Hostname: page-component-7d684dbfc8-dh8xm Total loading time: 0 Render date: 2023-09-29T12:29:44.698Z Has data issue: false Feature Flags: { "corePageComponentGetUserInfoFromSharedSession": true, "coreDisableEcommerce": false, "coreDisableSocialShare": false, "coreDisableEcommerceForArticlePurchase": false, "coreDisableEcommerceForBookPurchase": false, "coreDisableEcommerceForElementPurchase": false, "coreUseNewShare": true, "useRatesEcommerce": true } hasContentIssue false
  • English
  • Français

Genetic variation of the greenhouse whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae), among populations from Serbia and neighbouring countries, as inferred from COI sequence variability

Published online by Cambridge University Press:  24 March 2014

M. Prijović ,
M. Škaljac ,
T. Drobnjaković ,
K. Žanić ,
P. Perić ,
D. Marčić  and
J. Puizina
M. Prijović
Affiliation:
Institute of Pesticides and Environmental Protection, Banatska 31b, 11080 Belgrade, Serbia
M. Škaljac
Affiliation:
Department of Applied Sciences, Institute for Adriatic Crops, Put Duilova 11, 21000 Split, Croatia
T. Drobnjaković
Affiliation:
Institute of Pesticides and Environmental Protection, Banatska 31b, 11080 Belgrade, Serbia
K. Žanić
Affiliation:
Department of Applied Sciences, Institute for Adriatic Crops, Put Duilova 11, 21000 Split, Croatia
P. Perić
Affiliation:
Institute of Pesticides and Environmental Protection, Banatska 31b, 11080 Belgrade, Serbia
D. Marčić
Affiliation:
Institute of Pesticides and Environmental Protection, Banatska 31b, 11080 Belgrade, Serbia
J. Puizina*
Affiliation:
Department of Biology, Faculty of Science, University of Split, Teslina 12, 21000 Split, Croatia
*
*Author for correspondence Phone: 00385 21 385 133 Fax: 00385 21 384 086 E-mail: puizina@pmfst.hr
Get access Rights & Permissions [Opens in a new window]

Abstract

The greenhouse whitefly Trialeurodes vaporariorum Westwood, 1856 (Hemiptera: Aleyrodidae) is an invasive and highly polyphagous phloem-feeding pest of vegetables and ornamentals. Trialeurodes vaporariorum causes serious damage due to direct feeding and transmits several important plant viruses. Excessive use of insecticides has resulted in significantly reduced levels of susceptibility of various T. vaporariorum populations. To determine the genetic variability within and among populations of T. vaporariorum from Serbia and to explore their genetic relatedness with other T. vaporariorum populations, we analysed the mitochondrial cytochrome c oxidase I (COI) sequences of 16 populations from Serbia and six neighbouring countries: Montenegro (three populations), Macedonia (one population) and Croatia (two populations), for a total of 198 analysed specimens. A low overall level of sequence divergence and only five variable nucleotides and six haplotypes were found. The most frequent haplotype, H1, was identified in all Serbian populations and in all specimens from distant localities in Croatia and Macedonia. The COI sequence data that was retrieved from GenBank and the data from our study indicated that H1 is the most globally widespread T. vaporariorum haplotype. A lack of spatial genetic structure among the studied T. vaporariorum populations, as well as two demographic tests that we performed (Tajima's D value and Fu's Fs statistics), indicate a recent colonisation event and population growth. Phylogenetic analyses of the COI haplotypes in this study and other T. vaporariorum haplotypes that were retrieved from GenBank were performed using Bayesian inference and median-joining (MJ) network analysis. Two major haplogroups with only a single unique nucleotide difference were found: haplogroup 1 (containing the five Serbian haplotypes and those previously identified in India, China, the Netherlands, the United Kingdom, Morocco, Reunion and the USA) and haplogroup 3 (containing the single Serbian haplotype H3 and haplotypes from Costa Rica, the USA and Spanish Canary Islands). Collectively, our data indicate a rather limited value of COI as a genetic marker for discrimination between different T. vaporariorum populations in the investigated area. Possible explanations for the observed lack of COI sequence variability, such as specific genetics of biological invasion and/or the influence of bacterial symbionts that manipulate insect reproduction, are discussed.

