Skip to main content
SpringerLink
Log in

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 transferability

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The Mediterranean fruit fly, Ceratitis capitata, is a pest of major economic importance and has become a model for the development of SIT control programs for insect pests. Significant information has been accumulated on classical and population genetics of this species during the past 2 decades. However, the availability of molecular markers is limited. Here, we present the isolation and characterization of 159 microsatellite clones and the development of 108 polymorphic microsatellite markers for this insect pest. Mapping by in situ hybridization to polytene chromosomes of 21 microsatellite clones enriched the cytogenetic map that was previously constructed by our group. The enriched map provides a large number of STSs for future genome mapping projects. Cross-species amplification of these microsatellite loci in 12 Tephritidae species and sequence analysis of several amplification products indicated a varying degree of transferability and their possible usefulness as molecular and genetic markers in these species where genetic and molecular tools are limited.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams MD, Celniker SE, Holt RA et al (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195

    Article  PubMed  Google Scholar 

  • Alphey LS (2007) Engineering insects for the sterile insect technique. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Springer, Netherlands, pp 51–60

    Chapter  Google Scholar 

  • Ashburner M (1989) Drosophila: a laboratory manual. Cold Spring Harbour Laboratory Press, New York, pp 108–109

    Google Scholar 

  • Augustinos AA, Stratikopoulos EE, Drosopoulou E, Kakani EG, Mavragani-Tsipidou P, Zacharopoulou A, Mathiopoulos KD (2008) Isolation and characterization of polymorphic microsatellite markers from the olive fly, Bactrocera oleae, and their cross-species amplification in the Tephritidae family. BMC Genomics 9:618

    Article  PubMed  Google Scholar 

  • Bachtrog D, Weiss S, Zangerl B, Brem G, Schlötterer C (1999) Distribution of dinucleotide microsatellites in the Drosophila melanogaster genome. Mol Biol Evol 16:602–610

    PubMed  CAS  Google Scholar 

  • Baliraine FN, Bonizzoni M, EO Osir, Lux SA, Mulaa FJ, Zheng L, Gomulski LM, Gasperi G, Malacrida AR (2003) Comparative analysis of microsatellite loci in four fruit fly species of the genus Ceratitis (Diptera: Tephritidae). Bul Entom Res 93:1–10

    CAS  Google Scholar 

  • Barbará T, Palma-Silva C, Paggi GM, Bered F, Fay MF, Lexer C (2007) Cross-species transfer of nuclear microsatellite markers: potential and limitations. Mol Ecol 16:3759–3767

    Article  PubMed  Google Scholar 

  • Bonizzoni M, Malacrida AR, Guglielmino CR, Gomulski LM, Gasperi G, Zheng L (2000) Microsatellite polymorphism in the Mediterranean fruit fly, Ceratitis capitata. Insect Mol Biol 9:251–261

    Article  PubMed  CAS  Google Scholar 

  • Bonizzoni M, Zheng L, Guglielmino CR, Haymer DS, Gasperi G, Gomulski LM, Malacrida AR (2001) Microsatellite analysis of medfly bioinfestations in California. Mol Ecol 10:2515–2524

    Article  PubMed  CAS  Google Scholar 

  • Bonizzoni M, Katsoyannos BI, Marguerie R, Guglielmino CR, Gasperi G, Malacrida A, Chapman T (2002) Microsatellite analysis reveals remating by wild Mediterranean fruit fly females, Ceratitis capitata. Mol Ecol 11:1915–1921

    Article  PubMed  CAS  Google Scholar 

  • Bonizzoni M, Guglielmino CR, Smallridge CJ, Gomulski M, Malacrida AR, Gasperi G (2004) On the origins of medfly invasion and expansion in Australia. Mol Ecol 13:3845–3855

    Article  PubMed  CAS  Google Scholar 

  • Bruford MW, Wayne RK (1993) Microsatellites and their application to population genetic studies. Cur Opin Gen Dev 3:939–943

    Article  CAS  Google Scholar 

  • Chirhart SE, Honeycutt RL, Greenbaum IF (2005) Microsatellite variation and evolution in the Peromyscus maniculatus species group. Mol Phyl Evol 34:408–415

    Article  CAS  Google Scholar 

  • Cuadrado A, Schwarzacher T (1998) The chromosomal organization of simple sequence repeats in wheat and rye genomes. Chromosoma 107:587–594

