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Genetic analysis of Cydia pomonella (Lepidoptera: Tortricidae) populations with different levels of sensitivity towards the Cydia pomonella granulovirus (CpGV)

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Abstract

Microsatellite (simple sequence repeats, SSR) and mitochondrial DNA markers were used to assess the structure of European codling moth populations showing different levels of susceptibility towards one of the most important biocontrol agents used in apple production, the Cydia pomonella granulovirus CpGV-M. In 638 C. pomonella individuals from 33 different populations a total of 92 different alleles were scored using six SSR loci. The global estimate of genetic differentiation for all 33 populations was not significantly different from zero, thus indicating a lack of genetic differentiation. AMOVA analysis revealed a very weak but significant variance among C. pomonella populations from different geographic regions, however, no significant variation was evident between CpGV-M resistant or susceptible C. pomonella populations. Sequence analysis of a fragment of the cytochrome oxidase subunit 1 in eight C. pomonella populations resulted in 27 haplotypes, which were grouped in two distinct clusters. Again, no genetic differentiation between CpGV-M resistant and susceptible codling moth populations was detectable. In addition, Structure analysis using microsatellites and association tests with mtDNA haplotypes found neither population-level nor individual correlations associated with CpGV-M resistance. Accordingly, this lack of population structure does not allow discriminating between one or several, separate origins of CpGV-M resistance.

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References

  • Asser-Kaiser S, Fritsch E, Undorf-Spahn K, Kienzle J, Eberle KE, Gund NA, Reineke A, Zebitz CPW, Heckel DG, Huber J, Jehle JA (2007) Rapid emergence of baculovirus resistance in codling moth due to dominant, sex-linked inheritance. Science 317:1916–1918

    Article  CAS  PubMed  Google Scholar 

  • Asser-Kaiser S, Heckel DG, Jehle JA (2010) Sex linkage of CpGV resistance in a heterogeneous field strain of the codling moth Cydia pomonella (L.). J Invertebr Pathol 103:59–64

    Article  CAS  PubMed  Google Scholar 

  • Bale JS, van Lenteren JC, Bigler F (2008) Biological control and sustainable food production. Philos T R Soc B 363:761–776

    Article  CAS  Google Scholar 

  • Barnes MM (1991) Codling moth occurence, host race formation, and damage. In: Van der Geest LPS, Evenhuis HH (eds) Tortricid pests. Their biology, natural enemies and control. Elsevier, Amsterdam, pp 313–328

    Google Scholar 

  • Basoalto E, Miranda M, Knight AL, Fuentes-Contreras E (2010) Landscape analysis of adult codling moth (Lepidoptera: Tortricidae) distribution and dispersal within typical agroecosystems dominated by apple production in central Chile. Environ Entomol 39:1399–1408. doi:10.1603/en09371

    Article  CAS  PubMed  Google Scholar 

  • Berling M, Blachere-Lopez C, Soubabere O, Lery X, Bonhomme A, Sauphanor B, Lopez-Ferber M (2009a) Cydia pomonella granulovirus genotypes overcome virus resistance in the codling moth and improve virus efficiency by selection against resistant hosts. Appl Environ Microb 75:925–930. doi:10.1128/aem.01998-08

    Article  CAS  Google Scholar 

  • Berling M, Rey J, Ondet S, Tallot Y, Soubabère O, Bonhomme A, Sauphanor B, Lopez-Ferber M (2009b) Field trials of CpGV virus isolates overcoming resistance to CpGV-M. Virol Sin 24:470–477

    Article  Google Scholar 

  • Buès R, Toubon JF (1992) Polymorphisme enzymatique dans différentes populations de Cydia pomonella L. (Lepidoptera: Toricidae). Acta Oecologie 13:583–591

    Google Scholar 

  • Chen MH, 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). Bull Ent Res 100:75–85. doi:10.1017/s0007485309006786

    Article  CAS  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Cross JV, Solomon MG, Babendreier D, Blommers L, Easterbrook MA, Jay CN, Jenser G, Jolly RL, Kuhlmann U, Lilley R, Olivella E, Toepfer S, Vidal S (1999a) Biocontrol of pests of apples and pears in Northern and Central Europe: 2. Parasitoids. Biocontrol Sci Technol 9:277–314

    Article  Google Scholar 

  • Cross JV, Solomon MG, Chandler D, Jarrett P, Richardson PN, Winstanley D, Bathon H, Huber J, Keller B, Langenbruch GA, Zimmermann G (1999b) Biocontrol of pests of apples and pears in Northern and Central Europe: 1. Microbial agents and nematodes. Biocontrol Sci Technol 9:125–149

    Article  Google Scholar 

  • Denholm I, Devine GJ, Williamson MS (2002) Insecticide resistance on the move. Science 297:2222–2223

