Genetica

, Volume 139, Issue 1, pp 41–52

Safe and fit genetically modified insects for pest control: from lab to field applications

  • F. Scolari
  • P. Siciliano
  • P. Gabrieli
  • L. M. Gomulski
  • A. Bonomi
  • G. Gasperi
  • A. R. Malacrida
SI-Molecular Technologies to Improve SIT

Abstract

Insect transgenesis is continuously being improved to increase the efficacy of population suppression and replacement strategies directed to the control of insect species of economic and sanitary interest. An essential prerequisite for the success of both pest control applications is that the fitness of the transformant individuals is not impaired, so that, once released in the field, they can efficiently compete with or even out-compete their wild-type counterparts for matings in order to reduce the population size, or to spread desirable genes into the target population. Recent research has shown that the production of fit and competitive transformants can now be achieved and that transgenes may not necessarily confer a fitness cost. In this article we review the most recent published results of the fitness assessment of different transgenic insect lines and underline the necessity to fulfill key requirements of ecological safety. Fitness evaluation studies performed in field cages and medium/large-scale rearing will validate the present encouraging laboratory results, giving an indication of the performance of the transgenic insect genotype after release in pest control programmes.

Keywords

Fitness Transgenesis SIT Population replacement 

References

  1. Abraham EG, Donnelly-Doman M, Fujioka H, Ghosh A, Moreira L, Jacobs-Lorena M (2005) Driving midgut-specific expression and secretion of a foreign protein in transgenic mosquitoes with AgAper1 regulatory elements. Insect Mol Biol 14:271–279CrossRefPubMedGoogle Scholar
  2. Ahmed AM, Hurd H (2006) Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes Infect 8:308–315CrossRefPubMedGoogle Scholar
  3. Allen ML, Scholl PJ (2005) Quality of transgenic laboratory strains of Cochliomyia hominivorax (Diptera: Calliphoridae). J Econ Entomol 98:2301–2306CrossRefPubMedGoogle Scholar
  4. Allen ML, Handler AM, Berkebile DR, Skoda SR (2004a) PiggyBac transformation of the new world screwworm, Cochliomyia hominivorax, produces multiple distinct mutant strains. Med Vet Entomol 18:1–9CrossRefPubMedGoogle Scholar
  5. Allen ML, Berkebile DR, Skoda SR (2004b) Postlarval fitness of transgenic strains of Cochliomyia hominivorax (Diptera: Calliphoridae). J Econ Entomol 97:1181–1185CrossRefPubMedGoogle Scholar
  6. Alphey L (2007) Engineering insects for the sterile insect technique. In: Vreysen M, Robinson A, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Springer, Dordrecht, pp 51–60CrossRefGoogle Scholar
  7. Alphey L, Andreasen M (2002) Dominant lethality and insect population control. Mol Biochem Parasitol 121:173–178CrossRefPubMedGoogle Scholar
  8. Alphey L, Beard B, Billingsley P, Coetzee M, Crisanti A, Curtis CF, Eggleston P, Godfray C, Hemingway J, Jacobs-Lorena M, James A, Kafatos F, Mukwaya L, Paton M, Powell J, Schneider W, Scott T, Sine B, Sinden R, Sinkins S, Spielman A, Touré Y, Collins F (2002) Malaria control with genetically modified vectors. Science 298:119–121CrossRefPubMedGoogle Scholar
  9. Amenya DA, Bonizzoni M, Isaacs AT, Jasinskiene N, Chen H, Marinotti O, Yan G, James AA (2010) Comparative fitness assessment of Anopheles stephensi transgenic lines receptive to site-specific integration. Insect Mol Biol 19:263–269CrossRefPubMedGoogle Scholar
  10. Atkinson PW, Pinkerton AC, O’Brochta DA (2001) Genetic transformation systems in insects. Annu Rev Entomol 46:317–346CrossRefPubMedGoogle Scholar
