Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-28T05:36:08.090Z Has data issue: false hasContentIssue false

Rapid genetic turnover in populations of the insect pest Bemisia tabaci Middle East: Asia Minor 1 in an agricultural landscape

Published online by Cambridge University Press:  15 March 2012

A. Dinsdale*
Affiliation:
The University of Queensland, School of Biological Sciences, Queensland 4072, Australia CSIRO Ecosystem Sciences, GPO Box 2583, Brisbane, Queensland 4001, Australia
N.A. Schellhorn
Affiliation:
CSIRO Ecosystem Sciences, GPO Box 2583, Brisbane, Queensland 4001, Australia
P. De Barro
Affiliation:
CSIRO Ecosystem Sciences, GPO Box 2583, Brisbane, Queensland 4001, Australia
Y.M. Buckley
Affiliation:
The University of Queensland, School of Biological Sciences, Queensland 4072, Australia CSIRO Ecosystem Sciences, GPO Box 2583, Brisbane, Queensland 4001, Australia
C. Riginos
Affiliation:
The University of Queensland, School of Biological Sciences, Queensland 4072, Australia
*
*Author for correspondence Postal address: CSIRO Ecosystem Sciences, GPO Box 2583, Brisbane, Queensland, Australia4001 Phone: +61 40 225 0557 E-mail: [email protected]

Abstract

Organisms differ greatly in dispersal ability, and landscapes differ in amenability to an organism's movement. Thus, landscape structure and heterogeneity can affect genetic composition of populations. While many agricultural pests are known for their ability to disperse rapidly, it is unclear how fast and over what spatial scale insect pests might respond to the temporally dynamic agricultural landscapes they inhabit. We used population genetic analyses of a severe crop pest, a member of the Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidea) cryptic species complex known as Middle East-Asia Minor 1 (commonly known as biotype B), to estimate spatial and temporal genetic diversity over four months of the 2006–2007 summer growing season. We examined 559 individuals from eight sites, which were scored for eight microsatellite loci. Temporal genetic structure greatly exceeded spatial structure. There was significant temporal change in local genetic composition from the beginning to the end of the season accompanied by heterozygote deficits and inbreeding. This temporal structure suggests entire cohorts of pests can occupy a large and variable agricultural landscape but are rapidly replaced. These rapid genetic fluctuations reinforce the concept that agricultural landscapes are dynamic mosaics in time and space and may contribute to better decisions for pest and insecticide resistance management.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bezemer, T.M. & Jones, T.H. (1998) Plant-insect herbivore interactions in elevated atmospheric CO2: quantitative analyses and guild effects. Oikos 82, 212222.CrossRefGoogle Scholar
Bossart, J.L. & Prowell, D.P. (1998) Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends in Ecology & Evolution 13, 202206.CrossRefGoogle ScholarPubMed
Bradley, J.R. Jr, (1993) Influence of habitat on the pest status and management of Heliothis species on cotton in the southern United States. pp. 375391in Kim, K.C. & McPheron, B.A. (Eds) Evolution of Insect Pests: Patterns of Variation. New York, USA, John Wiley & Sons.Google Scholar
Byrne, D.N. (1999) Migration and dispersal by the sweet potato whitefly, Bemisia tabaci. Agricultural and Forest Meteorology 97, 309316.CrossRefGoogle Scholar
Byrne, D.N. & Miller, W.B. (1990) Carbohydrate and amino acid composition of phloem sap and honeydew produced by Bemisia tabaci. Journal of Insect Physiology 36, 433439.CrossRefGoogle Scholar
Byrne, D.N., Rathman, R.J., Orum, T.V. & Palumbo, J.C. (1996) Localized migration and dispersal by the sweet potato whitefly Bemisia tabaci. Oecologia 105, 320328.CrossRefGoogle ScholarPubMed
