci, with implications for the evolution of acoustic communication. Molecular Phylogenetics and Evolution 38, 510–530.Google Scholar
Judd, W.W. (1947) A comparative study of the proventriculus of orthopteroid insects with reference to its use in taxonomy. Canadian Journal of Research 26, 93–159.Google Scholar
Kevan, D.K.M. (1982) Orthoptera. pp. 352–383 in Parker, S.P. (Ed) Synopsis and Classification of Living Organisms. New York, Mc Graw-Hill Book Company, Inc.Google Scholar
Kim, I., Cha, S.Y., Yoon, M.H., Hwang, J.S., Lee, S.M., Sohn, H.D. & Jin, B.R. (2005) The complete nucleotide sequence and gene organization of the mitochondrial genome of the oriental mole cricket, Gryllotalpa orientalis (Orthoptera: Gryllotalpidae). Gene 353, 155–168.CrossRefGoogle ScholarPubMed
Kodandaramaiah, U. (2011) Tectonic calibrations in molecular dating. Current Zoology 57, 116–124.CrossRefGoogle Scholar
Kristensen, N.P. (1991). Phylogeny of extant hexapods. In “The Insects of Australia: A Textbook for Students and Research Workers” (I. D. Naumann, P. B. Carne, J. F. Lawrence, E. S. Nielsen, J. P Spradberry, R. W. Taylor, M. J. Whitten, and M. J. Littlejohn, Eds.), 2nd ed., pp. 125–140. CSIRO, Melbourne University Press, Melbourne.Google Scholar
Lande, R. (1981) Models of speciation by sexual selection on polygenic traits. Proceedings of the National Academy of Sciences of the United States of America 78, 3721–3725.Google Scholar
Leavitt, J.R., Hiatt, K.D., Whiting, M.F. & Song, H. (2013) Searching for the optimal data partitioning strategy in mitochondrial phylogenomics: a phylogeny of Acridoidea (Insecta: Orthoptera: Caelifera) as a case study. Molecular Phylogenetics and Evolution 67, 494–508.Google Scholar
Lemmon, A.R., Emme, S.A. & Lemmon, E.M. (2012) Anchored hybrid enrichment for massively high-throughput phylogenomics. Systematic Biology 61, 727–744.CrossRefGoogle ScholarPubMed
Litzenberger, G. & Chapco, W. (2001) A molecular phylogeographic perspective on a fifty-year-old taxonomic issue in grasshopper systematics. Heredity 86, 54–59.Google Scholar
Liu, H. & Beckenbach, A.T. (1992) Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects. Molecular Phylogenetics and Evolution 1, 41–52.Google Scholar
Ma, C., Liu, C., Yang, P. & Kang*, L. (2009) The complete mitochondrial genomes of two band-winged grasshoppers, Gastrimargus marmoratus and Oedaleus asiaticus. BMC Genomics 10, 156.CrossRefGoogle ScholarPubMed
Magallon, S.A. (2004) Dating lineages: molecular and paleontological approaches to the temporal framework of clades. International Journal of Plant Science 165, S7–S21.Google Scholar
Mendelson, T.C. & Shaw, K.L. (2005) Rapid speciation in an arthropod. Nature 433, 375–376.CrossRefGoogle Scholar
Misof, B., Liu, S., Meusemann, K., Peters, R.S., Donath, A., Mayer, C., Frandsen, P.B., Ware, J., Flouri, T., Beutel, R.G., Niehuis, O., Petersen, M., Izquierdo-Carrasco, F., Wappler, T., Rust, J., Aberer, A.J., Aspöck, U., Aspöck, H., Bartel, D., Blanke, A., Berger, S., Böhm, A., Buckley, T.R., Calcott, B., Chen, J., Friedrich, F., Fukui, M., Fujita, M., Greve, C., Grobe, P., Gu, S., Huang, Y., Jermiin, L.S., Kawahara, A.Y., Krogmann, L., Kubiak, M., Lanfear, R., Letsch, H., Li, Y., Li, Z., Li, J., Lu, H., Machida, R., Mashimo, Y., Kapli, P., McKenna, D.D., Meng, G., Nakagaki, Y., Navarrete-Heredia, J.L., Ott, M., Ou, Y., Pass, G., Podsiadlowski, L., Pohl, H., von Reumont, B.M., Schütte, K., Sekiya, K., Shimizu, S., Slipinski, A., Stamatakis, A., Song, W., Su, X., Szucsich, N.U., Tan, M., Tan, X., Tang, M., Tang, J., Timelthaler, G., Tomizuka, S., Trautwein, M., Tong, X., Uchifune, T., Walzl, M.G., Wiegmann, B.M., Wilbrandt, J., Wipfler, B., Wong, T.K., Wu, Q., Wu, G., Xie, Y., Yang, S., Yang, Q., Yeates, D.K., Yoshizawa, K., Zhang, Q., Zhang, R., Zhang, W., Zhang, Y., Zhao, J., Zhou, C., Zhou, L., Ziesmann, T., Zou, S., Li, Y., Xu, X., Zhang, Y., Yang, H., Wang, J., Wang, J., Kjer, K.M. & Zhou, X. (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767.Google Scholar