  11. Bellini R, Calvitti M, Medici A, Carrieri M, Celli G, Maini S (2007) Use of the sterile insect technique against Aedes albopictus in Italy: first results of a pilot trial. In: Vreysen MB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests. Springer, Dordrecht, pp 505–515CrossRefGoogle Scholar
  12. Bellows TS, Paine TD, Gould JR, Bezark LG, Ball J (1992) Biological control of ash whitefly: a success in progress. Calif Agric 46:124–128Google Scholar
  13. Benedict MQ, Robinson AS (2003) The first releases of transgenic mosquitoes: an argument for the sterile insect technique. Trends Parasitol 19:349–355CrossRefPubMedGoogle Scholar
  14. Benedict MQ, Robinson AS (2008) Impact of technological improvements on traditional control strategies. In: Aksoy S (ed) Transgenesis and management of vector-borne diseases. Landes Bioscience, New York, pp 84–90CrossRefGoogle Scholar
  15. Bergmann A, Agapite J, McCall K, Steller H (1998) The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95:331–341CrossRefPubMedGoogle Scholar
  16. Bloem KA, Bloem S, Carpenter JE (2005) Impact of moth suppression/eradication programmes using the sterile insect technique or inherited sterility. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique. Principles and practice in area-wide integrated pest management. Springer, Dordrecht, pp 677–700Google Scholar
  17. Boëte C (2005) Malaria parasites in mosquitoes: laboratory models, evolutionary temptation and the real world. Trends Parasitol 21:445–447CrossRefPubMedGoogle Scholar
  18. Boete C, Koella JC (2002) A theoretical approach to predicting the success of genetic manipulation of malaria mosquitoes in malaria control. Malar J 1:3CrossRefPubMedGoogle Scholar
  19. Catteruccia F, Nolan T, Loukeris TG, Blass C, Savakis C, Kafatos FC, Crisanti A (2000) Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405:959–962CrossRefPubMedGoogle Scholar
  20. Catteruccia F, Godfray HCJ, Crisanti A (2003) Impact of genetic manipulation on the fitness of Anopheles stephensi mosquitoes. Science 299:1225–1227CrossRefPubMedGoogle Scholar
  21. Catteruccia F, Benton JP, Crisanti A (2005) An Anopheles transgenic sexing strain for vector control. Nat Biotechnol 23:1414–1417CrossRefPubMedGoogle Scholar
  22. Condon KC, Condon GC, Dafa’alla TH, Forrester OT, Phillips CE, Scaife S, Alphey L (2007a) Germ-line transformation of the Mexican fruit fly. Insect Mol Biol 16:573–580CrossRefPubMedGoogle Scholar
  23. Condon KC, Condon GC, Dafa’alla TH, Fu G, Phillips CE, Jin L, Gong P, Alphey L (2007b) Genetic sexing through the use of Y-linked transgenes. Insect Biochem Mol Biol 37:1168–1176CrossRefPubMedGoogle Scholar
  24. Davis S, Bax N, Grewe P (2001) Engineered underdominance allows efficient and economical introgression of traits into pest populations. J Theor Biol 212:83–98CrossRefPubMedGoogle Scholar
  25. Enkerlin WR (2005) Impact of fruit fly control programmes using the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique. Principles and practice in area-wide integrated pest management. Springer, Dordrecht, pp 651–676Google Scholar
  26. Franz AW, Sanchez-Vargas I, Adelman ZN, Blair CD, Beaty BJ, James AA, Olson KE (2006) Engineering RNA interference-based resistance to dengue virus type 2 in genetically modified Aedes aegypti. Proc Natl Acad Sci USA 103:4198–4203CrossRefPubMedGoogle Scholar
  27. Fu G, Condon KC, Epton MJ, Gong P, Jin L, Condon GC, Morrison NI, Dafa’alla TH, Alphey L (2007) Female-specific insect lethality engineered using alternative splicing. Nat Biotechnol 25:353–357CrossRefPubMedGoogle Scholar
