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Population differentiation between Australian and Chinese Helicoverpa armigera occurs in distinct blocks on the Z-chromosome

Published online by Cambridge University Press:  05 February 2018

S.V. Song ,
C. Anderson ,
R.T. Good ,
S. Leslie ,
Y. Wu ,
J.G. Oakeshott  and
C. Robin
S.V. Song
Affiliation:
School of Biosciences, University of Melbourne, Victoria, Australia Bio21 Institute, Parkville, Victoria, Australia
C. Anderson
Affiliation:
MRC Human Genetics Unit, MRC Institute of Genetics and Molecular Medicine, University of Edinburgh, Western General Hospital, Edinburgh, UK Land and Water Flagship, Commonwealth Scientific and Industrial Research Organisation, Australian Capital Territory, Australia
R.T. Good
Affiliation:
School of Biosciences, University of Melbourne, Victoria, Australia Bio21 Institute, Parkville, Victoria, Australia
S. Leslie
Affiliation:
School of Biosciences, University of Melbourne, Victoria, Australia School of Mathematics and Statistics, University of Melbourne, Victoria, Australia Centre for Systems Genomics, University of Melbourne, Victoria, Australia
Y. Wu
Affiliation:
College of Plant Protection, Nanjing Agricultural University, Nanjing, China
J.G. Oakeshott
Affiliation:
Land and Water Flagship, Commonwealth Scientific and Industrial Research Organisation, Australian Capital Territory, Australia
C. Robin*
Affiliation:
School of Biosciences, University of Melbourne, Victoria, Australia Bio21 Institute, Parkville, Victoria, Australia
*
*Author for correspondence: Tel: +61 3 8344 2349 E-mail: [email protected]
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Abstract

Over the last 40 years, many types of population genetic markers have been used to assess the population structure of the pest moth species Helicoverpa armigera. While this species is highly vagile, there is evidence of inter-continental population structure. Here, we examine Z-chromosome molecular markers within and between Chinese and Australian populations. Using 1352 polymorphic sites from 40 Z-linked loci, we compared two Chinese populations of moths separated by 700 km and found virtually no population structure (n = 41 and n = 54, with <1% of variation discriminating between populations). The levels of nucleotide diversity within these populations were consistent with previous estimates from introns in Z-linked genes of Australian samples (π = 0.028 vs. 0.03). Furthermore, all loci surveyed in these Chinese populations showed a skew toward rare variants, with ten loci having a significant Tajima's D statistic, suggesting that this species could have undergone a population expansion. Eight of the 40 loci had been examined in a previous study of Australian moths, of which six revealed very little inter-continental population structure. However, the two markers associated with the Cyp303a1 locus that has previously been proposed to be a target of a selective sweep, exhibited allele structuring between countries. Using a separate dataset of 19 Australian and four Chinese moths, we scanned the molecular variation distributed across the entire Z-chromosome and found distinct blocks of differentiation that include the region containing Cyp303a1. We recommend some of these loci join those associated with insecticide resistance to form a set of genes best suited to analyzing population structure in this global pest.

