Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-19T07:34:02.343Z Has data issue: false hasContentIssue false
  • English
  • Français

A novel set of microsatellite markers for the European Grapevine Moth Lobesia botrana isolated using next-generation sequencing and their utility for genetic characterization of populations from Europe and the Middle East

Published online by Cambridge University Press:  08 April 2015

A. Reineke ,
H.A. Assaf ,
D. Kulanek ,
N. Mori ,
A. Pozzebon  and
C. Duso
A. Reineke*
Affiliation:
Department of Phytomedicine, Geisenheim University, D-65366 Geisenheim, Germany
H.A. Assaf
Affiliation:
Department of Phytomedicine, Geisenheim University, D-65366 Geisenheim, Germany Department of Agronomy, Food, Natural Resources, Animals and the Environment, University of Padova, 35020 Legnaro (Padova), Italy
D. Kulanek
Affiliation:
Department of Phytomedicine, Geisenheim University, D-65366 Geisenheim, Germany
N. Mori
Affiliation:
Department of Agronomy, Food, Natural Resources, Animals and the Environment, University of Padova, 35020 Legnaro (Padova), Italy
A. Pozzebon
Affiliation:
Department of Agronomy, Food, Natural Resources, Animals and the Environment, University of Padova, 35020 Legnaro (Padova), Italy
C. Duso
Affiliation:
Department of Agronomy, Food, Natural Resources, Animals and the Environment, University of Padova, 35020 Legnaro (Padova), Italy
*
*Author for correspondence E-mail: annette.reineke@hs-gm.de
Get access Rights & Permissions [Opens in a new window]

Abstract

Using a high-throughput 454 pyrosequencing approach a novel set of microsatellite markers was developed for one of the key grapevine insect pests, the European grapevine moth Lobesia botrana (Lepidoptera: Tortricidae). 20 primer pairs flanking a microsatellite motif were designed based on the sequences obtained and were subsequently evaluated in a sample of 14 L. botrana populations from Europe and the Middle East. 11 markers showed stable and reproducible amplification patterns; however, one of the 11 markers was monomorphic in all L. botrana populations analysed. Estimated frequencies of null alleles of more than 20% were evident for two of the markers tested, but varied substantially depending on the respective L. botrana population. In 12 of the 14 L. botrana populations observed heterozygosities were lower to those expected under Hardy–Weinberg equilibrium, indicating a deficiency of heterozygotes in the respective populations. The overall FST value of 0.075 suggested a moderate but significant genetic differentiation between the L. botrana populations included in this study. In addition, a clear geographic structure was detected in the set of samples, evident through a significant isolation by distance and through results from structure analysis. In structure analysis, L. botrana populations were grouped in two clearly separated clusters according to their European (Spain, Italy, Germany) or Middle Eastern (Israel, Syria, Turkey) origin. This novel set of microsatellite markers can now be applied to study the evolutionary ecology of this species including host shifts and host adaptation as well as spread of individuals across worldwide viticulture.

Keywords

microsatellitesSSR markersLobesia botrana454 pyrosequencingpopulation genetics
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 4 , August 2015 , pp. 408 - 416
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

