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Comparative analysis of microsatellite loci in four fruit fly species of the genus Ceratitis (Diptera: Tephritidae)

Published online by Cambridge University Press:  09 March 2007

F.N. Baliraine ,
M. Bonizzoni ,
E.O. Osir ,
S.A. Lux ,
F.J. Mulaa ,
L. Zheng ,
L.M. Gomulski ,
G. Gasperi  and
A.R. Malacrida
F.N. Baliraine
Affiliation:
International Centre of Insect Physiology and Ecology (ICIPE), PO Box 30772, Nairobi, Kenya Dipartimento di Biologia Animale, Piazza Botta 9, 27100 Pavia, Italia Department of Biochemistry, University of Nairobi, PO Box 30197, Nairobi, Kenya
M. Bonizzoni
Affiliation:
Dipartimento di Biologia Animale, Piazza Botta 9, 27100 Pavia, Italia
E.O. Osir
Affiliation:
International Centre of Insect Physiology and Ecology (ICIPE), PO Box 30772, Nairobi, Kenya
S.A. Lux
Affiliation:
International Centre of Insect Physiology and Ecology (ICIPE), PO Box 30772, Nairobi, Kenya
F.J. Mulaa
Affiliation:
Department of Biochemistry, University of Nairobi, PO Box 30197, Nairobi, Kenya
L. Zheng
Affiliation:
Yale University School of Medicine, Department of Epidemiology and Public Health, New Haven, CT 06520, USA
L.M. Gomulski
Affiliation:
Dipartimento di Biologia Animale, Piazza Botta 9, 27100 Pavia, Italia
G. Gasperi
Affiliation:
Dipartimento di Biologia Animale, Piazza Botta 9, 27100 Pavia, Italia
A.R. Malacrida*
Affiliation:
Dipartimento di Biologia Animale, Piazza Botta 9, 27100 Pavia, Italia
*
*Fax: 0039 0382 506294 E-mail: malacrid@unipv.it
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Abstract

The possibility to cross-species amplify microsatellites in fruit flies of the genus Ceratitis was tested with the polymerase chain reaction (PCR) by analysing 23 Ceratitis capitata (Wiedemann) microsatellite markers on the genomic DNA of three other economically important, congeneric species: C. rosa (Karsch), C. fasciventris (Bezzi) and C. cosyra (Walker). Twenty-two primer pairs produced amplification products in at least one of the three species tested. The majority of the products were similar, if not identical in size to those expected in C. capitata. The structures of the repeat motifs and their flanking sequences were examined for a total of 79 alleles from the three species. Sequence analysis revealed the same repeat type as the homologous C. capitata microsatellites in the majority of the loci, suggesting their utility for population analysis across the species range. A total of seven loci were differentially present/absent in C. capitata, C. rosa, C. fasciventris and C. cosyra, suggesting that it may be possible to differentiate these four species using a simple sequence repeat-based PCR assay. It is proposed that medfly-based microsatellite markers could be utilized in the identification and tracing of the geographical origins of colonist pest populations of the four tested species and in the assessment of their risk and invasive potentials; thereby assisting regulatory authorities in implementing quarantine restrictions and other pest control measures.