  28. Fu G, Lees RS, Nimmo D, Aw D, Jin L, Gray P, Berendonk TU, White-Cooper H, Scaife S, Kim Phuc H, Marinotti O, Jasinskiene N, James AA, Alphey L (2010) Female-specific flightless phenotype for mosquito control. Proc Natl Acad Sci USA 107:4550–4554CrossRefPubMedGoogle Scholar
  29. Gong P, Epton MJ, Fu G, Scaife S, Hiscox A, Condon KC, Condon GC, Morrison NI, Kelly DW, Dafa’alla TH, Coleman PG, Alphey L (2005) A dominant lethal genetic system for autocidal control of the Mediterranean fruit fly. Nat Biotechnol 23:453–456CrossRefPubMedGoogle Scholar
  30. Grossman GL, Rafferty CS, Clayton JR, Stevens TK, Mukabayire O, Benedict MQ (2001) Germline transformation of the malaria vector Anopheles gambiae, with the piggyBac transposable element. Insect Mol Biol 10:597–604CrossRefPubMedGoogle Scholar
  31. Hahn MW, Nuzhdin SV (2004) The fixation of malaria refractoriness in mosquitoes. Curr Biol 14:264–265CrossRefGoogle Scholar
  32. Handler AM (2002) Prospects for using genetic transformation for improved SIT and new biocontrol methods. Genetica 116:137–149CrossRefPubMedGoogle Scholar
  33. Handler AM, Harrell RA II (2001) Transformation of the Caribbean fruit fly, Anastrepha suspensa, with a piggyBac vector marked with polyubiquitin-regulated GFP. Insect Biochem Mol Biol 31:199–205CrossRefPubMedGoogle Scholar
  34. Handler AM, McCombs SD (2000) The piggyBac transposon mediates germ-line transformation in the Oriental fruit fly and closely related elements exist in its genome. Insect Mol Biol 9:605–612CrossRefPubMedGoogle Scholar
  35. Handler AM, O’Brochta DA (2005) Transposable elements for insect transformation. In: Gilbert LI, Iatrou K, Gill S (eds) Comprehensive insect physiology, biochemistry, pharmacology, and molecular biology. Elsevier Ltd, Oxford, pp 437–474Google Scholar
  36. Handler AM, McCombs SD, Fraser MJ, Saul SH (1998) The lepidopteran transposon vector, piggyBac, mediates germ-line transformation in the Mediterranean fruit fly. Proc Natl Acad Sci USA 95:7520–7525CrossRefPubMedGoogle Scholar
  37. Handler AM, Allen ML, Skoda SR (2009) Development and utilization of transgenic new world screwworm, Cochliomyia hominivorax. Med Vet Entomol 23(1):98–105CrossRefPubMedGoogle Scholar
  38. Heinrich J, Scott M (2000) A repressible female-specific lethal genetic system for making transgenic insect strains suitable for a sterile-release program. Proc Natl Acad Sci USA 97:8229–8232CrossRefPubMedGoogle Scholar
  39. Hendrichs J (2000) Use of the sterile insect technique against key insect pests. Sustainable Dev Int 2:75–79Google Scholar
  40. Horn C, Wimmer EA (2003) A transgene-based, embryo-specific lethality system for insect pest management. Nat Biotechnol 21:64–70CrossRefPubMedGoogle Scholar
  41. Huang Y, Magor K, Lloyd AL, Gould F (2007) Introducing desirable transgenes into insect populations using Y-linked meiotic drive—a theoretical assessment. Evolution 61:717–726CrossRefPubMedGoogle Scholar
  42. Hurd H, Taylor PJ, Adams D, Underhill A, Eggleston P (2005) Evaluating the costs of mosquito resistance to malaria parasites. Evol Int J Org Evol 59:2560–2572Google Scholar
  43. Irvin N, Hoddle MS, O’Brochta DA, Carey B, Atkinson PW (2004) Assessing fitness costs for transgenic Aedes aegypti expressing the GFP marker and transposase genes. Proc Natl Acad Sci USA 101:891–896CrossRefPubMedGoogle Scholar
  44. Ito J, Ghosh A, Moreira LA, Wimmer EA, Jacobs-Lorena M (2002) Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417:452–455CrossRefPubMedGoogle Scholar
  45. James AA (2005) Gene drive systems in mosquitoes: rules of the road. Trends Parasitol 21:64–67CrossRefPubMedGoogle Scholar