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

Amsellem, L., Risterucci, A.M. & Benrey, B. (2003) Isolation and characterization of polymorphic microsatellite loci in Lobesia botrana Den. & Schiff. (Lepidoptera: Tortricidae). Molecular Ecology Notes 3, 117–119.Google Scholar
CABI/EPPO (2012) Lobesia botrana. Distribution Map. Wallingford, UK, CABI.Google Scholar
Chapuis, M.-P. & Estoup, A. (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621–631.Google Scholar
Chen, M.H. & 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
Dobes, C.H. & Scheffknecht, S. (2012) Isolation and characterization of microsatellite loci for the Potentilla core group (Rosaceae) using 454 sequencing. Molecular Ecology Resources 12, 726–739.Google Scholar
Earl, D.A. & vonHoldt, B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.CrossRefGoogle Scholar
Endersby, N.M., Ridland, P.M. & Hoffmann, A.A. (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. Bulletin of Entomological Research 98, 145–157.Google Scholar
Espinoza, J.L., Fuentes-Contreras, E., Barros, W. & Ramirez, C. (2007) Utilization of microsatellites to determine genetic variability of the codling moth Cydia pomonella L. (Lepidoptera: Tortricidae) in Central Chile. Agricultura Tecnica 67, 244–252.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, 2611–2620.Google Scholar
Excoffier, L. & Lischer, H.E.L. (2010) Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.Google Scholar
Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.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). Molecular Ecology Notes 5, 99–102.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.Google Scholar
Goudet, J. (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86, 485–486.Google Scholar
Groot, A.T., Marr, M., Heckel, D.G. & Schöfl, G. (2010) The roles and interactions of reproductive isolation mechanisms in fall armyworm (Lepidoptera: Noctuidae) host strains. Ecological Entomology 35, 105–118.Google Scholar
Gund, N., Wagner, A., Timm, A., Schulze-Bopp, S., Jehle, J., Johannesen, J. & Reineke, A. (2012) Genetic analysis of Cydia pomonella (Lepidoptera: Tortricidae) populations with different levels of sensitivity towards the Cydia pomonella granulovirus (CpGV). Genetica 140, 235–247.Google Scholar
Gutierrez, A.P., Ponti, L., Cooper, M.L., Gilioli, G., Baumgartner, J. & Duso, C. (2012) Prospective analysis of the invasive potential of the European grapevine moth Lobesia botrana (Den. & Schiff.) in California. Agricultural and Forest Entomology 14, 225–238.Google Scholar
Jensen, J.L., Bohonak, A.J. & Kelley, S.T. (2005) Isolation by distance, web service, v.3.23. BMC Genetics 6, 13.CrossRefGoogle Scholar
Ji, Y.-J., Zhang, D.X., Hewitt, G.M., Kang, L. & Li, D.-M. (2003) Polymorphic microsatellite loci for the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) and some remarks on their isolation. Molecular Ecology Notes 3, 102–104.CrossRefGoogle Scholar
Kalinowski, S.T., Taper, M.L. & Marshall, T.C. (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16, 1099–1006.Google Scholar
Lombaert, E., Guillemaud, T., Cornuet, J.-M., Malausa, T., Facon, B. & Estoup, A. (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE 5, e9743.Google Scholar
Lozier, J.D., Roderick, G.K. & Mills, N.J. (2009) Molecular markers reveal strong geographic, but not host associated, genetic differentiation in Aphidius transcaspicus, a parasitoid of the aphid genus Hyalopterus . Bulletin of Entomological Research 99, 83–96.Google Scholar
Maher, N. & Thiéry, D. (2006) Daphne gnidium, a possible native host plant of the European grapevine moth Lobesia botrana, stimulates its oviposition. Is a host shift relevant? Chemoecology 16, 135–144.CrossRefGoogle Scholar
Meglécz, E., Petenian, F., Danchin, E., 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, 1693–1700.Google Scholar
Meglécz, E., Anderson, S.J., Bourguet, D., Butcher, R., Caldas, A., Cassel-Lundhagen, A., d'Acier, A.C., Dawson, D.A., Faure, N., Fauvelot, C., Franck, P., Harper, G., Keyghobadi, N., Kluetsch, C., Muthulakshmi, M., Nagaraju, J., Patt, A., Péténian, F., Silvain, J.-F. & Wilcock, H.R. (2007) Microsatellite flanking region similarities among different loci within insect species. Insect Molecular Biology 16, 175–185.Google Scholar
Michel, A.P., Rull, J., Aluja, M. & Feder, J.L. (2007) The genetic structure of hawthorn-infesting Rhagoletis pomonella populations in Mexico: implications for sympatric host race formation. Molecular Ecology 16, 2867–2878.CrossRefGoogle ScholarPubMed
