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Population genetic structure and secondary endosymbionts of Q Bemisia tabaci (Hemiptera: Aleyrodidae) from Greece

Published online by Cambridge University Press:  27 January 2012

A. Tsagkarakou ,
L. Mouton ,
J.B. Kristoffersen ,
E. Dokianakis ,
M. Grispou  and
K. Bourtzis
A. Tsagkarakou*
Affiliation:
National Agricultural Research Foundation, Plant Protection Institute, Laboratory of Entomology and Agricultural Zoology, PO Box 2228, 71003 Heraklion, Greece
L. Mouton
Affiliation:
Université Lyon1, CNRS, UMR 5558, Laboratoire de Biométrie et Biologie Évolutive, F-69622, Villeurbanne, France
J.B. Kristoffersen
Affiliation:
National Agricultural Research Foundation, Plant Protection Institute, Laboratory of Entomology and Agricultural Zoology, PO Box 2228, 71003 Heraklion, Greece
E. Dokianakis
Affiliation:
National Agricultural Research Foundation, Plant Protection Institute, Laboratory of Entomology and Agricultural Zoology, PO Box 2228, 71003 Heraklion, Greece Department of Environmental and Natural Resources Management, University of Ioannina, 2 Seferi St., 30100 Agrinio, Greece
M. Grispou
Affiliation:
National Agricultural Research Foundation, Plant Protection Institute, Laboratory of Entomology and Agricultural Zoology, PO Box 2228, 71003 Heraklion, Greece
K. Bourtzis
Affiliation:
Department of Environmental and Natural Resources Management, University of Ioannina, 2 Seferi St., 30100 Agrinio, Greece Biomedical Sciences Research Centre, Al. Fleming, 16672 Vari, Greece
*
*Author for correspondence Fax: 0030 2810245858 E-mail: [email protected]
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Abstract

We investigated the molecular diversity of the major agricultural pest Bemisia tabaci and of its associated secondary endosymbionts in Greece. Analyzing mitochondrial DNA, we found that the Q1 (=Q west) is predominant. We used eight microsatellite polymorphic markers to study the genetic structure of 37 populations from mainland and insular Greece, collected on different host species from outdoor and protected crops as well as from non-cultivated plants. In some cases, gene flow was found to be low even between populations separated by just a few kilometres. Bayesian analysis identified two main genetic groups, the first encompassing populations from south Crete and the second composed of populations from north Crete, two other Aegean islands and mainland Greece. Genetic differentiation was not correlated with different host plant species or habitat, or greenhouse versus open environment populations. Gene flow significantly decreased with geographic distance, but no isolation by distance existed when only the samples from mainland Greece or only the samples from Crete were considered. The secondary symbionts Wolbachia and Hamiltonella were present at high frequencies while Arsenophonus, Cardinium and Rickettsia were absent from Greek populations. Multilocus sequence typing of Wolbachia identified two Wolbachia strains. These two strains were found together in most of the populations studied but never in the same host individual. Their role on the observed population structure is discussed.

Keywords

Q Bemisia tabacipopulation structuremicrosatellitessecondary endosymbiontsWolbachia
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 3 , June 2012 , pp. 353 - 365
Copyright
Copyright © Cambridge University Press 2012

