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Comparing the genetic structure of codling moth Cydia pomonella (L.) from Greece and France: long distance gene-flow in a sedentary pest species

Published online by Cambridge University Press:  28 October 2011

C.Ch. Voudouris ,
P. Franck ,
J. Olivares ,
B. Sauphanor ,
Z. Mamuris ,
J.A. Tsitsipis  and
J.T. Margaritopoulos
C.Ch. Voudouris
Affiliation:
Department of Biochemistry & Biotechnology, University of Thessaly, Ploutonos 26, 41221 Larissa, Greece
P. Franck
Affiliation:
UR 1115, Plantes et Systèmes de culture Horticoles, INRA. Site Agroparc, 84914 Avignon Cedex 9, France
J. Olivares
Affiliation:
UR 1115, Plantes et Systèmes de culture Horticoles, INRA. Site Agroparc, 84914 Avignon Cedex 9, France
B. Sauphanor
Affiliation:
UR 1115, Plantes et Systèmes de culture Horticoles, INRA. Site Agroparc, 84914 Avignon Cedex 9, France
Z. Mamuris
Affiliation:
Department of Biochemistry & Biotechnology, University of Thessaly, Ploutonos 26, 41221 Larissa, Greece
J.A. Tsitsipis
Affiliation:
Laboratory of Entomology and Agricultural Zoology, Department of Agriculture Crop Production and Rural Environment, University of Thessaly, Fytokou Str., 38446 Nea Ionia, Greece
J.T. Margaritopoulos*
Affiliation:
Department of Biochemistry & Biotechnology, University of Thessaly, Ploutonos 26, 41221 Larissa, Greece
*
*Author for correspondence Fax: 00302410565290 E-mail: johnmargaritopoulos@gmail.com
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Abstract

Codling moth Cydia pomonella L. (Lepidoptera: Tortricidae) is the most important insect pest of apple production in Europe. Despite the economic importance of this pest, there is not information about the genetic structure of its population in Greece and the patterns of gene-flow which might affect the success of control programs. In this study, we analysed nine samples from apple, pear and walnut from various regions of mainland Greece using 11 microsatellite loci. Six samples from the aforementioned hosts from southern France were also examined for comparison. Bayesian clustering and genetic distance analyses separated the codling moth samples in two genetic clusters. The first cluster consisted mainly of the individuals from Greece, and the second of those from France, although admixture and miss-classified individuals were also observed. The low genetic differentiation among samples within each country was also revealed by FST statistics (0.009 among Greek samples and 0.0150 among French samples compared to 0.050 global value among all samples and 0.032 the mean of the pair-wise values between the two countries). These FST values suggest little structuring at large geographical scales in agreement with previous published studies. The host species and local factors (climatic conditions, topography, pest control programs) did not affect the genetic structure of codling moth populations within each country. The results are discussed in relation to human-made activities that promote gene-flow even at large geographic distances. Possible factors for the genetic differentiation between the two genetic clusters are also discussed.

Keywords

codling mothpopulation structuregene-flowappleTorticidaeLepidoptera
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 2 , April 2012 , pp. 185 - 198
Copyright
Copyright © Cambridge University Press 2011