Montealegre-Z, F. (2009) Scale effects and constraints for sound production in katydids (Orthoptera: Tettigoniidae): generator morphology constrains signal parameters. Journal of Evolutionary Biology 22, 355–366.Google Scholar
Otte, D. (1992) Evolution of cricket songs. Journal of Orthoptera Research 1, 25–49.Google Scholar
Pascoal, S., Cezard, T., Eik-Nes, A., Gharbi, K., Majewska, J., Payne, E., Ritchie, M.G., Zuk, M. & Bailey, N.W. (2014) Rapid convergent evolution in wild crickets. Current Biology 24, 1369–1374.Google Scholar
Pener, M.P. & Simpson, S.J. (2009) Locust phase polyphenism: an update. Advances in Insect Physiology 36, 1–286.Google Scholar
Perna, N.T. & Kocher, T.D. (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal Molecular Evolution 41, 353–358.Google Scholar
Piton, L.E. (1940) Paleontologie du gisement eocene de Menat (Puy-de-Dom) (Flore et Faune). Memoir Society History Nature Auvergne 1, 1–303.Google Scholar
Ragge, D.R. (1955) The Wing-Venation of the Orthoptera Saltatoria, With Notes on Dictyopteran Wing-Venation. London, British Museum of Natural History.Google Scholar
Ragge, D.R. (1977) Classification of the Tettigonioidea. Lyman Entomological Museum and Reserch Laboratory Memboir 4, 44–46.Google Scholar
Rambaut, A. (2007) FigTree, a graphical viewer of phylogenetic trees. Available online at http://tree.bio.ed.ac.uk/software/figtree.Google Scholar
Rambaut, A. & Charleston, M. (2001) TreeEdit: Phylogenetic Tree Editor v1.0 alpha 8.Google Scholar
Rambaut, A. & Drummond, A.J. (2002–2013b) TreeAnnotator v1.8.0.Google Scholar
Reyes, A., Gissi, C., Pesole, G. & Saccone, C. (1998) Asymmetrical directional mutation pressure in the mitochondrial genome of mammals. Molecular Biology Evolution 15, 957–966.Google Scholar
Roberts, H.R. (1941) A comparative study of the subfamilies of the Acrididae (Orthoptera) primarily on the bases of their phallic structures. Proceedings of the National Academy of Sciences of the United States of America 93, 201–246.Google Scholar
Robillard, T., Grandcolas, P. & Desutter-Grandcolas, L. (2007) A shift toward harmonics for high-frequency calling shown with phylogenetic study of frequency spectra in Eneopterinae crickets (Orthoptera, Grylloidea, Eneopteridae). Canadian Journal of Zoolog 85, 1264–1275.Google Scholar
Ronquist, F., Teslenko, M., Van der Mark, P., Ayres, D.L., Darling, A., H€ohna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
Russo, C.A.M., Takezaki, M. & Nei, M. (1996) Efficiencies of different genes and different tree-building methods in recovering a known vertebrate phylogeny. Molecular Biology Evolution 13, 525–536.Google Scholar
Saccone, C., De Giorgi, C., Gissi, C., Pesole, G. & Reyes, A. (1999) Evolutionary genomics in Metazoa: the mitochondrial DNA as a model system. Gene 238, 195–209.CrossRefGoogle ScholarPubMed
Saito, S., Tmura, K. & Aotsuka, T. (2005) Replication origin of mitochondrial DNA in insects. Genetics 171, 1695–1705.Google Scholar
Sambrook, J. & Russell, D.W. (2001) Molecular Cloning. 3rd edn. pp. 1949. New York, Cold Spring Harbor Laboratory Press.Google Scholar
Sanderson, M.J., Thorne, J.L., Wikstrom, N. & Bremer, K. (2004) Molecular evidence on plant divergence times. American Journal of Botany 91, 1656–1665.Google Scholar
Sharov, A.G. (1968) Phylogeny of the Orthopteroidea. Trudy Paleontological Insect 118, 1–216.Google Scholar
Shendure, J. & Ji, H. (2008) Next-generation DNA sequencing. Nature Biotechnology 26, 1135–1145.Google Scholar
Simon, C., Rati, F.F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.Google Scholar
Slifer, E.H. (1939) The internal genitalia of female Acridinae, Oedipodinae and Pauliniinae (Orthoptera, Acrididae). Journal of Morphology 65, 437–469.CrossRefGoogle Scholar
Song, H., Amédégnato, C., Cigliano, M.M., Desutter-Grandcolas, L., Heads, S.W., Huang, Y., Otte, D. & Whiting, M.F. (2015) 300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling. Cladistics 31, 621–651.Google Scholar