    Article  PubMed  CAS  Google Scholar 

  • Estoup A, Solignac M, Harry M, Cornuet J (1993) Characterization of (GT)(n) and (CT)(n) microsatellites in two insect species: Apis mellifera and Bombus terrestris. Nucl Acid Res 21:1427–1431

    Article  CAS  Google Scholar 

  • Fletcher BS (1989) Life history strategies of tephritid fruit flies. In: Robinson AS, Hooper G (eds) Fruit flies, their biology, natural enemies and control, vol 3B. Elsevier Science Publishers, Amsterdam, pp 195–208

    Google Scholar 

  • Forbes SH, Hogg JT, Buchanan FC, Crawford AM, Allendorf FW (1995) Microsatellite evolution in congeneric mammals: domestic and bighorn sheep. Mol Biol Evol 12:1106–1113

    PubMed  CAS  Google Scholar 

  • Franz G (2005) Genetic sexing strains in Mediterranean fruit fly, an example for other species amenable to large-scale rearing for the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide integrated management. Springer, Netherlands, pp 427–452

    Google Scholar 

  • Gariou-Papalexiou A, Gourzi P, Delprat A, Kritikou D, Rapti K, Chrysanthakopoulou B, Mintzas A, Zacharopoulou A (2002) Polytene chromosomes as tools in the genetic analysis of the Mediterranean fruit fly, Ceratitis capitata. Genetica 116:59–71

    Article  PubMed  CAS  Google Scholar 

  • Gasperi G, Bonizzoni M, Gomulski LM, Murelli V, Torti C, Malacrida AR, Guglielmino CR (2002) Genetic differentiation, gene flow and the origin of infestations of the medfly, Ceratitis capitata. Genetica 116:125–135

    Article  PubMed  CAS  Google Scholar 

  • Goldstein DB, Pollock DD (1997) Launching microsatellites: a review of mutation processes and methods of phylogenetic inference. J. Heredity 88:335–342

    CAS  Google Scholar 

  • Gomulski LM, Torti C, Malacrida AR, Gasperi G (1997) Ccmar1, a full-length mariner element from the Mediterranean fruit fly, Ceratitis capitata. Insect Mol Biol 6:241–253

    Article  PubMed  CAS  Google Scholar 

  • Gomulski LM, Torti C, Murelli V, Bonizzoni M, Gasperi G, Malacrida AR (2004) Medfly transposable elements: diversity, evolution, genomic impact and possible applications. Insect Bioch Mol Biol 34:139–148

    Article  CAS  Google Scholar 

  • Gomulski LM, Dimopoulos G, Xi Z, Soares MB, Bonaldo MF, Malacrida AR, Gasperi G (2008) Gene discovery in an invasive tephritid model pest species, the Mediterranean fruit fly, Ceratitis capitata. BMC Genomics 9:243

    Article  PubMed  Google Scholar 

  • Han HY, Ro KE, McPheron BA (2006) Molecular phylogeny of the Subfamily Tephritinae (Diptera: Tephritidae) Based on Mitochondrial 16S rDNA Sequences. Mol Cells 22:78–88

    PubMed  CAS  Google Scholar 

  • Hoelzel AR (1998) Molecular genetic analysis of populations: a practical approach, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Hutter CM, Schug MD, Aquadro CF (1998) Microsatellite variation in Drosophila melanogaster and Drosophila simulans: a reciprocal test of the ascertainment bias hypothesis. Mol Biol Evol 15:1620–1636

    PubMed  CAS  Google Scholar 

  • Jin L, Macaubas C, Hallmayer J, Kimura A, Mignot E (1996) Mutation rate varies among alleles at microsatellite locus: phylogenetic evidence. Proc Natl Acad Sci USA 75:15285–15288

    Article  Google Scholar 

  • Kinnear MW, Bariana HS, Sved JA, Frommer M (1998) Polymorphic microsatellite markers for population analysis of a Tephritidae pest species, Bactrocera tryoni. Mol Ecol 7:1489–1495

    Article  PubMed  CAS  Google Scholar 

  • Kraaijeveld K, Katsoyannos BI, Stavrinides M, Kouloussis NA, Chapman T (2005) Remating in wild females of the Mediterranean fruit fly, Ceratitis capitata. Anim Behav 69:771–776

    Article  Google Scholar 

  • Kumar S, Dudley J, Nei M, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:9–306