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References

Armstrong, K.F. & Wratten, S.D. (1996) The use of DNA analysis and the polymerase chain reaction in the study of introduced pests in New Zealand. pp. 231–263in Symondson, W.O.C. & Liddell, J.E. (Eds) The Ecology of Agricultural Pests: Biochemical Approaches. London, UK, Chapman & Hall.Google Scholar
Barnes, M.M. (1991) Codling moth occurrence, host race formation and damage. pp. 313–327in van der Geest, L.P.S. & Evenhuis, H.H. (Eds) Tortricid Pests: Their Biology, Natural Enemies and Control. Amsterdam, The Netherlands, Elsevier.Google Scholar
Baur, B. & Schmid, B. (1996) Spatial and temporal patterns of genetic diversity within species. pp. 169–201in Gaston, K.J. (Ed.) Biodiversity: A Biology of Numbers and Difference. Oxford, UK, Blackwell.Google Scholar
Behura, S.K. (2006) Molecular marker systems in insects: current trends and future avenues. Molecular Ecology 15, 3087–3113.CrossRefGoogle ScholarPubMed
Bohonak, A.J. (1999) Dispersal, gene flow, and population structure. Quarterly Review of Biology 74, 21–45.CrossRefGoogle ScholarPubMed
Boivin, T., Bouvier, J.-C., Beslay, D. & Sauphanor, B. (2004) Variability in diapause propensity within populations of a temperate insect species: interactions between insecticide resistance genes and photoperiodism. Biological Journal of the Linnean Society 83, 341–351.CrossRefGoogle Scholar
Brookfield, J.F.Y. (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology 5, 453–455.CrossRefGoogle ScholarPubMed
Buès, R. & Toubon, J.F. (1992) Polymorphisme enzymatique dans différentes populations de Cydia pomonella L. (Lep. Tortricidae). Acta Oecologica-International Journal of Ecology 13, 583–591.Google Scholar
Buès, R., Toubon, J.F. & Poitout, H.S. (1995) Variabilité écophysiologique et enzymatique de Cydia pomonella L. En fonction de l'origine géographique et de la plante hôte. Agronomie 15, 221–231.CrossRefGoogle Scholar
Chakraborty, R. & Jin, L. (1993) A unified approach to study hypervariable polymorphisms: statistical considerations of determining relatedness and population distances. pp. 153–175in Pena, S.D.J., Chakraborty, R., Epplen, J.T. & Jeffreys, A.J. (Eds) DNA Fingerprinting: State of the Science. Basel, Switzerland, Birkhäuser, Verlag.CrossRefGoogle Scholar
Chen, H.M. & Dorn, S. (2010) Microsatellites reveal genetic differentiation among populations in an insect species with high genetic variability in dispersal, the codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae). Bulletin of Entomological Research 100, 75–85.Google Scholar
Coates, B.S., Sumerford, D.V. & Hellmich, R.L. (2004) Geographic and voltinism differentiation among North American Ostrinia nubilalis (European corn borer) mitochondrial cytochrome c oxidase haplotypes. Journal of Insect Science 4, 35, 9 pp. Available online at www.insectscience.org/4.35.CrossRefGoogle ScholarPubMed
Corander, J., Marttinen, P., Sirén, J. & Tang, J. (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9, 539, 14 pp. Available online at http://www.biomedcentral.com/1471-2105/9/539.CrossRefGoogle ScholarPubMed
Cornuet, J.M. & Luikart, G. (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.CrossRefGoogle ScholarPubMed
Delmotte, F., Leterme, N., Gauthier, J.-P., Rispe, C., Simon, J.-C. (2002) Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers. Molecular Ecology 11, 711–723.CrossRefGoogle ScholarPubMed
Denholm, I. & Rowland, M.W. (1992) Tactics for managing pesticide resistance in arthropods: theory and practice. Annual Review of Entomology 37, 91–112.CrossRefGoogle ScholarPubMed
Endersby, N.M., McKechnie, S.W., Ridland, P.M. & Weeks, A.R. (2006) Microsatellites reveal a lack of structure in Australian populations of the diamondback moth, Plutella xylostella (L.). Molecular Ecology 15, 107–118.CrossRefGoogle ScholarPubMed
Endersby, N.M., Hoffmann, A.A., McKechnie, S.W. & Weeks, A.R. (2007) Is there genetic structure in populations of Helicoverpa armigera from Australia? Entomologia Experimentalis et Applicata 122, 253–263.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., 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, 479–491.CrossRefGoogle ScholarPubMed
Fenton, B., Malloch, G., Navajas, M., Hillier, J. & Birch, A.N.E. (2003) Clonal composition of the peach-potato aphid Myzus persicae (Homoptera: Aphididae) in France and Scotland: Comparative analysis with IGS fingerprinting and microsatellite markers. Annals of Applied Biology 142, 255–267.CrossRefGoogle Scholar
Franck, P. & Timm, A.E. (2010) Population genetic structure of Cydia pomonella: a review and case study comparing spatiotemporal variation. Journal of Applied Entomology 134, 191–200.CrossRefGoogle Scholar