    Article  CAS  PubMed  Google Scholar 

  • Eberle KE, Jehle JA (2006) Field resistance of codling moth against Cydia pomonella granulovirus (CpGV) is autosomal and incompletely dominant inherited. J Invertebr Pathol 93:201–206

    Article  PubMed  Google Scholar 

  • Eberle KE, Asser-Kaiser S, Sayed SM, Nguyen HT, Jehle JA (2008) Overcoming the resistance of codling moth against conventional Cydia pomonella granulovirus (CpGV-M) by a new isolate CpGV-I12. J Invertebr Pathol 98:293–298

    Article  CAS  PubMed  Google Scholar 

  • Eberle KE, Sayed S, Rezapanah M, Shojai-Estabragh S, Jehle JA (2009) Diversity and evolution of the Cydia pomonella granulovirus. J Gen Virol 90:662–671. doi:10.1099/vir.0.006999-0

    Article  CAS  PubMed  Google Scholar 

  • Endersby NM, Ridland PM, Hoffmann AA (2008) The effects of local selection versus dispersal on insecticide resistance patterns: longitudinal evidence from diamondback moth (Plutella xylostella (Lepidoptera : Plutellidae)) in Australia evolving resistance to pyrethroids. Bull Entomol Res 98:145–157. doi:10.1017/s0007485307005494

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  Google Scholar 

  • Franck P, Timm AE (2010) Population genetic structure of Cydia pomonella: a review and case study comparing spatiotemporal variation. J Appl Entomol 134:191–200. doi:10.1111/j.1439-0418.2009.01426.x

    Article  Google Scholar 

  • Franck P, Guerin B, Loiseau A, Sauphanor B (2005) Isolation and characterization of microsatellite loci in the codling moth Cydia pomonella L. (Lepidoptera, Tortricidae). Mol Ecol Notes 5:99–102

    Article  CAS  Google Scholar 

  • Franck P, Reyes M, Olivares J, Sauphanor B (2007) Genetic architecture in codling moth populations: comparison between microsatellite and insecticide resistance markers. Mol Ecol 16:3554–3564. doi:10.1111/j.1365-294X.2007.03410.x

    Article  CAS  PubMed  Google Scholar 

  • Franck P, Ricci B, Klein EK, Olivares J, Simon S, Cornuet JM, Lavigne C (2011) Genetic inferences about the population dynamics of codling moth females at a local scale. Genetica 139:949–960

    Article  CAS  PubMed  Google Scholar 

  • Fritsch E, Undorf-Spahn K, Kienzle J, Zebitz CPW, Huber J (2005) Apfelwickler Granulovirus: Erste Hinweise auf Unterschiede in der Empfindlichkeit lokaler Apfelwickler-Populationen. Nachrbl Dtsch Pflanzenschutzd 57:29–34

    Google Scholar 

  • Fuentes-Contreras E, Espinoza JL, Lavandero B, Ramirez CC (2008) Population genetic structure of codling moth (Lepidoptera: Tortricidae) from apple orchards in central Chile. J Econ Entomol 101:190–198. doi:10.1603/0022-0493(2008)101[190:pgsocm]2.0.co;2

    Article  PubMed  Google Scholar 

  • Hedin MC, Maddison WP (2001) A combined molecular approach to phylogeny of the jumping spider subfamily Dendryphantinae (Araneae: Salticidae). Mol Phylogenet Evol 18:386–403

    Article  CAS  PubMed  Google Scholar 

  • Jehle JA, Eberle KE, Asser-Kaiser S, Schulze-Bopp S, Schmitt A (2010) Resistance of codling moth against Cydia pomonella granulovirus (CpGV): state of knowledge. In: FÖKO (ed) 14th international conference on organic fruit-growing, Hohenheim, Germany, 22.–24. pp 133–136

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service, v. 3.23. BMC Genet 6:13

    Article  PubMed  Google Scholar 

  • Labbe P, Lenormand T, Raymond M (2005) On the worldwide spread of an insecticide resistance gene: a role for local selection. J Evolution Biol 18:1471–1484. doi:10.1111/j.1420-9101.2005.00938.x

    Article  CAS  Google Scholar 

  • Lacey LA, Thomson D, Vincent C, Arthurs SP (2008) Codling moth granulovirus: a comprehensive review. Biocontrol Sci Technol 18:639–663. doi:10.1080/09583150802267046

    Article  Google Scholar 

  • Meraner A, Brandstätter A, Thaler R, Aray B, Unterlechner M, Niederstätter H, Parson W, Zelger R, Dalla Via J, Dallinger R (2008) Molecular phylogeny and population structure of the codling moth (Cydia pomonella) in Central Europe: I. Ancient clade splitting revealed by mitochondrial haplotype markers. Mol Phylogenet Evol 48:825–837

