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Cross-amplified microsatellites in the European cherry fly, Rhagoletis cerasi: medium polymorphic–highly informative markers

Published online by Cambridge University Press:  08 July 2010

A.A. Augustinos ,
A.K. Asimakopoulou ,
N.T. Papadopoulos  and
K. Bourtzis
A.A. Augustinos*
Affiliation:
Department of Environmental and Natural Resources Management, University of Ioannina, 2, Seferi St., 30100Agrinio, Greece Department of Biology, University of Patras, Greece Department of Biochemistry and Biotechnology, University of Thessaly, Greece
A.K. Asimakopoulou
Affiliation:
Department of Biochemistry and Biotechnology, University of Thessaly, Greece
N.T. Papadopoulos
Affiliation:
Department of Agriculture, Crop Production, and Agricultural Environment, University of Thessaly, Greece
K. Bourtzis
Affiliation:
Department of Environmental and Natural Resources Management, University of Ioannina, 2, Seferi St., 30100Agrinio, Greece
*
*Author for correspondence Fax: 30-26410-74171 E-mail: augustin@cc.uoi.gr, augustin@upatras.gr
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Abstract

The European cherry fruit fly, Rhagoletis cerasi (Diptera: Tephritidae), is a major pest of cherries in Europe and parts of Asia. Despite its big economic significance, there is a lack of studies on the genetic structure of its natural populations. Knowledge about an insect pest on molecular, genetic and population levels facilitates the development of environmentally friendly control methods. In this study, we present the development of 13 microsatellite markers for R. cerasi, through cross-species amplification. These markers have been used for the genotyping of 130 individuals from five different sampling sites in Greece. Our results indicate that (i) cross-species amplification is a versatile and rapid tool for developing microsatellite markers in Rhagoletis spp., (ii) the microsatellite markers presented here constitute an important tool for population studies on this pest, and (iii) there is clear structuring of natural European cherry fly populations.

Keywords

Rhagoletis cerasiTephritidaemicrosatellitescross-species amplificationpopulation analysis
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 101 , Issue 1 , February 2011 , pp. 45 - 52
Copyright
Copyright © Cambridge University Press 2010