  46. Jordan IK, Matyunina LV, McDonald JF (1999) Evidence for the recent horizontal transfer of long terminal repeat retrotransposon. Proc Natl Acad Sci USA 96:12621–12625CrossRefPubMedGoogle Scholar
  47. Kidwell MG (1992a) Horizontal transfer. Curr Opin Genet Dev 2:868–873CrossRefPubMedGoogle Scholar
  48. Kidwell MG (1992b) Horizontal transfer of P elements and other short inverted repeat transposons. Genetica 86:275–286CrossRefPubMedGoogle Scholar
  49. Kim W, Koo H, Richman AM, Seeley D, Vizioli J, Klocko AD, O’Brochta DA (2004) Ectopic expression of a cecropin transgene in the human malaria vector mosquito Anopheles gambiae (Diptera: Culicidae): effects on susceptibility to Plasmodium. J Med Entomol 41:447–455CrossRefPubMedGoogle Scholar
  50. Klassen W, Curtis CF (2005) History of the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique. Principles and practice in area-wide integrated pest management. Springer, Dordrecht, pp 3–36Google Scholar
  51. Knipling E (1955) Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol 48:459–462Google Scholar
  52. Knols BG, Njiru BN, Mathenge EM, Mukabana WR, Beier JC, Killeen GF (2002) MalariaSphere: a greenhouse-enclosed simulation of a natural Anopheles gambiae (Diptera: Culicidae) ecosystem in western Kenya. Malar J 1:19CrossRefPubMedGoogle Scholar
  53. Koukidou M, Klinakis A, Reboulakis C, Zagoraiou L, Tavernarakis N, Livadaras I, Economopoulos A, Savakis C (2006) Germ line transformation of the olive fly Bactrocera oleae using a versatile transgenesis marker. Insect Mol Biol 15:95–103CrossRefPubMedGoogle Scholar
  54. Lambrechts L, Koella JC, Boëte C (2007) Can transgenic mosquitoes afford the fitness cost? Trends Parasitol 24:4–7CrossRefPubMedGoogle Scholar
  55. Landahl JT, Root RB (1969) Differences in the life tables of tropical and temperate milkweed bugs, genus oncopeltus (Hemiptera:Lygaeidae). Ecology 50:734–737CrossRefGoogle Scholar
  56. Li C, Marrelli MT, Yan G, Jacobs-Lorena M (2008) Fitness of transgenic Anopheles stephensi mosquitoes expressing the SM1 peptide under the control of a vitellogenin promoter. J Hered 99:275–282CrossRefPubMedGoogle Scholar
  57. Liu HS, Jan MS, Chou CK, Chen PH, Ke NJ (1999) Is green fluorescent protein toxic to the living cells? Biochem Biophys Res Commun 260:712–717CrossRefPubMedGoogle Scholar
  58. Loukeris TG, Livadaras I, Arcà B, Zabalou S, Savakis C (1995) Gene transfer into the medfly, Ceratitis capitata, with a Drosophila hydei transposable element. Science 270:2002–2005CrossRefPubMedGoogle Scholar
  59. Mackay TF (1989) Transposable elements and fitness in Drosophila melanogaster. Genome 31:284–295PubMedGoogle Scholar
  60. Markstein M, Pitsouli C, Villalta C, Celniker SE, Perrimon N (2008) Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat Genet 40:476–483CrossRefPubMedGoogle Scholar
  61. Marrelli MT, Moreira CK, Kelley D, Alphey L, Jacobs-Lorena M (2006) Mosquito transgenesis: what is the fitness cost? Trends Parasitol 22:197–202CrossRefPubMedGoogle Scholar
  62. Marrelli MT, Li C, Rasgon JL, Jacobs-Lorena M (2007) Transgenic malaria-resistant mosquitoes have a fitness advantage when feeding on Plasmodium-infected blood. Proc Natl Acad Sci USA 104:5580–5583CrossRefPubMedGoogle Scholar
  63. Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23:23–35CrossRefGoogle Scholar
  64. Michel K, Stamenova A, Pinkerton AC, Franz G, Robinson AS, Gariou-Papalexiou A, Zacharopoulou A, O’Brochta DA, Atkinson PW (2001) Hermes-mediated germ-line transformation of the Mediterranean fruit fly Ceratitis capitata. Insect Mol Biol 10:155–162CrossRefPubMedGoogle Scholar