Keywords

Trialeurodes vaporariorumwhitefliescytochrome c oxidase ICOIpopulation geneticsbiological invasionhaplotypesmolecular phylogenyphylogeography
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 3 , June 2014 , pp. 357 - 366
Copyright
Copyright © Cambridge University Press 2014 

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

Akaike, H. (1974) A new look at the statistical model identification. IEEE Transaction on Automatic Control 19, 716–723.CrossRefGoogle Scholar
Alba, V.R. (1950) Viropatogenos. pp. 52–58 in Conferencia Latinoamericana de Especialistas en Papa. Colombia, Bogota.Google Scholar
Albajes, R., Lodovica Gullino, M., van Lenteren, J.C. & Elad, Y. (1999) Integrated Pest and Disease Management in Greenhouse Crops. Dordrecht, The Netherlands, Kluwer Academic Publishers.CrossRefGoogle Scholar
Armstrong, K.F. & Ball, S.L. (2005) DNA barcodes for biosecurity: invasive species identification. Philosophical Transactions of the Royal Society B: Biological Sciences 360(1462), 1813–1823.CrossRefGoogle ScholarPubMed
Ball, S.L. & Armstrong, K.F. (2006) DNA barcodes for insect pest identification: a test case with tussock moths (Lepidoptera: Lymantriidae). Canadian Journal of Forest Research 36, 337–350.CrossRefGoogle Scholar
Bandlet, H.J., Foster, P. & Rohl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–34.CrossRefGoogle Scholar
Barr, N.B. (2009) Pathway analysis of Ceratitis capitata (Diptera: Tephritidae) using mitochondrial DNA. Journal of Economic Entomology 102, 401–411.CrossRefGoogle ScholarPubMed
Bogdanowicz, S.M., Wallner, W.E., Bell, J., ODell, T.M. & Harrison, R.G. (1993) Asian gypsy moth (Lepidoptera: Lymantriidae) in North America: evidence from molecular data. Annals of the Entomological Society of America 86, 710–715.CrossRefGoogle Scholar
Bogdanowicz, S.M., Schaefer, P.W. & Harrison, R.G. (2000) Mitochondrial DNA variation among worldwide populations of gypsy moths, Lymantria dispar . Molecular Phylogenetics and Evolution 15, 487–495. doi: 10.1006/mpev.1999.0744.CrossRefGoogle ScholarPubMed
Boykin, L.M., Shatters, R.G. Jr., Rosell, R.C., McKenzie, C.L., Bagnall, R.A., De Barro, P. & Frohlich, D.R. (2007) Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial COI DNA sequences. Molecular Phylogenetics and Evolution 44, 1306–1319.CrossRefGoogle ScholarPubMed
Boykin, L.M., Armstrong, K.F., Kubatko, L. & De Barro, P. (2012 a) Species delimitation and global biosecurity. Evolutionary Bioinformatics 8, 1–37.Google ScholarPubMed
Boykin, L.M., De Barro, P., Hall, D.G., Hunter, W.B., McKenzie, C.L., Powell, C.A. & Shatters, R.G. Jr. (2012 b) Overview of worldwide diversity of Diaphorina citri Kuwayama Mitochondrial Cytochrome Oxidase 1 Haplotypes: two old world lineages and a new world invasion. Bulletin of Entomological Research 102(5), 573–582.CrossRefGoogle Scholar
CABI (2013) Trialeurodes vaporariorum. in Invasive Species Compendium. Wallingford, UK, CAB International. Available online at http://www.cabi.org/isc Google Scholar
Caciagli, P. (2007) Survival of whiteflies during long-distance transportation of agricultural products and plants. pp. 57–63 in Czosnek, H. (Ed.) Tomato Yellow Leaf Curl Virus Disease (Management, Molecular Biology, Breeding for Resistance. Netherlands, Springer.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Chiel, E., Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Katzir, N., Inbar, M. & Ghanim, M. (2007) Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bulletin of Entomological Research 97, 407–413.CrossRefGoogle ScholarPubMed
De Barro, P. & Ahmed, M.Z. (2011) Genetic networking of the Bemisia tabaci cryptic species complex reveals pattern of biological invasions. PLoS ONE 6(10), e25579. doi: 10.1371/journal.pone.0025579.CrossRefGoogle ScholarPubMed
De Barro, J., Liu, S., Boykin, L. & Dinsdale, A. (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 1–19.CrossRefGoogle ScholarPubMed