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References

Aketarawong, N., Bonizzoni, M., Thanaphum, S., Gomulski, L.M., Gasperi, G., Malacrida, A.R. & Gugliemino, C.R. (2007) Inferences on the population structure and colonization process of the invasive oriental fruit fly, Bactrocera dorsalis (Hendel). Molecular Ecology 16, 3522–3532.Google Scholar
Arthofer, W., Krumböck, S., Schuler, H., Rasool, B., Riegler, M., Köppler, K. & Stauffer, C. (2009a) Thirteen new microsatellite loci in Rhagoletis cerasi (Diptera: Tephritidae), a model host species for Wolbachia symbiosis in field populations. Molecular Ecology Resources 9, 1460–1466.Google Scholar
Arthofer, W., Riegler, M., Schneider, D., Krammer, M., Miller, W.J. & Stauffer, C. (2009b) Hidden Wolbachia diversity in field populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera, Tephritidae). Molecular Ecology 18, 3816–3830.Google Scholar
Ashburner, M. (1989) Drosophila: A Laboratory Manual. New York, Cold Spring Harbour Laboratory Press.Google Scholar
Augustinos, A.A., Mamuris, Z., Stratikopoulos, E., D'Amelio, S., Zacharopoulou, A. & Mathiopoulos, K.D. (2005) Microsatellite analysis of olive fly populations in the Mediterranean indicates a westward expansion of the species. Genetica 125, 231–241.Google Scholar
Augustinos, A.A., Stratikopoulos, E.E., Drosopoulou, E., Kakani, E.G., Mavragani-Tsipidou, P., Zacharopoulou, A. & Mathiopoulos, K.D. (2008) Isolation and characterization of microsatellite markers from the olive fly, Bactrocera oleae, and their cross-species amplification in the Tephritidae family. BMC genomics 9, 618.Google Scholar
Baliraine, F.N., Bonizzoni, M., Osir, E.O., Lux, S.A., Mulaa, F.J., Zheng, L., Gomulski, L.M., Gasperi, G. & Malacrida, A.R. (2003) Comparative analysis of microsatellite loci in four fruit fly species of the genus Ceratitis (Diptera: Tephritidae). Bulletin of Entomological Research 93, 1–10.Google Scholar
Baliraine, F.N., Bonizzoni, M., Guglielmino, C.R., Osir, E.O., Lux, S.A., Mulaa, F.J., Gomulski, L.M., Zheng, L., Quilici, S., Gasperi, G. & Malacrida, A.R. (2004) Population genetics of the potentially invasive African fruit fly species, Ceratitis rosa and Ceratitis fasciventris (Diptera: Tephritidae). Molecular Ecology 13, 683–695.CrossRefGoogle Scholar
Boller, E.F. & Prokopy, R.J. (1976) Bionomics and management of Rhagoletis. Annual Reviews of Entomology 21, 223–246.CrossRefGoogle Scholar
Boller, E.F., Katsoyannos, B.I. & Hippe, C. (1998) Host races of Rhagoletis cerasi L. (Dipt., Tephritidae): Effect of prior adult experience on oviposition site preference. Journal of Applied Entomology 122, 231–237.Google Scholar
Bonizzoni, M., Malacrida, A.R., Guglielmino, C.R., Gomulski, L.M., Gasperi, G. & Zheng, L. (2000) Microsatellite polymorphism in the Mediterranean fruit fly, Ceratitis capitata. Insect Molecular Biology 9, 251–261.Google Scholar
Bonizzoni, M., Zheng, L., Guglielmino, C.R., Haymer, D.S., Gasperi, G., Gomulski, L.M. & Malacrida, A.R. (2001) Microsatellite analysis of medfly bioinfestations in California. Molecular Ecology 10, 2515–2524.Google Scholar
Bonizzoni, M., Katsoyannos, B.I., Marguerie, R., Guglielmino, C.R., Gasperi, G., Malacrida, A. & Chapman, T. (2002) Microsatellite analysis reveals remating by wild Mediterranean fruit fly females, Ceratitis capitata. Molecular Ecology 11, 1915–1921.CrossRefGoogle ScholarPubMed
Bonizzoni, M., Guglielmino, C.R., Smallridge, C.J., Gomulski, M., Malacrida, A.R. & Gasperi, G. (2004) On the origins of medfly invasion and expansion in Australia. Molecular Ecology 13, 3845–3855.Google Scholar
Bonizzoni, M., Gomulski, L.M., Mossinson, S., Guglielmino, C.R., Malacrida, A.R., Yuval, B. & Gasperi, G. (2006) Is polyandry a common event among wild populations of the pest Ceratitis capitata? Journal of Economic Entomology 99, 1420–1429.Google Scholar
Bourtzis, K. (2008) Wolbachia-based technologies for insect pest control. in Aksoy, S. (Ed.) Transgenesis and the Management of Vector-Borne Disease, Advances in Experimental Medicine and Biology 627, 104–113.Google Scholar