Franck, P., Guérin, F., Loiseau, A. & Sauphanor, B. (2005) Isolation and characterisation of microsatellite loci in the codling moth Cydia pomonella L. (Lepidoptera, Tortricidae). Molecular Ecology Notes 5, 99–102.CrossRefGoogle 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.Google Scholar
Franck, P., Ricci, B., Klein, E.K., Olivares, J., Simon, S., Cornuet, J.-M. & Lavigne, C. (2011) Genetic inferences about the population dynamics of codling moth females at a local scale. Genetica 39, 949–960.CrossRefGoogle Scholar
Fuentes-Contreras, E., Reyes, M., Barros, W. & Sauphanor, B. (2007) Evaluation of azinphosmethyl resistance and activity of detoxifying enzymes in codling moth (Lepidoptera: Tortricidae) from central Chile. Journal of Economic Entomology 100, 551–556.CrossRefGoogle ScholarPubMed
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, 190–198.CrossRefGoogle ScholarPubMed
Garnier, S., Alibert, P., Audiot, P., Prieur, B. & Rasplus, J.-Y. (2004) Isolation by distance and sharp discontinuities in gene frequencies: implications for the phylogeography of an alpine insect species, Carabus solieri. Molecular Ecology 13, 1883–1897.CrossRefGoogle ScholarPubMed
Goudet, J. (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86, 485–486.CrossRefGoogle Scholar
Goudet, J., Raymond, M., de Meeüs, T. & Rousset, F. (1996) Testing differentiation in diploid populations. Genetics 144, 1933–1940.CrossRefGoogle ScholarPubMed
Harper, G.L., Maclean, N. & Goulson, D. (2003) Microsatellite markers to assess the influence of population size, isolation and demographic change on the genetic structure of the UK butterfly Polyommatus bellargus. Molecular Ecology 12, 3349–3357.CrossRefGoogle ScholarPubMed
Higbee, B.S., Calkins, C.O. & Temple, C.A. (2001) Overwintering of codling moth (Lepidoptera: Tortricidae) larvae in apple harvest bins and subsequent moth emergence. Journal of Economic Entomology 94, 1511–1517.CrossRefGoogle ScholarPubMed
Keil, S., Gu, H.N. & Dorn, S. (2001) Response of Cydia pomonella to selection on mobility: laboratory evaluation and field verification. Ecological Entomology 26, 495–501.CrossRefGoogle Scholar
Keyghobadi, N., Roland, J. & Strobeck, C. (1999) Influence of landscape on the population genetic structure of the alpine butterfly Parnassius smintheus (Papilionidae). Molecular Ecology 8, 1481–1495.Google Scholar
Knight, A.L., Brunner, J.F. & Alston, D. (1994) Survey of azinphos methyl resistance in codling moth (Lepidoptera: Tortricidae) in Washington and Utah. Journal of Economic Entomology 87, 285–292.Google Scholar
Loxdale, H.D. & Lushai, G. (2001) Use of genetic diversity in movement studies of flying insects. pp. 361–386in Woiwod, I.P., Reynolds, D.R. & Thomas, C.D. (Eds) Insect Movement: Mechanisms and Consequences. Wallingford, UK, CABI Publishing.Google Scholar
Manel, S., Gaggiotti, O.E. & Waples, R.S. (2005) Assignment methods: matching biological questions with appropriate techniques. Trends in Ecology and Evolution 20, 136–142.Google Scholar
Mani, E. & Wildbolz, T. (1977) The dispersal of male codling moths (Laspeyresia pomonella L.) in the Upper Rhine Valley. Journal of Applied Entomology 83, 161–168.Google Scholar
Mantel, N. (1967) The detection of disease clustering and generalized regression approach. Cancer Research 27, 209–220.Google ScholarPubMed
Meglécz, E. & Solignac, M. (1998) Microsatellite loci for Parnassius mnemosyne (Lepidoptera). Hereditas 128, 179–180.CrossRefGoogle Scholar
Meglécz, E., Petenian, F., Danchin, E., Coeur, , D'Acier, A.C., Rasplus, J.Y. & Faure, E. (2004) High similarity between flanking regions of different microsatellites detected within each of two species of Lepidoptera: Parnassius Apollo and Euphydryas aurinia. Molecular Ecology 13, 1696–1700.CrossRefGoogle ScholarPubMed
Orsini, L., Wheat, C.W., Haag, C.R., Kvist, J., Frilander, M.J. & Hanski, I. (2008) Fitness differences associates with Pgi SNP genotypes in the Glanville fritillary butterfly (Melitaea cinxia). Journal of Evolutionary Biology 22, 367–375.Google Scholar
Paetkau, D., Slade, R., Burden, M. & Estoup, A. (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Molecular Ecology 13, 55–65.CrossRefGoogle Scholar
Pashley, D.P. & Bush, G.L. (1979) The use of allozymes in studying insect movement with special reference to the codling moth, Laspeyresia pomonella (L.) (Olethreutidae). pp. 333–341in Rabb, R.L. & Kennedy, G.G. (Eds) Movement of Highly Mobile Insects: Concepts and Methodology in Research. Raleigh, NC, USA, North Carolina State University Press.Google Scholar
Palo, J., Varvio, S.L., Hanski, I. & Vainola, R. (1995) Developing micro-satellite markers for insect population structure–complex variation in a checkerspot butterfly. Hereditas 123, 295–300.Google Scholar
Peakall, R. & Smouse, P.E. (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.CrossRefGoogle Scholar
Peterson, M.A. (1996) Long-distance gene flow in the sedentary butterfly, Euphilotes enoptes (Lepidoptera: Lycaenidae). Evolution 50, 1990–1999.Google ScholarPubMed