Castle, S.J. (1999) Agricultural intensification and pest outbreaks: a reappraisal of events in the Sudan Gezira. Annals of the Entomological Society of America 92, 840852.CrossRefGoogle Scholar
Coviella, C.E. & Trumble, J.T. (1999) Effects of elevated atmospheric carbon dioxide on insect-plant interactions. Conservation Biology 13, 700712.CrossRefGoogle Scholar
De Barro, P.J. (2005) Genetic structure of the whitefly Bemisia tabaci in the Asia-Pacific region revealed using microsatellite markers. Molecular Ecology 14, 36953718.CrossRefGoogle ScholarPubMed
De Barro, P.J. & Driver, F. (1997) Use of RAPD PCR to distinguish the B biotype from other biotypes of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Australian Journal of Entomology 36, 149152.CrossRefGoogle Scholar
De Barro, P.J., Sherratt, T.N., Carvalho, G.R., Nicol, D., Iyengar, A. & Maclean, N. (1995a) Geographic and microgeographic genetic differentiation in two aphid species over southern England using the multilocus (GATA)4 probe. Molecular Ecology 4, 375382.CrossRefGoogle Scholar
De Barro, P.J., Sherratt, T.N., Brookes, C.P., David, O. & Maclean, N. (1995b) Spatial and temporal genetic variation in British field populations of the grain aphid Sitobion avenae (F) (Hemiptera: Aphididae) studied using RAPD-PCR. Proceedings of the Royal Society, Series B: Biological Sciences 262, 321327.Google ScholarPubMed
De Barro, P.J., Scott, K.D., Graham, G.C., Lange, C.L. & Schutze, K. (2003) Isolation and characterization of microsatellite loci in Bemisia tabaci. Molecular Ecology Notes 3, 4043.CrossRefGoogle Scholar
De Barro, P.J., Liu, S.S., Boykin, L.M. & Dinsdale, A.B. (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 119.CrossRefGoogle ScholarPubMed
Delatte, H., David, P., Granier, M., Lett, J.M., Goldbach, R., Peterschmitt, M. & Reynaud, B. (2006) Microsatellites reveal extensive geographical, ecological and genetic contacts between invasive and indigenous whitefly biotypes in an insular environment. Genetical Research 87, 109124.CrossRefGoogle Scholar
Dinsdale, A., Cook, L., Riginos, C., Buckley, Y.M. & De Barro, P. (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America 103, 196208.CrossRefGoogle Scholar
Dittrich, V., Ernst, G.H., Ruesch, O. & Uk, S. (1990) Resistance mechanisms in sweet potato whitefly (Homoptera: Aleyrodidae) populations from Sudan, Turkey, Guatemala, and Nicaragua. Journal of Economic Entomology 83, 16651670.CrossRefGoogle Scholar
Drake, B.G., GonzalezMeler, M.A. & Long, S.P. (1997) More efficient plants: a consequence of rising atmospheric CO2? Annual Review of Plant Physiology and Plant Molecular Biology 48, 609639.CrossRefGoogle ScholarPubMed
Duffus, J.E. (1987) Whitefly transmission of plant viruses. Current Topics in Vector Research 4, 7391.Google Scholar
Duffus, J.E. (1996) Whitefly borne virus. pp. 255263in Gerling, D. & Mayer, R.T. (Eds) Bemisia: 1995 Taxonomy, Biology, Damage, Control and Management. Andover, UK, Intercept.Google Scholar
Ellsworth, P.C., Dennehy, T.J. & Nichols, R.L. (1996) Whitefly management in Arizona cotton 1996. Tucson, AZ, USA, University of Arizona, College of Agriculture and Life Sciences, Cooperative Extension.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, 26112620.CrossRefGoogle ScholarPubMed
Eveleens, K.G. (1983) Cotton-insect control in the Sudan Gezira: analysis of a crisis. Crop Protection 2, 273287.CrossRefGoogle Scholar
Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479491.CrossRefGoogle ScholarPubMed
Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 15671587.CrossRefGoogle ScholarPubMed
Flint, H.M., Naranjo, S.E., Leggett, J.E. & Henneberry, T.J. (1996) Cotton water stress, arthropod dynamics, and management of Bemisia tabaci (Homoptera: Aleyrodidae). Journal of Economic Entomology 89, 12881300.CrossRefGoogle Scholar