Type
Research Article
Information
Bulletin of Entomological Research , Volume 93 , Issue 1 , January 2003 , pp. 1 - 10
Copyright
Copyright © Cambridge University Press 2003

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References

Ashkenazi, V., Chani, E., Lavi, U., Levy, D., Hillel, J. & Veilleux, R.E. (2001) Development of microsatellite markers in potato and their use in phylogenetic and fingerprinting analyses. Genome 44, 50–62.CrossRefGoogle ScholarPubMed
Armstrong, K.F., Cameron, C.M. & Frampton, E.R. (1997) Fruit fly (Diptera: Tephritidae) species identification: a rapid molecular diagnostic technique for quarantine application. Bulletin of Entomogical Research 87, 111–118.CrossRefGoogle Scholar
Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. & Struhl, K. (2001) In Current protocols in molecular biology. New York, John Wiley & Sons: Inc.CrossRefGoogle Scholar
Baratti, M., Alberti, A., Groenen, M., Veenendaal, T. & Fulgheri, F.D. (2001) Polymorphic microsatellites developed by cross-species amplification in common pheasant breeds. Animal Genetics 32, 222–225.CrossRefGoogle ScholarPubMed
Baruffi, L., Damiani, G., Guglielmino, G.R., Bandi, C., Malacrida, A.R. & Gasperi, G. (1995) Polymorphism within and between populations of Ceratitis capitata: comparison between RAPD and multilocus enzyme electrophoresis data. Heredity 74, 425–437.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Bruford, M.W. & Wayne, R.K. (1993) Microsatellites and their application to population genetic studies. Current Opinions in Genetics and Development 3, 939–943.CrossRefGoogle ScholarPubMed
Casey, D.G. & Burnell, M. (2001) The isolation of microsatellite loci in the Mediterranean fruit fly Ceratitis capitata (Diptera: Tephritidae) using a biotin/ streptavidin enrichment technique. Molecular Ecology Notes 1, 120–122.CrossRefGoogle Scholar
Colson, I. & Goldstein, D.B. (1999) Evidence for complex mutations at microsatellite loci in Drosophila. Genetics 152, 617–627.CrossRefGoogle ScholarPubMed
Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research 16, 10881–10890.CrossRefGoogle ScholarPubMed
Crawford, A.M., Kappes, S.M., Paterson, K.A., deGotari, M.J., Dodds, K.G., Freking, B.A., Stone, R.T. & Beattie, C.W. (1998) Microsatellite evolution: testing the ascertainment bias hypothesis. Journal of Molecular Evolution 46, 256–260.CrossRefGoogle ScholarPubMed
De Meyer, M. (1999) Phylogeny of the genus Ceratitis (Dacinae: Ceratitidini). In Fruit flies (Tephritidae): phylogeny and evolution of behavior. pp 409–428. [Aluja, M. and Norrbom, A.L., editors]. New York: CRC Press.CrossRefGoogle Scholar
De Meyer, M. (2001) On the identity of the Natal fruit fly Ceratitis rosa Karsch (Diptera, Tephritidae). Entomologie 71, 55–62.Google Scholar
De Meyer, M. (2001) Distribution patterns and host-plant relationships within the genus Ceratitis MacLeay (Diptera: Tephritidae) in Africa. Cimbebasia 17, 219–228.Google Scholar
Douglas, L.J. & Haymer, D.S. (2001) Ribosomal ITS1 polymorphism in Ceratitis capitata and Ceratitis rosa (Diptera: Tephritidae). Annals of the Entomological Society of America 94, 726–731.CrossRefGoogle Scholar
Duyck, P.F. & Quilici, S. (2002) Survival and development of different life stages of three Ceratitis spp. (Diptera: Tephritidae) reared at five constant temperatures. Bulletin of Entomological Research 92, 461–469.CrossRefGoogle ScholarPubMed
Ellegren, H., Primmer, C.R. & Sheldon, B.C. (1995) Microsatellite ‘evolution‘: directionally or bias?. Nature Genetics 11, 359–360.CrossRefGoogle ScholarPubMed
Estoup, A., Tailliez, C., Cornuet, J.M. & Solignac, M. (1995) Size homoplasy and mutational processes of interrupted microsatellites in two bee species, Apis mellifera and Bombus terrestris (Apidae). Molecular Biology and Evolution 12, 1074–1084.Google ScholarPubMed