    Article  CAS  PubMed  Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reineke A, Karlovsky P, Zebitz CPW (1998) Preparation and purification of DNA from insects for AFLP-analysis. Insect Mol Biol 7:95–99

    Article  CAS  PubMed  Google Scholar 

  • Reyes M, Franck P, Charmillot P-J, Ioriatti C, Olivares J, Pasqualini E, Sauphanor B (2007) Diversity of insecticide resistance mechanisms and spectrum in European populations of the codling moth, Cydia pomonella. Pest Manag Sci 63:890–902

    Article  CAS  PubMed  Google Scholar 

  • Rezapanah M, Shojai-Estabragh S, Huber J, Jehle JA (2008) Molecular and biological characterization of new isolates of Cydia pomonella granulovirus from Iran. J Pest Sci 81:187–191. doi:10.1007/s10340-008-0204-2

    Article  Google Scholar 

  • Sauphanor B, Berling M, Toubon J-F, Reyes M, Delnatte J (2006) Carpocapse des pommes. Cas de résistance aux virus de la granulose dans le Sud-Est. Phytoma—La Défense des Végétaux 590:24–27

  • Schulze-Bopp S, Jehle JA (2012) Development of a direct test of baculovirus resistance in wild codling moth populations. J Appl Entomol (in press: no–no). doi:10.1111/j.1439-0418.2012.01733.x

  • Schumacher P, Weber DC, Hagger C, Dorn S (1997a) Heritability of flight distance for Cydia pomonella. Ent Exp Appl 85:169–175. doi:10.1046/j.1570-7458.1997.00247.x

    Article  Google Scholar 

  • Schumacher P, Weyeneth A, Weber DC, Dorn S (1997b) Long flights in Cydia pomonella L (Lepidoptera: Tortricidae) measured by a flight mill: influence of sex, mated status and age. Physiol Entomol 22:149–160. doi:10.1111/j.1365-3032.1997.tb01152.x

    Article  Google Scholar 

  • Scott KD, Lawrence N, Lange CL, Scott LJ, Wilkinson KS, Merritt MA, Miles M, Murray D, Graham GC (2005) Assessing moth migration and population structuring in Helicoverpa armigera (Lepidoptera : Noctuidae) at the regional scale: example from the Darling Downs, Australia. J Econ Entomol 98:2210–2219

    Article  PubMed  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compliation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Tanada Y (1964) A granulovirus of the codling moth Carpocapsa pomonella (L.) (Lepidoptera: Olethreutidae). J Insect Pathol 6:378–380

    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. Mol Phylogenet Evol 48:838–849

    Article  CAS  PubMed  Google Scholar 

  • Timm AE, Geertsema H, Warnich L (2006) Gene flow among Cydia pomonella (Lepidoptera : Tortricidae) geographic and host populations in South Africa. J Econ Entomol 99:341–348

    Article  CAS  PubMed  Google Scholar 

  • Voudouris CC, Franck P, Olivares J, Sauphanor B, Mamuris Z, Tsitsipis JA, Margaritopoulos JT (2012) Comparing the genetic structure of codling moth Cydia pomonella (L.) from Greece and France: long distance gene-flow in a sedentary pest species. Bull Ent Res 102:185–198. doi:10.1017/S0007485311000563

    Article  Google Scholar 

  • Zehnder G, Gurr GM, Kuhne S, Wade MR, Wratten SD, Wyss E (2007) Arthropod pest management in organic crops. Ann Rev Entomol 52:57–80. doi:10.1146/annurev.ento.52.110405.091337

    Article  CAS  Google Scholar 

  • Zingg D (2008) Madex Plus and Madex I12 overcome virus resistance of codling moth. Paper presented at the 13th international conference on cultivation technique and phytopathological problems in organic fruit-growing, Weinsberg, Germany, 18.–20 February 2008

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Acknowledgments

We thank Dustin Kulanek (Geisenheim) for help during SSR marker analysis and Eva Fritsch, Kathrin Undorf-Spahn (JKI Darmstadt) and Jutta Kienzle (Kernen) for providing codling moth samples. This work was supported by a grant of the Federal Organic Farming Scheme (05OE023/1) by the Federal Agency for Agriculture and Food (BLE) of Germany to the groups in Geisenheim, Neustadt and Darmstadt and by a grant of the “Stiftung Rheinland-Pfalz für Innovation” (grant 0861) to Jes Johannesen.

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Correspondence to Annette Reineke.

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Gund, N.A., Wagner, A., Timm, A.E. et al. Genetic analysis of Cydia pomonella (Lepidoptera: Tortricidae) populations with different levels of sensitivity towards the Cydia pomonella granulovirus (CpGV). Genetica 140, 235–247 (2012). https://doi.org/10.1007/s10709-012-9675-4

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