Cameron, E.C., Sved, J.A. & Gilchrist, A.S. (2010) Pest fruit fly (Diptera: Tephritidae) in northwestern Australia: one species or two? Bulletin of Entomological Research 100, 197–206.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.CrossRefGoogle ScholarPubMed
Fimiani, P. (1989) Mediterranean regin. pp. 39–50 in Robinson, A.S. & Hopper, G. (Eds) Fruit Flies: Their Biology, Natural Enemies and Control. Amsterdam, the Netherlands, Elsevier.Google Scholar
Fitzsimmons, N.N., Moritz, C. & Moore, S.S. (1995) Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Molecular Biology and Evolution 12, 432–440.Google Scholar
Forbes, S.H., Hogg, J.T., Buchanan, F.C., Crawford, A.M. & Allendorf, F.W. (1995) Microsatellite evolution in congeneric mammals: Domestic and bighorn sheep. Molecular Biology and Evolution 12, 1106–1113.Google Scholar
Gilchrist, A.S., Sved, J.A. & Meats, A. (2004) Genetic relations between outbreaks of the Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae), in Adelaide in 2000 and 2002. Australian Journal of Entomology 43, 157–163.Google Scholar
Goudet, J. (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3).Google Scholar
Katsoyannos, B.I., Papadopoulos, N.T. & Stavridis, D. (2000) Evaluation of trap types and food attractants for Rhagoletis cerasi (Diptera: Tephritidae). Journal of Economic Entomology 93, 1005–1010.CrossRefGoogle Scholar
Kounatidis, I., Papadopoulos, N., Bourtzis, K. & Mavragani-Tsipidou, P. (2008) Genetic and cytogenetic analysis of the fruit fly Rhagoletis cerasi (Diptera: Tephritidae). Genome 51, 479–491.Google Scholar
Kovanci, O.B. & Kovanci, B. (2006) Effect of altitude on seasonal flight activity of Rhagoletis cerasi flies (Diptera: Tephritidae). Bulletin of Entomological Research 96, 345–351.Google Scholar
Kraaijeveld, K., Katsoyannos, B.I., Stavrinides, M., Kouloussis, N.A. & Chapman, T. (2005) Remating in wild females of the Mediterranean fruit fly, Ceratitis capitata. Animal Behaviour 69, 771–776.CrossRefGoogle Scholar
Maxwell, S.A., Rasic, G. & Keyghobadi, N. (2009) Characterization of microsatellite loci for the western cherry fruit fly, Rhagoletis indifferens (Diptera: Tephritidae). Molecular Ecology Resources 9, 1025–1028.Google Scholar
Meixner, M.D., Mcpheron, B.A., Silva, J.G., Gasparich, G.E. & Sheppard, W.S. (2002) The Mediterranean fruit fly in California: Evidence for multiple introductions and persistent populations based on microsatellite and mitochondrial DNA variability. Molecular Ecology 11, 891–899.CrossRefGoogle ScholarPubMed
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.Google Scholar
Nardi, F., Carapelli, A., Dallai, R., Roderick, G.K. & Frati, F. (2005) Population structure and colonization history of the olive fly, Bactrocera oleae (Diptera, Tephritidae). Molecular Ecology 14, 2729–2738.Google Scholar
Nei, M. (1972) Genetic distance between populations. American Naturalist 106, 283–292.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.Google Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.Google Scholar
Ranson, H., Paton, M.G., Jensen, B., McCarroll, L., Vaughan, A., Hogan, J.R., Hemingway, J. & Collins, F.H. (2004) Genetic mapping of genes conferring permethrin resistance in the malaria vector, Anopheles gambiae. Insect Molecular Biology 13, 379–386.Google Scholar
Raymond, M. & Rousset, F. (1995) GENEPOP v.1.2: population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.Google Scholar
Riegler, M. & Stauffer, C. (2002) Wolbachia infections and superinfections in cytoplasmically incompatible populations of the European cherry fruit fly Rhagoletis cerasi (Diptera, Tephritidae). Molecular Ecology 11, 2425–2434.Google Scholar
Rubinsztein, D.C., Amos, W., Leggo, J., Goodburn, S., Jain, S., Li, S.H., Margolis, R.L., Ross, C.A. & Ferguson-Smith, M.A. (1995) Microsatellite evolution – Evidence for directionality and variation in rate between species. Nature Genetics 10, 337–343.Google Scholar