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References

Arthofer, W., Riegler, M., Schneider, D., Krammer, M., Miller, W.J. & Stauffer, C. (2009) Hidden Wolbachia diversity in field populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera, Tephritidae). Molecular Ecology 18, 3816–3830.CrossRefGoogle Scholar
Baldo, L., Dunning Hotopp, J.C., Jolley, K.A., Bordenstein, S.R., Biber, S.A., Choudhury, R.R., Hayashi, C., Maiden, M.C., Tattelin, H. & Werren, J.H. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Applied and Environmental Microbiology 72, 7098–7110.CrossRefGoogle ScholarPubMed
Bian, G., Xu, Y., Lu, P., Xie, Y. & Xi, Z. (2010) Wolbachia induces resistance to dengue virus in Aedes aegypti. PLos Pathogens 6, e1000833.CrossRefGoogle ScholarPubMed
Byrne, D..N. (1999) Migration and dispersal by the sweet potato whitefly, Bemisia tabaci. Agricultural and Forest Meteorology 97, 309–316.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, 1–7.CrossRefGoogle ScholarPubMed
Dalmon, A., Halkett, F., Granier, M., Delatte, H. & Peterschmitt, M. (2008) Genetic structure of the invasive pest Bemisia tabaci: evidence of limited but persistent genetic differentiation in glasshouse populations. Heredity 100, 316–325.CrossRefGoogle ScholarPubMed
De Barro, P.J. (2005) Genetic structure of the whitefly Bemisia tabaci in the Asia-Pacific region revealed using microsatellite markers. Molecular Ecology 14, 3695–3718.CrossRefGoogle ScholarPubMed
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, 1–19.CrossRefGoogle ScholarPubMed
Delatte, H., David, P., Granier, M., Lett, J.M., Goldbach, R., Peterscmitt, 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, 109–124.CrossRefGoogle Scholar
Delatte, H., Holota, H., Warren, B.H., Becker, N., Thierry, M. & Reynaud, B. (2011) Genetic diversity, geographical range and origin of Bemisia tabaci (Hemiptera: Aleyrodidae) Indian Ocean Ms. Bulletin of Entomological Research 101, 487–497.CrossRefGoogle ScholarPubMed
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, 196–208.CrossRefGoogle Scholar
Duron, O., Bouchon, D., Boutin, S., Bellamy, L., Zhou, L., Engelstädter, J. & Hurst, G.D. (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biology 6, 27–39.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Gennadius, P. (1889) Disease of tobacco plantations in the Trikonia. The aleyrodid of tobacco. Ellenike Georgia 5, 1–3 (in Greek).Google Scholar
Franck, P., Reyes, M., Olivares, J. & Sauphanor, B. (2007) Genetic architecture in codling moth populations, comparison between microsatellite and insecticide resistance markers. Molecular Ecology 16, 3554–3564.CrossRefGoogle ScholarPubMed
Franklin, M.T., Ritland, C.E. & Myers, J.H. (2010) Spatial and temporal changes in genetic structure of greenhouse and field populations of cabbage looper, Trichoplusia ni. Molecular Ecology 19, 1122–1133.CrossRefGoogle ScholarPubMed
Gómez-Valero, L., Soriano-Navarro, M., Pérez-Brocal, V., Heddi, A., Moya, A., García-Verdugo, J.M. & Latorre, A. (2004) Coexistence of Wolbachia with Buchnera aphidicola and a secondary symbiont in the aphid Cinara cedri. Journal of Bacteriology 186, 6626–6633.CrossRefGoogle Scholar
Gottlieb, Y., Ghanim, M., Gueguen, G., Kontsedalov, S., Vavre, F., Fleury, F. & Zchori-Fein, E. (2008) Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. Faseb Journal 22, 2591–2599.CrossRefGoogle ScholarPubMed
Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Kontsedalov, S., Skaljac, M., Brumin, M., Sobol, I., Czosnek, H., Vavre, F., Fleury, F. & Ghanim, M. (2010) The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. Journal of Virology 84, 9310–9317.CrossRefGoogle ScholarPubMed
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, 4365–4376.CrossRefGoogle ScholarPubMed
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
Higgins, D.G., Thompson, J.D. & Gibson, T.J. (1996) Using Clustal for multiple sequence alignments. Methods Enzymology 266, 383–402.CrossRefGoogle ScholarPubMed
Himler, A.G., Adachi-Hagimori, T., Bergen, J.E., Kozuch, A., Kelly, S.E., Tabashnik, B.E., Chiel, E., Duckworth, V.E., Dennehy, T.J., Zchori-Fein, E. & Hunter, M.S. (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332, 254–256.CrossRefGoogle Scholar
Holm, S. (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6, 65–70.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, e16061 (doi:10.1371/journal.pone.0016061).CrossRefGoogle ScholarPubMed
Hunter, M.S., Perlman, S.J. & Kelly, S.E. (2003) A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proceedings of the Royal Society of London, Series B 270, 2185–2190.CrossRefGoogle ScholarPubMed
Jiu, M., Zhou, X.-P., Tong, L., Xu, J., Yang, X., Wan, F.H. & Liu, S.-S. (2007) Vector-Virus Mutualism Accelerates Population Increase of an Invasive Whitefly. PLoS ONE 2(1), e182 (doi:10.1371/journal.pone.0000182).CrossRefGoogle ScholarPubMed
Jones, D.R. (2003) Plant viruses transmitted by whiteflies. European Journal of Plant Pathology 109, 195–219.CrossRefGoogle Scholar