Delatte, H., Reynaud, B., Granier, M., Thornary, L., Lett, J.M., Goldbach, R. & Peterschmitt, M. (2005) A new silverleaf-inducing biotype Ms of Bemisia tabaci (Hemiptera: Aleyrodidae), indigenous to the islands of the south west Indian Ocean. Bulletin of Entomological Research 95, 1–7.CrossRefGoogle Scholar
Dinsdale, A.B., Cook, L., Riginos, C., Buckley, Y.M. & De Barro, P. (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase I to identify species level genetic boundaries. Annals of the Entomological Society of America 103, 196–208.CrossRefGoogle Scholar
Duffus, J.E. (1965) Beet pseudo-yellows virus, transmitted by the greenhouse whitefly (Trialeurodes vaporariorum). Phytopathology 55, 450–453.Google Scholar
Duffus, J.E., Liu, H.-Y. & Wisler, G.C. (1996) Tomato infectious chlorosis virus – a new clostero-like virus transmitted by Trialeurodes vaporariorum . European Journal of Plant Pathology 102, 219–226.CrossRefGoogle Scholar
Floyd, R.M., Wilson, J.J. & Hebert, P.D.N. (2009) DNA Barcodes and Insect Biodiversity. doi: 10.1002/9781444308211.ch17 ISBN: 9781444308211, In: Insect Biodiversity: Science and Society, pp. 417–431.CrossRefGoogle Scholar
Floyd, R., Lima, J., deWaard, J.R., Humble, L.M. & Hanner, R.H. (2010) Common goals: policy implications of DNA barcoding as a protocol for identification of arthropod pests. Biological Invasions 12(9), 2947–2954.CrossRefGoogle Scholar
Fortes, I.M., Moriones, E. & Navas-Castillo, J. (2012) Tomato chlorosis virus in pepper: prevalence in commercial crops in southeastern Spain and symptomatology under experimental conditions. Plant Pathology 61, 994–1001.CrossRefGoogle Scholar
Frohlich, D.R., Torres-Jerez, I.I., Bedford, I.D., Markham, P.G. & Brown, J.K. (1999) A phylogeographical analysis of the Bemisia tabaci species complex based on mitochondrial DNA markers. Molecular Ecology 8, 1683–1691.CrossRefGoogle ScholarPubMed
Galtier, N., Nabholz, B., Gle´min, S. & Hurst, G.D.D. (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology 18, 4541–4550.CrossRefGoogle ScholarPubMed
Gorman, K., Devine, G., Bennison, J., Coussons, P., Punchard, N. & Denholm, I. (2007) Rapid report of resistance to the neonicotinoid insecticide imidacloprid in Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). Pest Management Science 63, 555–558.CrossRefGoogle Scholar
Gorman, K., Slater, R., Blande, J.D., Clarke, A., Wren, J., McCaffery, A. & Denholm, I. (2010) Cross-resistance relationships between neonicotinoids and pymetrozine in Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science 66, 1186–1190.CrossRefGoogle Scholar
Gueguen, G., Vavre, F., Gnankine, O., Peterschmitt, M., Charif, D., Chiel, E., Gottlieb, Y., Ghanim, M., Zchori-Fein, E. & Fleury, F. (2010) Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Molecular Ecology 19, 4365–4378.CrossRefGoogle ScholarPubMed
Guevara-Coto, J.A., Barboza-Vargas, N., Hernandez-Jimenez, E., Hammond, R.W. & Ramirez-Fonseca, P. (2011) Bemisia tabaci Biotype Q is present in Costa Rica. European Journal of Plant Pathology 131, 167–170.CrossRefGoogle Scholar
Higgins, D.G., Thompson, J.D. & Gibson, T.J. (1996) Using CLUSTAL for multiple sequence alignments. Methods in Enzymology 266, 383–402.CrossRefGoogle ScholarPubMed
Hebert, P.D.N. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of LondonSeries B, Biological Sciences 270, S596–S599.Google ScholarPubMed
Hu, J., De Barro, P., Zhao, H., Wang, J., Nardi, F. & Lui, 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(1), e16061. doi: 10.1371/journal.pone.0016061.CrossRefGoogle Scholar
Jones, D.R. (2003) Plant viruses transmitted by whiteflies. European Journal of Plant Pathology 109, 195–219.CrossRefGoogle Scholar
Karatolos, N., Denholm, I., Williamson, M., Nauen, R. & Gorman, K. (2010) Incidence and characterisation of resistance to neonicotinoid insecticides and pymetrozine in the greenhouse whitefly, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae). Pest Management Science 66, 1304–1307.CrossRefGoogle Scholar