Keywords

CYP303A1Helicoverpa armigera conferta
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 6 , December 2018 , pp. 817 - 830
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Copyright © Cambridge University Press 2018 

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References

Anderson, C.J., Tay, W.T., McGaughran, A., Gordon, K. & Walsh, T.K. (2016) Population structure and gene flow in the global pest, Helicoverpa armigera. Molecular Ecology 25(21), 5296–5311.Google Scholar
Arnemann, J.A., James, W.J., Walsh, T.K., Guedes, J.V.C., Smagghe, G., Castiglioni, E. & Tay, W.T. (2016) Mitochondrial DNA COI characterization of Helicoverpa armigera (Lepidoptera: Noctuidae) from Paraguay and Uruguay. Genetics and Molecular Research 15, 15028292.Google Scholar
Baird, N.A., Etter, P.D., Atwood, T.S., Currey, M.C., Shiver, A.L., Lewis, Z.A., Selker, E.U., Cresko, W.A. & Johnson, E.A. (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3, e3376, doi: 10.1371/journal.pone.0003376.Google Scholar
Battlay, P., Schmidt, J.M., Fournier-Level, A. & Robin, C. (2016) Genomic and transcriptomic associations identify a new insecticide resistance phenotype for the selective sweep at the Cyp6g1 locus of Drosophila melanogaster. G3 (Bethesda) 6, 2573–2581.Google Scholar
Behere, G., Tay, W., Russell, D., Heckel, D., Appleton, B., Kranthi, K. & Batterham, P. (2007) Mitochondrial DNA analysis of field populations of Helicoverpa armigera (Lepidoptera: Noctuidae) and of its relationship to H. zea. BMC Evolutionary Biology 7, 117.Google Scholar
Behere, G.T., Tay, W.T., Russell, D.A., Kranthi, K.R. & Batterham, P. (2013) Population genetic structure of the cotton bollworm Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in India as inferred from EPIC-PCR DNA markers. PLoS ONE 8, e53448. ISSN . doi: 10.1371/journal.pone.0053448.Google Scholar
Browning, S. R. & Browning, B. L. (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. The American Journal of Human Genetics 81, 1084–1097.Google Scholar
Buss, D. S. & Callaghan, A. (2008) Interaction of pesticides with p-glycoprotein and other ABC proteins: a survey of the possible importance to insecticide, herbicide and fungicide resistance. Pesticide Biochemistry and Physiology 90, 141–153.Google Scholar
Charlesworth, B., Coyne, J.A. & Barton, N.H. (1987) The relative rates of evolution of sex chromosomes and autosomes. American Naturalist 130, 113–146.Google Scholar
Cho, S., Mitchell, A., Mitter, C., Regier, J., Matthews, M. & Robertson, R. (2008) Molecular phylogenetics of heliothine moths (Lepidoptera: Noctuidae: Heliothinae), with comments on the evolution of host range and pest status. Systematic Entomology 33, 581–594.Google Scholar
Collart, M.A. & Panasenko, O.O. (2012) The CCR4-Not complex. Gene 492, 42–53.Google Scholar
Common, I. (1953) The Australian species of Heliothis (Lepidoptera: Noctuidae) and their pest status. Australian Journal of Zoology 1, 319–344.Google Scholar
Czepak, C., Albernaz, K.C., Vivan, L.M., Guimarães, H.O. & Carvalhais, T. (2013) First reported occurrence of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Brazil. Pesquisa Agropecuária Tropical 43, 110–113.Google Scholar
Daly, J.C. (1993) Ecology and genetics of insecticide resistance in Helicoverpa armigera: interactions between selection and gene flow. Genetica 90, 217–226.Google Scholar
Daly, J.C. & Fisk, J.H. (1998) Sex-linked inheritance of endosulphan resistance in Helicoverpa armigera. Heredity 81, 55–62.Google Scholar
Danecek, P., Auton, A., Abecasis, G., Albers, C.A., Banks, E., DePristo, M.A., Handsaker, R.E., Lunter, G., Marth, G.T., Sherry, S.T. & McVean, G. (2011) The variant call format and VCFtools. Bioinformatics 27, 2156–2158.Google Scholar
Earl, D.A. & vonHoldt, B.M. (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.Google Scholar