Saridaki, A. & Bourtzis, K. Wolbachia: more than just a bug in insects' genitals. Current Opinion in Microbiology, in press.Google Scholar
Schwarz, D., McPheron, B.A., Hartl, G.B., Boller, E.F. & Hoffmeister, T.S. (2003) A second case of genetic host races in Rhagoletis? A population genetic comparison of sympatric host populations in the European cherry fruit fly, Rhagoletis cerasi. Entomologia Experimentalis et Applicata 108, 11–17.Google Scholar
Shearman, D.C.A., Gilchrist, A.S., Crisafulli, D., Graham, G., Lange, C. & Frommer, M. (2006) Microsatellite markers for the pest fruit fly, Bactrocera papayae (Diptera: Tephritidae) and other Bactrocera species. Molecular Ecology Notes 6, 4–7.Google Scholar
Silva, J.G., Meixner, M.D., McPheron, B.A., Steck, G.J. & Sheppard, W.S. (2003) Recent Mediterranean Fruit Fly (Diptera: Tephritidae) Infestations in Florida – A Genetic Perspective. Journal of Economic Entomology 96, 1711–1718.Google Scholar
Song, S.D., Drew, R.A.I. & Hughes, J.M. (2007) Multiple paternity in a natural population of a wild tobacco fly, Bactrocera cacuminata (Diptera: Tephritidae), assessed by microsatellite DNA markers. Molecular Ecology 16, 2353–2361.CrossRefGoogle Scholar
Stratikopoulos, E.E., Augustinos, A.A., Petalas, Y.G., Vrahatis, M.N., Mintzas, A., Mathiopoulos, K.D. & Zacharopoulou, A. (2008) An integrated genetic and cytogenetic map for the Mediterranean fruit fly, Ceratitis capitata, based on microsatellite and morphological markers. Genetica 133, 147–157.Google Scholar
Stratikopoulos, E.E., Augustinos, A.A., Pavlopoulos, I., Economou, K., Mintzas, A., Mathiopoulos, K.D. & Zacharopoulou, A. (2009) Isolation and characterization of microsatellite markers from the Mediterranean fruit fly, Ceratitis capitata: cross-species amplification in other Tephritidae species reveals a varying degree of motif conservation. Molecular Genetics and Genomics 282, 283–306.Google Scholar
Velez, S., Taylor, M.S., Noor, M.A.F., Lobo, N.F. & Feder, J.L. (2006) Isolation and characterization of microsatellite loci from the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae). Molecular Ecology Notes 6, 90–92.Google Scholar
White, I.M. & Elson-Harris, M.M. (1992) Fruit Flies of Economic Significance: Their Identification and Bionomics. Wallingford, UK, CAB International.Google Scholar
Wondji, C.S., Morgan, J., Coetzee, M., Hunt, R.H., Steen, K., Black, W.C. IV, Hemingway, J. & Ranson, H. (2007) Mapping a Quantitative Trait Locus (QTL) conferring pyrethroid resistance in the African malaria vector Anopheles funestus. BMC Genomics 8, 34.Google Scholar
Yeh, F.C., Boyle, T., Rongcai, Y., Ye, Z. & Xiyan, J.M. (1999) Popgene version 1.31. Microsoft window-based Freeware for population Genetic Analysis. Edmonton, University of Alberta.Google Scholar
Yu, H., Frommer, M., Robson, M.K., Meats, A.W., Shearman, D.C.A. & Sved, J.A. (2001) Microsatellite analysis of the Queensland fruit fly Bactrocera tryoni (Diptera: Tephritidae) indicates spatial structuring: Implications for population control. Bulletin of Entomological Research 91, 139–147.Google Scholar
Zabalou, S., Riegler, M., Theodorakopoulou, M., Stauffer, C., Savakis, C. & Bourtzis, K. (2004) Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proceedings of the National Academy of Sciences of the United States of America 101, 15042–15045.Google Scholar
Zabalou, S., Apostolaki, A., Livadaras, I., Franz, G., Robinson, A.S., Savakis, C. & Bourtzis, K. (2009) Incompatible Insect Technique: Incompatible Males from a Ceratitis capitata (Diptera: Tephritidae) Genetic Sexing Strain. Entomologia Experimentalis et Applicata 132, 232–240.CrossRefGoogle Scholar
Zheng, L. (1997) Microsatellite mapping of insect genomes. pp. 321–329 in Crampton, J.M., Beard, C.B. & Louis, C. (Eds) Molecular Biology of Insect Disease Vectors: A Methods Manual. London, Chapman & Hall.CrossRefGoogle Scholar
Zygouridis, N.E., Augustinos, A.A., Zalom, F.G. & Mathiopoulos, K.D. (2009) Analysis of olive fly invasion in California based on microsatellite markers. Heredity 102, 402–412.CrossRefGoogle ScholarPubMed