    Article  Google Scholar 

  • Li Y, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11:2453–2465

    Article  PubMed  CAS  Google Scholar 

  • Malacrida AR, Gomulski LM, Bonizzoni M, Bertin S, Gasperi G, Guglielmino CR (2007) Globalization and fruitfly invasion and expansion: the medfly paradigm. Genetica 131:1–9

    Article  PubMed  CAS  Google Scholar 

  • Meixner MD, Mcpheron BA, Silva JG, Gasparich GE, Sheppard WS (2002) The Mediterranean fruit fly in California: evidence for multiple introductions and persistent populations based on microsatellite and mitochondrial DNA variability. Mol Ecol 11:891–899

    Article  PubMed  CAS  Google Scholar 

  • Ramsay L, Macaulay M, Cardle L, Morgante M, Degli Ivanissevich S, Maestri E, Powell W, Waugh R (1999) Intimate association of microsatellite repeats with retrotransposons and other dispersed repetitive elements in barley. Plant Sci 17:415–425

    CAS  Google Scholar 

  • Ranson H, Paton MG, Jensen B, McCarroll L, Vaughan A, Hogan JR, Hemingway J, Collins FH (2004) Genetic mapping of genes conferring permethrin resistance in the malaria vector, Anopheles gambiae. Insect Mol Biol 13:379–386

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86(24):8–249

    Google Scholar 

  • Robinson AS (2002) Genetic sexing strains in medfly, Ceratitis capitata, sterile insect technique programmes. Genetica 116:5–13

    Article  PubMed  CAS  Google Scholar 

  • Robinson AS (2005) Genetic basis of the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile Insect Technique: principles and practice in area-wide integrated management. Springer, Netherlands, pp 95–114

    Google Scholar 

  • Rubinsztein DC, Amos W, Leggo J, Goodburn S, Jain S, Li S, Margolis RL, Ross CA, Ferguson-Smith MA (1995) Microsatellite evolution—evidence for directionality and variation in rate between species. Nat Genet 10:337–343

    Article  PubMed  CAS  Google Scholar 

  • Schetelig MF, Caceres C, Zacharopoulou A, Franz G, Wimmer EA (2009) Conditional embryonic lethality to improve the sterile insect technique in Ceratitis capitata (Diptera: Tephritidae). BMC Biol 7:4

    Article  PubMed  Google Scholar 

  • Schlötterer C (1998) Genome evolution: are microsatellites really simple sequences? Curr Biol 8:R132–R134

    Article  PubMed  Google Scholar 

  • Schlötterer C (2001) Genealogical inference of closely related species based on microsatellites. Gen Res 78:209–212

    Article  Google Scholar 

  • Schlötterer C, Harr B (2000) Drosophila virilis has long and highly polymorphic microsatellites. Mol Biol Evol 17:1641–1646

    PubMed  Google Scholar 

  • Schlötterer C, Pemberton J (1994) The use of microsatellites for genetic analysis of natural populations. EXS 69:203–214

    PubMed  Google Scholar 

  • Schug MD, Wetterstrand KA, Gaudette MS, Lim RH, Hutter CM, Aquadro CF (1998) The distribution and frequency of microsatellite loci in Drosophila melanogaster. Mol Ecol 7:57–70

    Article  PubMed  CAS  Google Scholar 

  • Segura MD, Callejas C, Fernández MP, Ochando MD (2006) New contributions towards the understanding of the phylogenetic relationships among economically important fruit flies (Diptera: Tephritidae). Bull Entomol Res 96:279–288

    Article  PubMed  CAS  Google Scholar 

  • Stratikopoulos EE, Augustinos AA, Gariou-Papalexiou A, Zacharopoulou A, Mathiopoulos KD (2002) Identification and partial characterization of a new Ceratitis capitata-specific 44-bp pericentromeric repeat. Chrom Res 10:287–295

    Article  PubMed  CAS  Google Scholar 

  • Stratikopoulos EE, Augustinos AA, Petalas YG, Vrahatis MN, Mintzas A, Mathiopoulos KD, 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

    Article  PubMed  CAS  Google Scholar 

  • Tautz D, Schlötterer C (1994) Simple sequences. Curr Opin Genet Dev 4:832–837

    Article  PubMed  CAS  Google Scholar 

  • Van Treuren R, Kuittinen H, Karkkainen K, Baena-Gonzalez E, Savolainen O (1997) Evolution of microsatellites in Arabis petraea and Arabis lyrata, outcrossing relatives of Arabidopsis thaliana. Mol Biol Evol 14:220–229