Elshire, R.J., Glaubitz, J.C., Sun, Q., Poland, J.A., Kawamoto, K., Buckler, E.S. & Mitchell, S.E. (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6, e19379. doi: 10.1371/journal.pone.0019379.Google Scholar
Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.Google Scholar
Falush, D., Wirth, T., Linz, B., Pritchard, J.K., Stephens, M., Kidd, M., Blaser, M.J., Graham, D.Y., Vacher, S., Perez-Perez, G.I., Yamaoka, Y., Mégraud, F., Otto, K., Reichard, U., Katzowitsch, E., Wang, X., Achtman, M. & Suerbaum, S. (2003) Traces of human migrations in Helicobacter pylori populations. Science 299, 1582–1585.Google Scholar
Fitt, G.P. (1994) Cotton pest management: Part 3. An Australian perspective. Annual Review of Entomology 39, 543–562.Google Scholar
Gahan, L.J., Gould, F. & Heckel, D.G. (2001) Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293, 857–860.Google Scholar
Gahan, L.J., Pauchet, Y., Vogel, H. & Heckel, D.G. (2010) An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1ac toxin. PLoS Genetics 6, e1001248. doi: 10.1371/ journal.pgen.1001248.Google Scholar
Garud, N.R., Messer, P.W., Buzbas, E.O. & Petrov, D.A. (2015) Recent selective sweeps in North American Drosophila melanogaster show signatures of soft sweeps. PLoS Genetics 11, e1005004. doi: 10.1371/journal.pgen. 1005004.Google Scholar
Gilles, A., Meglécz, E., Pech, N., Ferreira, S., Malausa, T. & Martin, J.F. (2011) Accuracy and quality assessment of 454 GS-FLX Titanium pyrosequencing. BMC Genomics 12, 245.Google Scholar
Gordon, K.H.J., Tay, W.T., Collinge, D., Williams, A. & Batterham, P. (2010) Genetics and molecular biology of the major crop pest genus Helicoverpa. pp. 219–238 in Goldsmith, M.R. & Marec, F. (Eds) Molecular Biology and Genetics of the Lepidoptera. CRC Press, Boca Raton, FL, USA ISBN 978-1-4200-6020-1.Google Scholar
Goudet, J. (2005). HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Molecular Ecology Resources 5, 184–186.Google Scholar
Gouy, M., Guindon, S. & Gascuel, O. (2010) Seaview version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221–224.Google Scholar
Green, R.E., Krause, J., Briggs, A.W., Maricic, T., Stenzel, U., Kircher, M., Patterson, N., Li, H., Zhai, W., Fritz, M.H.Y., Hansen, N.F., Durand, E.Y., Malaspinas, A.S., Jensen, J.D., Marques-Bonet, T., Alkan, C., Prüfer, K., Meyer, M., Burbano, H.A., Good, J.M., Schultz, R., Aximu-Petri, A., Butthof, A., Höber, B., Höffner, B., Siegemund, M., Weihmann, A., Nusbaum, C., Lander, E.S., Russ, C., Novod, N., Affourtit, J., Egholm, M., Verna, C., Rudan, P., Brajkovic, D., Kucan, , Gušic, I., Doronichev, V.B., Golovanova, L.V., Lalueza-Fox, C., de la Rasilla, M., Fortea, J., Rosas, A., Schmitz, R.W., Johnson, P.L.F., Eichler, E.E., Falush, D., Birney, E., Mullikin, J.C., Slatkin, M., Nielsen, R., Kelso, J., Lachmann, M., Reich, D. & Pääbo, S. (2010) A draft sequence of the Neandertal genome. Science 328, 710–722.Google Scholar
Head, D.J., McCaffery, A.R. & Callaghan, A. (1998) Novel mutations in the para-homologous sodium channel gene associated with phenotypic expression of nerve insensitivity resistance to pyrethroids in Heliothine lepidoptera. Insect Molecular Biology 7, 191–196.Google Scholar
Hill, W.G. & Weir, B.S. (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theoretical Population Biology 33, 54–78.Google Scholar
Jombart, T. & Ahmed, I. (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071.Google Scholar
Joußen, N., Agnolet, S., Lorenz, S., Schöne, S.E., Ellinger, R., Schneider, B. & Heckel, D.G. (2012) Resistance of Australian Helicoverpa armigera to fenvalerate is due to the chimeric P450 enzyme CYP337B3. Proceedings of the National Academy of Sciences 109, 15206–15211.Google Scholar
Kamvar, Z.N., Tabima, J.F. & Grünwald, N.J. (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281. ISSN . doi: 10.7717/peerj.281.Google Scholar