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 ScholarPubMed
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 ScholarPubMed
Gomulski, L.M., Bourtzis, K., Brogna, S., Morandi, P.A., Bonvicini, C., Sebastiani, F., Torti, C., Guglielmino, C.R., Savakis, C., Gasperi, G. & Malacrida, A.R. (1998) Intron size polymorphism of the Adh1 gene parallels the worldwide colonization history of the Mediterranean fruit fly, Ceratitis capitata. Molecular Ecology 7, 1729–1741.CrossRefGoogle Scholar
Han, H.-Y. & McPheron, B. (1997) Molecular phylogenetic study of Tephritidae (Insecta: Diptera) using partial sequences of the mitochondrial 16S ribosomal DNA. Molecular Phylogenetics and Evolution 7, 17–32.CrossRefGoogle ScholarPubMed
Han, H.-Y. & McPheron, B. (1999) Nucleotide sequence data as a tool to test phylogenetic relationships among higher groups of Tephritidae: a case study using mitochondrial ribosomal DNA. pp 115–132 in Aluja, M. & Norrbom, A.L. (Eds). Fruit flies (Tephritidae): phylogeny and evolution of behavior. New York, CRC Press.Google Scholar
Hancock, J.M. (1996) Simple sequences and the expanding genome. BioEssays 18, 421–425.CrossRefGoogle ScholarPubMed
Harr, B. & Schlötterer, C. (2000) Long microsatellite alleles in D. melanogaster have a downward mutation bias and short time persistence times, which cause their genome wide under-representation. Genetics 155, 1213–1220.CrossRefGoogle Scholar
Harr, B., Zangerl, B. & Schlötterer, C. (2000) Evidence of microsatellite interruptions by DNA replication slippage: phylogenetic evidence from. Drosophila. Molecular Biology and Evolution 17, 1001–1009CrossRefGoogle ScholarPubMed
Hedrick, P.W., Parker, K.M. & Lee, R.N. (2001) Using microsatellite and MHC variation to identify species, ESUs, and Mus in the endangered Sonoran topminnow. Molecular Ecology 10, 1399–1412.CrossRefGoogle ScholarPubMed
Hutter, C.M., Schug, M.D. & Aquadro, C.F. (1998) Microsatellite variation in Drosophila melanogaster and Drosophila simulans: a reciprocal test of the ascertainment bias hypothesis. Molecular Biology and Evolution 12, 1620–1636.CrossRefGoogle Scholar
Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G. & Gibson, T.J. (1998) Multiple sequence alignment with Clustal X. Trends in Biochemical Science 23, 403–405.CrossRefGoogle ScholarPubMed
Kakuoli-Duarte, T., Casey, D.G. & Burnell, A.M. (2001) Development of a diagnostic DNA probe for the fruit flies Ceratitis capitata and Ceratitis rosa (Diptera: Tephritidae) using amplified fragment-length polymorphism. Journal of Economic Entomology 94, 989–997.CrossRefGoogle Scholar
Knipling, E.F. (1992) Principles of insect parasitism analyzed from new perspectives: practical implications for regulating insect populations by biological means. United States Department of Agriculture Handbook No. 693. 1–148.Google Scholar
Loridon, K., Cournoyer, B., Goubely, C., Depeiges, A. & Picard, G. (1998) Length polymorphism and allele structure of trinucleotide microsatellites in natural accessions of Arabidopsis thaliana. Theoretical and Applied Genetics 97, 597–604.CrossRefGoogle Scholar
Lux, S.A., Overholt, W., Kimani, N., Maniania, N., Miller, S. & Osir, E. (1995) Sustainable pest management for fruit crops. pp 29–33. in 1995–1997 ICIPE Annual Scientific Report. The International Centre of Insect Physiology and Ecology, Nairobi, Kenya.Google Scholar
Malacrida, A.R., Marinoni, F., Torti, C., Gomulski, L.M., Sebastiani, F., Bonvivini, C., Gasperi, G. & Guglielmnino, C.R. (1998) Genetic aspects of the worldwide colonization process of Ceratitis capitata. Journal of Heredity 89, 501–507.CrossRefGoogle ScholarPubMed
Marck, C. (1989) DNA Strider: a computer program for DNA and protein sequences analysis. Commissariat à l'Energie Atomique, France.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, 891–900.CrossRefGoogle ScholarPubMed