Li, Z.X., Lin, H.Z. & Guo, X.P. (2007) Prevalence of Wolbachia infection in Bemisia tabaci. Current Microbiology 54, 467–471.CrossRefGoogle ScholarPubMed
Mahadav, A., Gerling, D., Gottlieb, Y., Czosnek, H. & Ghanim, M. (2008) Parasitization by the wasp Eretmocerus mundus induces transcription of genes related to immune response and symbiotic bacteria proliferation in the whitefly Bemisia tabaci. BMC Genomics 9, 342.CrossRefGoogle ScholarPubMed
Maruthi, M.N., Colvin, J., Thwaites, R.M., Banks, G.K., Gibson, G. & Seal, S.E. (2004) Reproductive incompatibility and cytochrome oxidase I gene sequence variability among host-adapted and geographically separate Bemisia tabaci populations. Systematic Entomology 29, 560–568.CrossRefGoogle Scholar
McKenzie, C.L., Hodges, G., Osborne, L.S., Byrne, F.J. & Shatters, R.G. Jr (2009) Distribution of Bemisia tabaci (Hemiptera, Aleyrodidae) biotypes in Florida investigating the Q invasion. Journal of Economic Entomology 102, 670–676.CrossRefGoogle Scholar
Moran, N.A., McCutcheon, J.P. & Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42, 165–190.CrossRefGoogle ScholarPubMed
Mopper, S. (1996) Adaptive genetic structure in phytophagous insect populations. Trends in Ecology and Evolution 11, 235–238.CrossRefGoogle ScholarPubMed
Nirgianaki, A., Banks, G.K., Frohlich, D.R., Veneti, Z., Braig, H.R., Miller, T.A., Bedford, I.D., Markham, P.G., Savakis, C. & Bourtzis, K. (2003) Wolbachia infections of the whitefly Bemisia tabaci. Current Microbiology 47, 93–101.Google ScholarPubMed
Oliver, K.M., Degnan, P.H., Burke, G.R. & Moran, N.A. (2010) Facultative symbionts in Aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology 55, 247–266.CrossRefGoogle ScholarPubMed
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, 535–538.CrossRefGoogle Scholar
Papayiannis, L.C., Brownm, J.K., Hadjistylli, M. & Katis, N.I. (2008) Bemisia tabaci biotype B associated with tomato yellow leaf curl disease epidemics in Rhodes Island, Greece. Phytoparasitica 36, 20–22.CrossRefGoogle Scholar
Roditakis, E., Grispou, M., Morou, E., Kristoffersen, J.B., Roditakis, N., Nauen, R., Vontas, J. & Tsagkarakou, A. (2009) Current status of insecticide resistance in Q biotype Bemisia tabaci populations from Crete. Pest Management Science 65, 313–322.CrossRefGoogle ScholarPubMed
Rousset, F. (2007) GENEPOP'007, a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Notes 8, 103–106.CrossRefGoogle Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.CrossRefGoogle ScholarPubMed
Rosenberg, N.A. (2002) Distruct, a program for the graphical display of structure results. Available online at http://www.cmb.usc.edu/~noahr/distruct.html.Google Scholar
Saridaki, A. & Bourtzis, K. (2010) Wolbachia, more than just a bug in insects genitals. Current Opinion in Microbiology 13, 67–72.CrossRefGoogle ScholarPubMed
Simón, B., Cenis, J.L. & De La Rúa, P. (2007) Distribution patterns of the Q and B biotypes of Bemisia tabaci in the Mediterranean Basin based on microsatellite variation. Entomologia Experimentalis et Applicata 124, 327–336.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
Thao, M.L., Baumann, L., Hess, J.M., Falk, B.W., Ng, J.C.K., Gullan, P.J. & Baumann, P. (2003) Phylogenetic evidence for two new insect associated Chlamydia of the family Simkaniaceae. Current Microbiology 47, 46–50.CrossRefGoogle ScholarPubMed
Thao, M. & Baumann, P. (2004) Evolutionnary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Applied and Environnemental Microbiology 70, 3401–3406.CrossRefGoogle Scholar
Tsagkarakou, A. & Roditakis, N. (2003) Isolation & characterization of microsatellite loci in Bemisia tabaci (Hemiptera: Aleyrodidae). Molecular Ecology Notes 3, 196–198.CrossRefGoogle Scholar
Tsagkarakou, A., Tsigenopoulos, C., Gorman, K., Lagnel, J. & Bedford, I. (2007) Biotype status and genetic polymorphism of the whitefly Bemisia tabaci (Hemiptera, Aleyrodidae) in Greece, mitochondrial DNA and microsatellites. Bulletin of Entomological Research 97, 29–40.CrossRefGoogle ScholarPubMed
Tsagkarakou, A., Nikou, D., Roditakis, E., Sharvit, M., Morin, S. & Vontas, J. (2009) Molecular diagnostics for detecting pyrethroid and organophosphate resistance-associated point mutations in the white fly Bemisia tabaci. Pesticide Biochemistry and Physiology 94, 49–54.CrossRefGoogle Scholar
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google ScholarPubMed
Xu, J., De Barro, P.J. & Liu, S.S. (2010) Reproductive incompatibility among genetic groups of Bemisia tabaci supports the proposition that the whitefly is a cryptic species complex. Bulletin of Entomological Research 100, 359–366.CrossRefGoogle ScholarPubMed
Zchori-Fein, E. & Brown, J.K. (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera, Aleyrodidae). Annals of the Entomological Society of America 95, 711–718.CrossRefGoogle Scholar
Zhou, W., Rousset, F. & O'Neil, S. (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society of London, Series B 265, 509–515.CrossRefGoogle ScholarPubMed