Lakey, A., Labeit, S., Gautel, M., Ferguson, C., Barlow, D.P., Leonard, K. & Bullard, B. (1993) Kettin, a large modular protein in the Z-disc of insect muscles. The EMBO Journal 12, 2863–2871.Google Scholar
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.Google Scholar
Leite, N.A., Alves-Pereira, A., Corrêa, A.S., Zucchi, M.I. & Omoto, C. (2014) Demographics and genetic variability of the New World bollworm (Helicoverpa zea) and the Old World bollworm (Helicoverpa armigera) in Brazil. PLoS ONE 9, e113286. ISSN . doi: 10.1371/journal.pone. 0113286.Google Scholar
Mallet, J., Korman, A., Heckel, D.G. & King, P. (1993) Biochemical genetics of Heliothis and Helicoverpa (Lepidoptera: Noctuidae) and evidence for a founder event in Helicoverpa zea. Annals of the Entomological Society of America 86, 189–197.Google Scholar
Martinez-Torres, D., Devonshire, A.L. & Williamson, M.S. (1997) Molecular studies of knockdown resistance to pyrethroids: cloning of domain II sodium channel gene sequences from insects. Pesticide Science 51, 265–270.Google Scholar
Mastrangelo, T., Paulo, D.F., Bergamo, L.W., Morais, E.G.F., Silva, M., Bezerra-Silva, G. & Azeredo-Espin, A.M.L. (2014) Detection and genetic diversity of a heliothine invader (Lepidoptera: Noctuidae) from north and northeast of Brazil. Journal of Economic Entomology 107, 970–980.Google Scholar
Matthews, M. (1999) Heliothine moths of Australia: a guide to pest bollworms and related noctuid groups. Monographs on Australian Lepidoptera, Vol. 7. Melbourne, CSIRO Publishing. ISBN 0-643-06305-6.Google Scholar
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M. & DePristo, M.A. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research 20, 1297–1303.Google Scholar
Mitchell, A. & Gopurenko, D. (2016) DNA barcoding the Heliothinae (Lepidoptera: Noctuidae) of Australia and utility of DNA barcodes for pest identification in Helicoverpa and relatives. PLoS ONE 11, e0160895. ISSN . doi: 10.1371/journal.pone.0160895.Google Scholar
Murúa, M.G., Scalora, F.S., Navarro, F.R., Cazado, L.E., Casmuz, A., Villagrán, M.E., Lobos, E. & Gastaminza, G. (2014) First record of Helicoverpa armigera (Lepidoptera: Noctuidae) in Argentina. Florida Entomologist 97, 854–856.Google Scholar
Nibouche, S., Bues, R., Toubon, J.F. & Poitout, S. (1998) Allozyme polymorphism in the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae): comparison of African and European populations. Heredity 80, 438–445.Google Scholar
Nielsen, R. (2005) Molecular signatures of natural selection. Annual Review Of Genetics 39, 197–218.Google Scholar
Pearce, S.L., Clarke, D.F., East, P.D., Elfekih, S., Gordon, K.H.J., Jermiin, L.S., McGaughran, A., Oakeshott, J.G., Papanikolaou, A., Perera, O.P., Rane, R.V., Richards, S., Tay, W.T., Walsh, T.K., Anderson, A., Anderson, C.J., Asgari, S., Board, P.G., Bretschneider, A., Campbell, P.M., Chertemps, T., Christeller, J.T., Coppin, C.W., Downes, S.J., Duan, G., Farnsworth, C.A., Good, R.T., Han, L.B., Han, Y.C., Hatje, K., Horne, I., Huang, Y.P., Hughes, D.S.T., Jacquin-Joly, E., James, W., Jhangiani, S., Kollmar, M., Kuwar, S.S., Li, S., Liu, N.Y., Maibeche, M.T., Miller, J.R., Montagne, N., Perry, T., Qu, J., Song, S.V., Sutton, G.G., Vogel, H., Walenz, B.P., Xu, W., Zhang, H.J., Zou, Z., Batterham, P., Edwards, O.R., Feyereisen, R., Gibbs, R.A., Heckel, D.G., McGrath, A., Robin, C., Scherer, S.E., Worley, K.C. and Wu, Y.D. (2017) Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biology 15, 63.Google Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.Google Scholar
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A., Bender, D., Maller, J., Sklar, P., De Bakker, P.I., Daly, M.J. & Sham, P. C. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics 81, 559–575.Google Scholar
Rašić, G., Filipović, I., Weeks, A. R. & Hoffmann, A. A. (2014) Genome-wide SNPs lead to strong signals of geographic structure and relatedness patterns in the major arbovirus vector, Aedes aegypti. BMC Genomics 15, 275.Google Scholar
R Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Reinhardt, J.A., Kolaczkowski, B., Jones, C.D., Begun, D.J. & Kern, A.D. (2014) Parallel geographic variation in Drosophila melanogaster. Genetics 197, 361–373.Google Scholar
Rohland, N. & Reich, D. (2012) Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Research 22, 939–946.Google Scholar
Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.Google Scholar
Sackton, T.B., Corbett-Detig, R.B., Nagaraju, J., Vaishna, L., Arunkumar, K.P. & Hartl, D.L. (2014) Positive selection drives faster-Z evolution in silkmoths. Evolution 68, 2331–2342.Google Scholar
Slatkin, M. (2008) Linkage disequilibrium – understanding the evolutionary past and mapping the medical future. Nature Reviews Genetics 9, 477–485.Google Scholar
Song, S.V., Downes, S., Parker, T., Oakeshott, J.G. & Robin, C. (2015) High nucleotide diversity and limited linkage disequilibrium in Helicoverpa armigera facilitates the detection of a selective sweep. Heredity (Edinb) 115, 460–470.Google Scholar
Sosa-Gómez, D.R., Specht, A., Paula-Moraes, S.V., Lopes-Lima, A., Yano, S.A.C., Micheli, A., Morais, E.G.F., Gallo, P., Pereira, P.R.V.S., Sal-vadori, J.R., Botton, M., Zenker, M.M. & Azevedo-Filho, W.S. (2016) Timeline and geographical distribution of Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae: Heliothinae) in Brazil. Revista Brasileira de Entomologia 60, 101–104.Google Scholar
Srinivas, R., Udikeri, S. S., Jayalakshmi, S. K. & Sreeramulu, K. (2004) Identification of factors responsible for insecticide resistance in Helicoverpa armigera. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 137, 261–269.Google Scholar
Staubach, F., Lorenc, A., Messer, P.W., Tang, K., Petrov, D.A. & Tautz, D. (2012) Genome patterns of selection and introgression of haplotypes in natural populations of the house mouse (Mus musculus). PLoS Genetics 8, e1002891.Google Scholar
Tabashnik, B.E., Gould, F. & Carrière, Y. (2004) Delaying evolution of insect resistance to transgenic crops by decreasing dominance and heritability. Journal of Evolutionary Biology 17, 904–912.Google Scholar
Tay, W., Behere, G., Batterham, P. & Heckel, D. (2010) Generation of microsatellite repeat families by RTE retrotransposons in lepidopteran genomes. BMC Evolutionary Biology 10, 144.Google Scholar
Tay, W.T., Soria, M.F., Walsh, T., Thomazoni, D., Silvie, P., Behere, G.T., Anderson, C. & Downes, S. (2013) A brave new world for an Old World pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS ONE 8, e80134. doi: 10.1371/journal.pone.0080134.Google Scholar
Vicoso, B. & Charlesworth, B. (2006) Evolution on the X chromosome: unusual patterns and processes. Nature Reviews Genetics 7, 645–653.Google Scholar
Wallar, B.J. & Alberts, A.S. (2003) The formins: active scaffolds that remodel the cytoskeleton. Trends in Cell Biology 13, 435–446.Google Scholar
Wickham, H. (2009) ggplot2: Elegant Graphics for Data Analysis, vol. 1. New York, Springer, p. 3.Google Scholar
Zhang, D.X. (2004) Lepidopteran microsatellite DNA: redundant but promising. Trends in Ecology & Evolution 19, 507–509.Google Scholar
Zhou, X., Faktor, O., Applebaum, S.W. & Coll, M. (2000) Population structure of the pestiferous moth Helicoverpa armigera in the Eastern Mediterranean using RAPD analysis. Heredity 85, 251–256.Google Scholar
Zhu, L., Tatsuke, T., Li, Z., Mon, H., Xu, J., Lee, J.M. & Kusakabe, T. (2012) Molecular cloning of BmTUDOR-SN and analysis of its role in the RNAi pathway in the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Applied Entomology and Zoology 47, 207–215.Google Scholar
Zhu, L., Tatsuke, T., Mon, H., Li, Z., Xu, J., Lee, J.M. & Kusakabe, T. (2013) Characterization of Tudor-SN-containing granules in the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology 43, 664–674.Google Scholar
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