Morrow, J., Scott, L., Congdon, B., Yeates, D., Frommer, M. & Sved, J. (2000) Close genetic similarity between two sympatric species of tephritid fruit fly reproductively isolated by mating time. Evolution 54, 899–910.Google ScholarPubMed
Primmer, C.R., Møller, A.P. & Ellegren, H. (1996) A wide-range survey of cross-species microsatellite amplification in birds. Molecular Ecology 5, 365–378.CrossRefGoogle ScholarPubMed
Rubinsztein, D.C., Amos, W., Leggo, J., Goodburn, S., Jain, S., Li, S.-H., Margolis, L., Ross, A.A. & Ferguson-Smith, M.A. (1995) Microsatellite evolution – evidence for directionality and variation in rate between species. Nature Genetics 10, 337–343.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) In Molecular cloning, a laboratory manual. 2nd edn. New York: Cold Spring Harbor Laboratory Press.Google Scholar
Schlötterer, C. (1998) Are microsatellites really simple sequences?. Current Biology 8, R132 – R134.CrossRefGoogle ScholarPubMed
Schlötterer, C. & Harr, B. (2000) Drosophila virilis has long and highly polymorphic microsatellites. Molecular Biology and Evolution 17, 1641–1646.CrossRefGoogle ScholarPubMed
Schlötterer, C. & Zangerl, B. (1999) The use of imperfect microsatellites for DNA fingerprinting and population genetics. pp 153–165. in Epplen, J.T. & Lubjuhn, T. (Eds) DNA profiling and DNA fingerprinting. Basel: Birkhauser.CrossRefGoogle Scholar
Sonvico, A., Manso, F. & Quesada-Allue, L.A. (1996) Discrimination between the immature stages of Ceratitis capitata and Anastrepha fraterculus (Diptera: Tephritidae) populations by random amplified polymorphic DNA polymerase chain reaction. Journal of Economic Entomology 89, 1208–1212.CrossRefGoogle ScholarPubMed
Steck, G.J. & Wharton, R.A. (1988) Description of the immature stages of Anastrepha interrupta, A. linae, and A. grandis (Diptera: Tephritidae). Annals of the Entomological Society of America 81, 994–1003.CrossRefGoogle Scholar
Steck, G.J., Carroll, L.E., Celedonio-Hurtado, H. & Guillen-Aguilar, J. (1990) Methods for identification of Anastrepha larvae (Diptera: Tephritidae), and key to 13 species. Proceedings of the Entomological Society of Washington 92, 333–346.Google Scholar
Tautz, D. & Schlötterer, C. (1994) Simple sequences. Current Opinions in Genetics and Development 4, 832–837.CrossRefGoogle ScholarPubMed
Torti, C., Gomulski, L.M., Malacrida, A.R., Capy, P. & Gasperi, G. (1998) Characterization and evolution of mariner elements from closely related species of fruit flies (Diptera: Tephritidae). Journal of Molecular Evolution 46, 288–298.CrossRefGoogle Scholar
van Oppen, M.J.H., Rico, C., Turner, G.F. & Hewitt, G.M. (2000) Extensive homoplasy, nonstepwise mutations, and shared ancestral polymorphism at a complex microsatellite locus in lake Malawi cichlids. Molecular Biology and Evolution 17, 489–498.CrossRefGoogle Scholar
van Treuren, R., Kuittinen, H., Karkkainen, K., Baena-Gonzales, E. & Savolainen, O. (1997) Evolution of microsatellite in Arabis petraea and Arabis lyrata, outcrossing relatives of Arabidopsis thaliana. Molecular Biology and Evolution 14, 220–229.CrossRefGoogle ScholarPubMed
Viard, F., Franck, P., Dubois, M.P., Estoup, A. & Jarne, P. (1998) Variation of microsatellite size homoplasy across electromorphs, loci, and populations in three invertebrate species. Journal of Molecular Evolution 47, 42–51.CrossRefGoogle ScholarPubMed
White, I.M. & Elson-Harris, M.M. (1992) Fruit flies of economic significance: their identification and bionomics. 601 pp. Wallingford, CAB International, and Canberra: ACIAR.CrossRefGoogle Scholar
Zhu, Y., Queller, D.C. & Strassmann, J.E. (2000) A phylogenetic perspective on sequence evolution in microsatellite loci. Journal of Molecular Evolution 50, 324–338.CrossRefGoogle ScholarPubMed