Fuentes-Contreras, E., Espinoza, J.L., Lavandero, B. & Ramírez, C.C. (2008) Population genetic structure of codling moth (Lepidoptera: Tortricidae) from apple orchards in central Chile. Journal of Economic Entomology 101, 190198.CrossRefGoogle ScholarPubMed
Goudet, J. (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86, 485486.CrossRefGoogle Scholar
Gunning, R.V., Byrne, F.J., Conde, B.D., Connelly, M.I., Hergstrom, K. & Devonshire, A.L. (1995) First report of B biotype Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) in Australia. Journal of the Australian Entomological Society 34, 116120.CrossRefGoogle Scholar
Han, Q. & Caprio, M.A. (2004) Evidence from genetic markers suggests seasonal variation in dispersal in Heliothis virescens (Lepidoptera: Noctuidae). Environmental Entomology 33, 12231231.CrossRefGoogle Scholar
Hirano, K., Budiyanto, E. & Winarni, S. (1993) Biological characteristics and forecasting outbreaks of the whitefly, Bemisia tabaci, a vector of virus diseases in soybean fields. Asian Studies on the Pacific Coast Food and Fertiliser Technology Centre. Technical Bulletin 135, Taipei City, Taiwan, ASPAC.Google Scholar
Hu, J., De Barro, P., Zhao, H., Wang, J., Nardi, F. & Liu, S.S. (2011) An extensive field survey combined with a phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE 6, 19.Google ScholarPubMed
Kennedy, G.G. & Storer, N.P. (2000) Life systems of polyphagous arthropod pests in temporally unstable cropping systems. Annual Review of Entomology 45, 467493.CrossRefGoogle ScholarPubMed
Lavandero, B., Miranda, M., Ramirez, C.C. & Fuentes-Contreras, E. (2009) Landscape composition modulates population genetic structure of Eriosoma lanigerum (Hausmann) on Malus domestica Borkh in central Chile. Bulletin of Entomological Research 99, 97105.CrossRefGoogle Scholar
Loxdale, H.D., Hardie, J., Halbert, S., Foottit, R., Kidd, N.A.C. & Carter, C.I. (1993) The relative importance of short range and long range movement of flying aphids. Biological Reviews of the Cambridge Philosophical Society 68, 291311.CrossRefGoogle Scholar
Massonnet, B. & Weisser, W.W. (2004) Patterns of genetic differention between populations of the specialized herbivore Macrosiphoniella tanacetaria (Homoptera: Aphididae). Heredity 93, 577584.CrossRefGoogle ScholarPubMed
Oliveira, M.R.V., Henneberry, T.J. & Anderson, P. (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Protection 20, 709723.CrossRefGoogle Scholar
Palumbo, J.C., Horowitz, A.R. & Prabhaker, N. (2001) Insecticidal control and resistance management for Bemisia tabaci. Crop Protection 20, 739765.CrossRefGoogle Scholar
Peakall, R. & Smouse, P.E. (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288295.CrossRefGoogle Scholar
Perring, T.M. (2001) The Bemisia tabaci species complex. Crop Protection 20, 725737.CrossRefGoogle Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945959.CrossRefGoogle ScholarPubMed
Qiu, B.L., Ren, S.X., Mandour, N. S. & Wen, S.Y. (2006a) Population differentiation of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) by DNA polymorphism in China. Journal of Entomological Research (New Delhi) 30, 16.Google Scholar
Qiu, B.L., Ren, S.X., Wen, S.Y. & Mandour, S.N. (2006b) Population differentiation of three biotypes of Bemisia tabaci in China by DNA polymorphism. Journal of South China Agricultural University 27, 2933.Google Scholar
Raymond, M. & Rousset, F. (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248249.CrossRefGoogle Scholar
Riley, D.G. & Ciomperlik, M.A. (1997) Regional population dynamics of whitefly (Homoptera: Aleyrodidae) and associated parasitoids (Hymenoptera: Aphelinidae). Environmental Entomology 26, 10491055.CrossRefGoogle Scholar
Schellhorn, N.A., Macfadyen, S., Bianchi, F.J.J.A., Williams, D.G. & Zalucki, M.P. (2008) Managing ecosystem services in broadacre landscapes: what are the appropriate spatial scales? Australian Journal of Experimental Agriculture 48, 15491559.CrossRefGoogle Scholar