    PubMed  Google Scholar 

  • Verras M, Mavroidis M, Kokolakis G, Gourzi P, Zacharopoulou A, Mintzas AC (1999) Cloning and characterization of CcEcR. An ecdysone receptor homolog for the Mediterranean fruit fly Ceratitis capitata. Eur J Biochem 265:798–808

    Article  PubMed  CAS  Google Scholar 

  • Whitten MJ (1969) Automated sexing of pupae and its usefulness in control by sterile insects. J Econ Entomol 62:272–273

    Google Scholar 

  • Wierdl M, Dominska M, Petes TD (1997) Microsatellite instability in yeast: dependence on the length of the microsatellite. Genetics 146:769–779

    PubMed  CAS  Google Scholar 

  • Wilder J, Hollocher H (2001) Mobile elements and the genesis of microsatellites in Dipterans. Mol Biol Evol 18:384–392

    PubMed  CAS  Google Scholar 

  • Wondji CS, Morgan J, Coetzee M, Hunt RH, Steen K, Black WCIV, 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

    Article  PubMed  Google Scholar 

  • Yeh FC, Yang RC, Boyle TBJ, Ye ZH, Mao JX (1997) POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Center, University of Alberta, Canada

    Google Scholar 

  • Zacharopoulou A (1990) Polytene chromosome maps in the Medfly Ceratitis capitata. Genome 33:184–197

    Google Scholar 

  • Zacharopoulou A, Frisardi M, Savakis C, Robinson AS, Tolias P, Konsolaki M, Komitopoulou K, Kafatos FC (1992) The genome of the Mediterranean fruit fly C. capitata: localization of molecular markers by in situ hybridization to salivary gland polytene chromosomes. Chromosoma 101:448–455

    Article  PubMed  CAS  Google Scholar 

  • Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16

    Article  PubMed  CAS  Google Scholar 

  • Zheng L (1997) Microsatellite mapping of insect genomes. In: Crampton JM, Beard CB, Louis C (eds) Molecular biology of insect disease vectors: a methods manual. Chapman & Hall, London, pp. 321-329

  • Zheng L, Benedict MQ, Cornel AJ, Collins FH, Kafatos FC (1996) An integrated genetic map of the African human malaria vector mosquito, Anopheles gambiae. Genetics 143:941–952

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Hellenic General Secretariat of Research and Technology (97EL-17) and University of Patras, Greece. E. E. S. and A. A. A. were supported by a Fellowship from the National Fellowship Foundation (Greece) and K. D. M. by a grant from European Committee, contract No ERBFMBICT 983067. We would like to thank Dr. G. Franz for providing B. dorsalis, A. ludens samples, Dr. A Robinson for C. fasiventris and B. cucurbitae and the National Campaign Fruit Flies DGSV-SAGARPA, Tapachula, Chiapas, México for samples of A. fraterculus, A. obliqua, A, serpentina, A. striata and A. ludens. Dr. M. Frommer and Dr. N. Papadopoulos for providing B. tryoni and R. cerasi samples, respectively. We would also like to thank the two anonymous reviewers for their helpful comments.

Author information

Author notes

  1. E. E. Stratikopoulos & A. A. Augustinos

    Present address: Institute for Cancer Genetics, Columbia University, New York, NY, 10032, USA

Authors and Affiliations

  1. Department of Biology, University of Patras, 26500, Patras, Greece

    E. E. Stratikopoulos, A. A. Augustinos, I. D. Pavlopoulos, K. Ph. Economou, A. Mintzas, K. D. Mathiopoulos & Antigone Zacharopoulou

  2. Department of Biochemistry and Biotechnology, University of Thessaly, Larissa, Greece

    A. A. Augustinos & K. D. Mathiopoulos

Authors
  1. E. E. Stratikopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. A. Augustinos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. D. Pavlopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. Ph. Economou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Mintzas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. K. D. Mathiopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Antigone Zacharopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antigone Zacharopoulou.

Additional information

Communicated by G. Reuter.

E. E. Stratikopoulos and A. A. Augustinos contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stratikopoulos, E.E., Augustinos, A.A., Pavlopoulos, I.D. et al. 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 transferability. Mol Genet Genomics 282, 283–306 (2009). https://doi.org/10.1007/s00438-009-0465-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-009-0465-3

Keywords

Search

Navigation