Papura, D., Burban, C., van Helden, M., Giresse, X., Nusillard, B., Guillemaud, T. & Kerdelhue, C. (2012) Microsatellite and mitochondrial data provide evidence for a single major introduction for the neartic leafhopper Scaphoideus titanus in Europe. PLoS ONE 7, e36882.Google Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.Google Scholar
Raymond, M. & Rousset, F. (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.Google Scholar
Reineke, A., Karlovsky, P. & Zebitz, C.P.W. (1998) Preparation and purification of DNA from insects for AFLP-analysis. Insect Molecular Biology 7, 95–99.Google Scholar
Rice, W.R. (1989) Analyzing tables of statistical tests. Evolution 43, 223–225.CrossRefGoogle ScholarPubMed
Roehrich, R. & Boller, E. (1991) Tortricids in Vineyards. pp. 507–514 in Van der Geest, L.P.S. & Evenhuis, H.H. (Eds) Tortricid Pests. Their Biology, Natural Enemies and Control. Amsterdam, Elsevier Science Publishers.Google Scholar
Schmitz, V., Roehrich, R. & Stockel, J. (1996) Dispersal of marked and released Lobesia botrana in a small isolated vineyard and the effect of synthetic sex pheromone on moth movements. Journal International des Sciences de la Vigne et du Vin 30, 67–72.Google Scholar
Schoebel, C.N., Brodbeck, S., Buehler, D., Cornejo, C., Gajurel, J., Hartikainen, H., Keller, D., Leys, M., Říčanová, Š., Segelbacher, G., Werth, S. & Csencsics, D. (2013) Lessons learned from microsatellite development for nonmodel organisms using 454 pyrosequencing. Journal of Evolutionary Biology 26, 600–611.Google Scholar
Schuelke, M. (2000) An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18, 233–234.Google Scholar
Sciarretta, A., Zinni, A., Mazzocchetti, A. & Trematerra, P. (2008) Spatial analysis of Lobesia botrana (Lepidoptera: Tortricidae) male population in a Mediterranean agricultural landscape in Central Italy. Environmental Entomology 37, 382–390.Google Scholar
Sinama, M., Dubut, V., Costedoat, C., Gilles, A., Junker, M., Malausa, T., Martin, J.-F., Neve, G., Pech, N., Schmitt, T., Zimmermann, M. & Meglécz, E. (2011) Challenges of microsatellite development in Lepidoptera: Euphydryas aurinia (Nymphalidae) as a case study. European Journal of Entomology 108, 261–266.Google Scholar
Stellwaag, F. (1928) Die Weinbauinsekten der Kulturländer. Berlin, Paul Parey.Google Scholar
Svobodova, E., Trnka, M., Dubrovsky, M., Semeradova, D., Eitzinger, J., Stepanek, P. & Zalud, Z. (2014a) Determination of areas with the most significant shift in persistence of pests in Europe under climate change. Pest Management Science 70, 708–715.Google Scholar
Svobodova, E., Trnka, M., Zalud, Z., Semeradova, D., Dubrovsky, M., Eitzinger, J., Štepanek, P. & Brazdil, R. (2014b) Climate variability and potential distribution of selected pest species in south Moravia and north-east Austria in the past 200 years – lessons for the future. Journal of Agricultural Science 152, 225–237.Google Scholar
Thiéry, D. & Moreau, J. (2005) Relative performance of European grapevine moth (Lobesia botrana) on grapes and other hosts. Oecologia 143, 548–557.Google Scholar
Torriani, M.V.G., Mazzi, D., Hein, S. & Dorn, S. (2010) Structured populations of the oriental fruit moth in an agricultural ecosystem. Molecular Ecology 19, 2651–2660.CrossRefGoogle Scholar
Van't Hof, A.E., Zwaan, B.J., Saccheri, I.J., Daly, D., Bot, A.N.M. & Brakefield, P.M. (2005) Characterization of 28 microsatellite loci for the butterfly Bicyclus anynana . Molecular Ecology Notes 5, 169–172.Google Scholar
Vogelweith, F., Dourneau, M., Thiéry, D., Moret, Y. & Moreau, J. (2013) Geographical variation in parasitism shapes larval immune function in a phytophagous insect. Naturwissenschaften 100, 1149–1161.Google Scholar
Voudouris, C.C., Franck, P., Olivares, J., Sauphanor, B., Mamuris, Z., Tsitsipis, J.A. & Margaritopoulos, J.T. (2012) Comparing the genetic structure of codling moth Cydia pomonella (L.) from Greece and France: long distance gene-flow in a sedentary pest species. Bulletin of Entomological Research 102, 185–198.Google Scholar
Zane, L., Bargelloni, L. & Patarnello, T. (2002) Strategies for microsatellite isolation: a review. Molecular Ecology 11, 1–16.Google Scholar
Zhang, D.-X. (2004) Lepidopteran microsatellite DNA: redundant but promising. Trends in Ecology and Evolution 19, 507–509.Google Scholar