Schuelke, M. (2000) An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18, 233234.CrossRefGoogle ScholarPubMed
Simon, B., Cenis, J.L., Demichelis, S., Rapisarda, C., Caciagli, P. & Bosco, D. (2003) Survey of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in Italy with the description of a new biotype (T) from Euphorbia characias. Bulletin of Entomological Research 93, 259264.CrossRefGoogle ScholarPubMed
Storfer, A., Murphy, M.A., Evans, J.S., Goldberg, C.S., Robinson, S., Spear, S.F., Dezzani, R., Delmelle, E., Vierling, L. & Waits, L.P. (2007) Putting the 'landscape' in landscape genetics. Heredity 98, 128142.CrossRefGoogle ScholarPubMed
Sunnucks, P., DeBarro, P.J., Lushai, G., Maclean, N. & Hales, D. (1997) Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Molecular Ecology 6, 10591073.CrossRefGoogle ScholarPubMed
Sutherst, R.W. (2001) The biotic potential of Bemisia tabaci SLW around cotton growing regions of Australia in CSIRO. A Report to the Cotton Research and Development Corporation (CRDC).Google Scholar
Trumble, J.T. & Butler, C.D. (2009) Climate change will exacerbate California's insect pest problems. California Agriculture 63, 7378.CrossRefGoogle Scholar
Tsagkarakou, A. & Roditakis, N. (2003) Isolation and characterization of microsatellite loci in Bemisia tabaci (Hemiptera: Aleyrodidae). Molecular Ecology Notes 3, 196198.CrossRefGoogle Scholar
Tsagkarakou, A., Tsigenopoulos, C.S., Gorman, K., Lagnel, J. & Bedford, I.D. (2007) Biotype status and genetic polymorphism of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) in Greece: mitochondrial DNA and microsatellites. Bulletin of Entomological Research 97, 2940.CrossRefGoogle ScholarPubMed
Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. (2004) MICRO–CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535538.CrossRefGoogle Scholar
Vandergast, A.G., Bohonak, A.J., Weissman, D.B. & Fisher, R.N. (2007) Understanding the genetic effects of recent habitat fragmentation in the context of evolutionary history: phylogeography and landscape genetics of a southern California endemic jerusalem cricket (Orthoptera: Stenopelmatidae: Stenopelmatus). Molecular Ecology 16, 977992.CrossRefGoogle ScholarPubMed
Vorburger, C. (2006) Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae. Journal of Evolutionary Biology 19, 97107.CrossRefGoogle ScholarPubMed
Walsh, P.S., Metzger, D.A. & Higuchi, R. (1991) Chelex 100 as a medium for simple extraction of DNA for PCR based typing from forensic material. Biotechniques 10, 506513.Google ScholarPubMed
Wang, K.H. & Tsai, J.H. (1996) Temperature effect on development and reproduction of silverleaf whitefly (Homoptera: Aleyrodidae). Annals of the Entomological Society of America 89, 375384.CrossRefGoogle Scholar
Wang, Y.M., Shen, Z.R., Gao, L.W. & Zhang, G.L. (2008) Seasonal genetic structure in Beijing populations of the grain aphid Sitobion miscanthi (Takahashi): an investigation using microsatellites. Applied Entomology and Zoology 43, 97103.CrossRefGoogle Scholar
Wilson, A.C.C., Sunnucks, P., Blackman, R.L. & Hales, D.F. (2002) Microsatellite variation in cyclically parthenogenetic populations of Myzus persicae in south-eastern Australia. Heredity 88, 258266.CrossRefGoogle ScholarPubMed
Zang, L., Jiang, T., Xu, J., Liu, S. & Zhang, Y. (2006) SCAR molecular markers of the B biotype and two non-B populations of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). Chinese Journal of Agricultural Biotechnology 3, 189194.Google Scholar
Zhang, L.P., Zhang, Y.J., Zhang, W.J., Wu, Q.J., Xu, B.Y. & Chu, D. (2005) Analysis of genetic diversity among different geographical populations and determination of biotypes of Bemisia tabaci in China. Journal of Applied Entomology 129, 121128.CrossRefGoogle Scholar