Peterson, M.A. & Denno, R.F. (1998a) The influence of dispersal and diet breadth on patterns of genetic isolation by distance in phytophagous insects. American Naturalist 152, 428–446.CrossRefGoogle ScholarPubMed
Peterson, M.A. & Denno, R.F. (1998b) Life history strategies and the genetic structure of phytophagous insect populations. pp. 263–322in Mopper, S. & Strauss, S. (Eds) Genetic Structure and Local Adaptation in Natural Insect Populations: Effects of Ecology, Life History, and Behavior. New York, USA, Chapman & Hall.CrossRefGoogle Scholar
Piry, S., Luikart, G. & Cornuet, J.-M. (1999) Bottleneck: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90, 502–503.CrossRefGoogle Scholar
Piry, S., Alapetite, A., Cornuet, J.-M., Paetkau, D., Baudouin, L. & Estoup, A. (2004) GeneClass2: a software for genetic assignment and first generation migrants detection. Journal of Heredity 95, 536–539.CrossRefGoogle ScholarPubMed
Phillips, P.A. & Barnes, M.M. (1975) Host race formation among sympatric apple, walnut, and plum populations of the codling moth, Laspeyresia pomonella. Annals of the Entomological Society of America 68, 1053–1060.Google Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.Google Scholar
Rannala, B. & Mountain, J.L. (1997) Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences 94, 9197–9201.CrossRefGoogle ScholarPubMed
Raymond, M. & Rousset, F. (1995) An exact test for population differentiation. Evolution 49, 1280–1283.CrossRefGoogle ScholarPubMed
Riedl, H. & Croft, B.A. (1978) The effects of photoperiod and effective temperatures on the seasonal phenology of the codling moth (Lepidoptera: Tortricidae). Canadian Entomologist 110, 455–470.CrossRefGoogle Scholar
Roderick, G.K. (1996) Geographic structure of insect populations: gene flow, phylogeography, and their uses. Annual Review of Entomology 41, 325–352.CrossRefGoogle ScholarPubMed
Rousset, F. (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228.CrossRefGoogle ScholarPubMed
Rousset, R. (2008) GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8, 103–106.CrossRefGoogle ScholarPubMed
Sauphanor, B., Bouvier, J.C. & Brosse, V. (1998) Spectrum of insecticide resistance in Cydia pomonella (Lepidoptera: Tortricidae) in southeastern France. Journal of Economic Entomology 91, 1225–1231.CrossRefGoogle Scholar
Schumacher, P., Weyeneth, A., Weber, D.C. & Dorn, S. (1997) Long flights in Cydia pomonella L. (Lepidoptera: Tortricidae) measured by a flight mill: influence of sex, mated status and age. Physiological Entomology 22, 149–160.Google Scholar
Schneider, J.C. (1999) Dispersal of a highly vagile insect in a heterogeneous environment. Ecology 80, 2740–2749.Google Scholar
Schneider, S., Roessli, D. & Excoffier, L. (2000) Arelquin. A software for population genetic data analysis, Version 2.0. Genetics and Biometry Laboratory, University of Geneva, Geneva, Switzerland.Google Scholar
Shel'Deshova, G.G. (1967) Ecological factors determining the distribution of the codling moth Laspeyresia pomonella L. (Lepidoptera, Tortricidae) in the northern and southern hemispheres. Entomological Review 46, 349–361.Google Scholar
Slatkin, M. (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47, 264–279.CrossRefGoogle ScholarPubMed
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.Google Scholar
Thaler, R., Brandstätter, A., Meraner, A., Chabicovski, M., Parson, W., Zelger, R., Dalla Via, J. & Dallinger, R. (2008) Molecular phylogeny and population structure of the codling moth (Cydia pomonella) in Central Europe: II. AFLP analysis reflects human-aided local adaptation of a global pest species. Molecular Phylogenetics and Evolution 48, 838–849.CrossRefGoogle ScholarPubMed
Timm, A.E., Geertsema, H. & Warnich, L. (2006) Gene flow among Cydia pomonella (Lepidoptera: Tortricidae) geographic and host populations in South Africa. Journal of Economic Entomology 99, 341–348.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, 535–538.CrossRefGoogle Scholar
Voudouris, C.Ch., Sauphanor, B., Franck, P., Reyes, M., Mamuris, Z., Tsitsipis, J.A., Vontas, J. & Margaritopoulos, J.T. (2011) Insecticide resistance status of the codling moth Cydia pomonella (Lepidoptera: Tortricidae) from Greece. Pesticide Biochemistry and Physiology 100, 229–238.CrossRefGoogle Scholar
Walsh, P.S., Metzger, D.A. & Higuchi, R. (1991) Chelex (R) 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 507.Google Scholar
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google ScholarPubMed
Wright, S. (1943) Isolation by distance. Genetics 28, 114–138.CrossRefGoogle ScholarPubMed
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Table S1. Single and multilocus probability tests for deviations from HW equilibrium and FIS coefficient values.

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