Springer, M.S., DeBry, R.W., Douady, C., Amrine, H.M., Madsen, O., de Jong, W.W. & Stanhope, M.J. (2001) Mitochondrial versus nuclear gene sequences in deep-level mammalian phylogeny reconstruction. Molecular Biology Evolution 18, 132–143. doi: 10.1093/oxfordjournals.molbev.a003787.Google Scholar
Storozhenko, S.Y. (1997) Fossil history and phylogeny of orthopteroid insects. pp. 59–82 in Gangwere, S.K., Muralirangan, M.C. & Muralirangan, M. (Eds) The Bionomics of Grasshoppers, Katydids and Their Kin. CAB International, Wallingford.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumaret, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Terry, M.D. & Whiting, M.F. (2005) Mantophasmatodea and phylogeny of the lower neopterous insects. Cladistics 21, 240–257.Google Scholar
Uvarov, B.P. (1966) Grasshoppers and Locusts, Vol. 1. Cambridge, UK, University Press.Google Scholar
Van Raay, T.J. & Crease, T.J. (1994) Partial mitochondrial DNA sequence of the crustacean Daphnia pulex. Current Genetics 25, 66–72.Google Scholar
Vickery, V.R. (1977) Axon ranking in Grylloidea and Gryllotalpoidea. Lyman Entomological Museum and Reserch Laboratory Memboir 4, 1–31.Google Scholar
Vickery, V.R. (1997) Classification of the Orthoptera (sensu stricto) or Caelifera. pp. 5–40 in Gangwere, S.K., Muralirangan, M.C. & Muralirangan, M. (Eds) The Bionomics of Grasshoppers, Katydids and Their Kin. CAB International, Wallingford.Google Scholar
Vickery, V.R. & Kevan, D.K.M. (1983) A monograph of the orthopteroid insects of Canada and adjacent regions. Lyman Ent. Mus. Res. Lab. 13, 216–237.Google Scholar
Wang, X., Fang, X., Yang, P., Jiang, X., Jiang, F., Zhao, D., Li, B., Cui, F., Wei, J., Ma, C., Wang, Y., He, J., Luo, Y., Wang, Z., Guo, X., Guo, W., Zhang, Y., Yang, M., Hao, S., Chen, B., Ma, Z., Yu, D., Xiong, Z., Zhu, Y., Fan, D., Han, L., Wang, B., Chen, Y., Wang, J., Yang, L., Zhao, W., Feng, Y., Chen, G., Lian, J., Li, Q., Huang, Z., Yao, X., Lv, N., Zhang, G., Li, Y., Zhu, B. & Kang, L. (2014) The locust genome provides insight into swarm formation and long-distance flight. Nature Communications 5, 2957.Google Scholar
West-Eberhard, M.J. (1983) Sexual selection, social competition, and speciation. Quarterly Review of Biology 58, 155–183.Google Scholar
Yang, F., Du, Y.Z., Wang, L.P., Cao, J.M. & Yu, W.W. (2011) The complete mitochondrial genome of the leafminer Liriomyza sativae (Diptera: Agromyzidae): great difference in the A plus;T-rich region compared to Liriomyza trifolii. Gene 485, 7–15.Google Scholar
Zardoya, R. & Meyer, A. (1996) Phylogenetic performance of mitochondrial protein-coding genes in resolving relationships among vertebrates. Molecular Biology Evolution 13, 933–942. doi: 10.1093/oxfordjournals.molbev.a025661.Google Scholar
Zeuner, F.E. (1939) Fossil Orthoptera Ensifera. London, British Museum (Natural History).Google Scholar
Zeuner, F.E. (1942) The Locustopsidae and the phylogeny of the Ackidodea (Orthopteea). Systematic Entomology 11, 1–18.Google Scholar
Zhang, D.X. & Hewitt, F.M. (1997) Insect mitochondrial control region: a review of its structure, evolution and usefulness in evolutionary studies. Biochemical Systematics and Ecology 25, 99–120.Google Scholar
Zhang, D.X., Szymura, J.M. & Hewitt, G.M. (1995) Evolution and structural conservation of the control region of insect mitochondrial DNA. Journal of Molecular Evolution 40, 382–391.Google Scholar
Zhang, H., Huang, Y., Lin, L., Wang, X. & Zheng, Z. (2013 a) The phylogeny of the Orthoptera (Insecta) as deduced from mitogenomic gene sequences. Zoological Studies 52, 37.Google Scholar
Zhang, H.L., Zeng, H.H., Huang, Y. & Zheng, Z.M. (2013 b) The complete mitochondrial genomes of three grasshoppers, Asiotmethis zacharjini, Filchnerella helanshanensis and Pseudotmethis rubimarginis (Orthoptera: Pamphagidae). Gene 517, 89–98.Google Scholar
Zhou, Z., Huang, Y. & Shi, F. (2007) The mitochndrial genome of Ruspolia dubia (Orthoptera: Conocephalidae) contains a short A+T rich region of 70 bp in length. Genome 50, 855–866.Google Scholar
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