Karatolos, N., Williamson, M.S., Denholm, I., Gorman, K., French-Constant, R. & Nauen, R. (2012) Resistance to spiromesifen in Trialeurodes vaporariorum is associated with a single amino acid replacement in its target enzyme acetyl-coenzyme A carboxylase. Insect Molecular Biology 21(3), 327–334.CrossRefGoogle ScholarPubMed
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
Lopes, A. (2002) Whiteflies on tomato crops in Portugal. Bulletin OEPP/EPPO 32, 7–10.CrossRefGoogle Scholar
Luo, C., Wang, S.Q., Cui, W.Q. & Zhang, Z.L. (2004) The population dynamics of whiteflies and their natural enemy in Beijing suburb. Modern Entomology Research, Agricultural Science Press Beijing, China pp. 465–468.Google Scholar
Malumphy, C., Belen Suarez, M., Glover, R., Boonham, N. & Collins, D.W. (2007) Morphological and molecular evidence supporting the validity of Trialeurodes lauri and T. ricini (Hemiptera: Sternorrhyncha: Aleyrodidae. European Journal of Entomology 104, 295–301.CrossRefGoogle Scholar
Manzano, M.R. & van Lenteren, J.C. (2009) Life history parameters of Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) at different environmental conditions on two bean cultivars. Neotropical Entomology 38, 452–458.CrossRefGoogle ScholarPubMed
Marcic, D., Prijovic, M., Drobnjakovic, T., Peric, P., Sevic, M. & Stamenkovic, S. (2011) Effects of Bioinsecticides in control of greenhouse whitefly (Trialeurodes vaporariorum Westwood) on Tomato. Pesticides and Phytomedicine 26(4), 363–369.CrossRefGoogle Scholar
Martin, J.H., Mifsud, D. & Rapidsarda, C. (2000) The whiteflies (Hemiptera: Aleyrodidae) of Europe and Mediterranean basin. Bulletin of Entomological Research 90, 407–448.CrossRefGoogle ScholarPubMed
Mound, L.A. & Halsey, S.H. (1978) Whitefly of the world: a systematic catalogue of the Aleyrodidae (Homoptera) with host plant and natural enemy data. Chichester, British Museum (Natural History), p. 340.Google Scholar
Nagoshi, R.N., Paraiso, O., Brambila, J. & Kairo, M.T. (2012) Assessing the usefulness of DNA Barcoding to identify Oxycarenus hyalinipennis (Hemiptera: Oxycarenidae) in Florida, a Potentially Invasive Pest of Cotton. Florida Entomologist 95(4), 1174–1181.CrossRefGoogle Scholar
Omer, A.D., Leigh, T.E. & Granett, J. (1992) Insecticide resistance in field population of greenhouse whitefly (Homoptera: Aleyrodidae) in the San Joaquin valley (California) cotton cropping system. Journal of Economic Entomology 85, 21–27.CrossRefGoogle Scholar
Omer, A.D., Johnson, M.W., Tabashnik, B.E. & Ullman, D.E. (1993) Association between insecticide use and greenhouse whitefly (Trialeurodes vaporariorum Westwood) resistance to insecticides in Hawaii. Pest Management Science 37, 253–259.CrossRefGoogle Scholar
O'Reilly, C.J. (1974) Investigations on the biology and biological control of the glasshouse whitefly Trialeurodes vaporariorum (Westwood). PhD Thesis, National University of Ireland, Ireland.Google Scholar
Palevsky, E., Soroker, V., Weintraub, P., Mansour, F., Abu-Moach, F. & Gerson, U. (2001) How specific is the phoretic relationship between broad mite, Polyphagotarsonemus latus (Banks) (Acari: Tarsonemidae), and its insect vectors? Experimental and Applied Acarology 25, 217–224.CrossRefGoogle Scholar
Peric, P. (1999) Use of Autochthonous Species of Parasitoids from the Genus Encarsia for the Biological Control of the Whitefly (Trialeurodes vaporariorum Westwood) in Glasshouses. PhD Thesis, Faculty of Agriculture, University of Novi Sad, Serbia.Google Scholar
Petanovic, R., Marcic, D. & Vidovic, B. (2010) Mite Pest in plant crops – current issues, innovative approaches and possibilities for controlling them (1). Pesticides and Phytomedicine 25, 9–27.CrossRefGoogle Scholar
Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Prijovic, M., Drobnjakovic, T., Marcic, D., Peric, P., Petronijevic, S. & Stamenkovic, S. (2012) Efficacy of insecticides of natural origin in whitefly Trialeurodes vaporariorum control in tomato. Acta Horticulturae 960, 359–364.CrossRefGoogle Scholar
Ramos, N., Neto, E., Arsénio, A.F., Mangerico, S., Fortunato, E., Stigter, L., Fernandes, J.E., Lavadinho, A.M.P. & Louro, D. (2002) Situation of the whiteflies Bemisia tabaci and Trialeurodes vaporariorum in protected tomato crops in Algarve (Portugal). Bulletin OEPP/EPPO 32, 11–15.CrossRefGoogle Scholar
Ronquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Roopa, H.K., Krishna Kumar, N.K., Asokan, R., Rebijith, K.B., Mahmood, R. & Verghese, H. (2012) Phylogenetic analysis of Trialeurodes Spp. (Hemiptera: Aleyrodidae) from India based on differences in mitochondrial and nuclear DNA. Florida Entomologist 95(4), 1086–1094.CrossRefGoogle Scholar
Shin, D., Mo, H.-h., Lee, S.-E., Park, J.-J. & Cho, K. (2013) Elucidation of the genetic differences in Trialeurodes vaporariorum populations under vegetable greenhouse conditions by using the allozyme approach. Entomological Research 43, 271–281. doi: 10.1111/1748–5967.12032.Google Scholar
Simonsen, T.J., Brown, R.L. & Sperling, F.A.H. (2008) Tracing an invasion: phylogeography of Cactoblastis cactorum (Lepidoptera: Pyralidae) in the United States based on mitochondrial DNA. Annals of the Entomological Society of America 101(5), 899–905.CrossRefGoogle Scholar
Skaljac, M., Zanic, K., Goreta Ban, S., Kontsedalov, S. & Ghanim, M. (2010) Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiology 10, 142.CrossRefGoogle ScholarPubMed
Skaljac, M., Zanic, K., Hrncic, S., Radonjic, S., Perovic, T. & Ghanim, M. (2013) Diversity and localization of bacterial symbionts in three whitefly species (Hemiptera: Aleyrodidae) from the east coast of the Adriatic Sea. Bulletin of Entomological Research 103, 48–59.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Thao, M.L., Baumann, L. & Baumann, P. (2004) Organization of the mitochondrial genomes of whiteflies, aphids, and psyllids (Hemiptera, Sternorrhyncha). BMC Evolutionary Biology 4, 25.CrossRefGoogle Scholar
Tzanetakis, I.E., Wintermantel, W.M. & Martin, R.R. (2003) First report of Beet pseudo yellow virus in strawberry in the United States: a second crinivirus able to cause pallidosis disease. Plant Disease 87, 1398.CrossRefGoogle Scholar
Valverde, R.A., Sim, J. & Lotrakul, P. (2004) Whitefly transmission of sweet potato viruses. Virus Research 100(1), 123–128.CrossRefGoogle ScholarPubMed
Wang, H-L., Yang, J., Boykin, L.M., Zhao, Q-Y., Li, Q., Wang, X-W. & Liu, S-S. (2013) The characteristics and expression profiles of the mitochondrial genome for the Mediterranean species of the Bemisia tabaci complex. BMC Genomics, 14, 401. doi: 10.1186/1471–2164–14–401.CrossRefGoogle ScholarPubMed
Wisler, G.C., Duffus, J.E., Liu, H.Y. & Li, R.H. (1998 a) Ecology and epidemiology of whitefly-transmitted closteroviruses. Plant Disease 82, 270–280.CrossRefGoogle Scholar
Wisler, G.C., Li, R.H., Liu, H.Y., Lowry, D.S. & Duffus, J.E. (1998 b) Tomato chlorosis virus: a new whitefly-transmitted, phloem-limited, bipartite closterovirus of tomato. Phytopathology 88, 402–409.CrossRefGoogle ScholarPubMed
Zahradnik, J. (1963) Aleyrodina. in: Die Tiem'elt Mitteleuropas (N.S.) 4, 1–19.Google Scholar
Zanic, K., Goreta, S., Perica, S. & Sutic, J. (2008) Effects of alternative pesticides on greenhouse whitefly in protected cultivation. Journal of Pest Science 81 (3), 161–166.CrossRefGoogle Scholar
Žitko, T., Kovačić, A., Desdevises, Y. & Puizina, J. (2011) Genetic variation in East-Adriatic populations of the Asian tiger mosquito, Aedes albopictus (Diptera: Culicidae), inferred from NADH5 and COI sequence variability. European Journal of Entomology 108, 501–508.CrossRefGoogle Scholar
Supplementary material: File

Prijović Supplementary Material

Table 1

Download Prijović Supplementary Material(File)
File 141 KB