  65. Moreira LA, Ito J, Ghosh A, Devenport M, Zieler H, Abraham EG, Crisanti A, Nolan T, Catteruccia F, Jacobs-Lorena M (2002) Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes. J Biol Chem 277:40839–40843CrossRefPubMedGoogle Scholar
  66. Moreira LA, Wang J, Collins FH, Jacobs-Lorena M (2004) Fitness of Anopheline mosquitoes expressing transgenes that inhibit Plasmodium development. Genetics 166:1337–1341CrossRefPubMedGoogle Scholar
  67. Mori A, Chadee DD, Graham DH, Severson DW (2004) Reinvestigation of an endogenous meiotic drive system in the mosquito, Aedes aegypti (Diptera: Culicidae). J Med Entomol 41:1027–1033CrossRefPubMedGoogle Scholar
  68. Nimmo DD, Alphey L, Meredith JM, Eggleston P (2006) High efficiency site-specific genetic engineering of the mosquito genome. Insect Mol Biol 15:129–136CrossRefPubMedGoogle Scholar
  69. O’Brochta DA, Sethuraman N, Wilson R, Hice RH, Pinkerton AC, Levesque CS, Bideshi DK, Jasinskiene N, Coates CJ, James AA, Lehane MJ, Atkinson PW (2003) Gene vector and transposable element behavior in mosquitoes. J Exp Biol 206:3823–3834CrossRefPubMedGoogle Scholar
  70. Perera OP, Harrell IR, Handler AM (2002) Germ-line transformation of the South American malaria vector, Anopheles albimanus, with a piggyBac/EGFP transposon vector is routine and highly efficient. Insect Mol Biol 11:291–297CrossRefPubMedGoogle Scholar
  71. Phuc HK, Andreasen MH, Burton RS, Vass C, Epton MJ, Pape G, Fu G, Condon KC, Scaife S, Donnelly CA, Coleman PG, White-Cooper H, Alphey L (2007) Late-acting dominant lethal genetic systems and mosquito control. BMC Biol 5:11CrossRefPubMedGoogle Scholar
  72. Rasgon JL, Gould F (2005) Transposable element insertion location bias and the dynamics of gene drive in mosquito populations. Insect Mol Biol 14:493–500CrossRefPubMedGoogle Scholar
  73. Rasgon JL, Scott TW (2003) Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: parameter estimates and infection dynamics in natural populations. Genetics 165:2029–2038PubMedGoogle Scholar
  74. Robertson HM, Lampe DJ (1995) Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Mol Biol Evol 12:850–862PubMedGoogle Scholar
  75. Robinson AS, Vreysen MJB, Hendrichs J, Feldmann U (2009) Enabling technologies to improve area-wide integrated pest management programmes for the control of screwworms. Med Vet Entomol 23(Suppl 1):1–7CrossRefPubMedGoogle Scholar
  76. Rodrigues FG, Santos MN, de Carvalho TX, Rocha BC, Riehle MA, Pimenta PF, Abraham EG, Jacobs-Lorena M, Alves de Brito CF, Moreira LA (2008) Expression of a mutated phospholipase A2 in transgenic Aedes fluviatilis mosquitoes impacts Plasmodium gallinaceum development. Insect Mol Biol 17:175–183CrossRefPubMedGoogle Scholar
  77. Santos MN, Nogueira PM, Dias FBS, Valle D, Moreira LA (2010) Fitness aspects of transgenic Aedes fluviatilis mosquitoes expressing a Plasmodium-blocking molecule. Transgenic Res. doi:10.1007/s11248-010-9375-8
  78. Schetelig MF, Caceres C, Zacharopoulou A, Franz G, Wimmer EA (2009a) Conditional embryonic lethality to improve the sterile insect technique in Ceratitis capitata (Diptera:Tephritidae). BMC Biol 7:4CrossRefPubMedGoogle Scholar
  79. Schetelig MF, Scolari F, Handler AM, Kittelmann S, Gasperi G, Wimmer EA (2009b) Site-specific recombination for the modification of transgenic strains of the Mediterranean fruit fly Ceratitis capitata. Proc Natl Acad Sci USA 106:18171–18176CrossRefPubMedGoogle Scholar
  80. Schliekelman P, Gould F (2000) Pest control by the release of insects carrying a female-killing allele on multiple loci. J Econ Entomol 93:1566–1579CrossRefPubMedGoogle Scholar
  81. Scolari F, Schetelig MF, Gabrieli P, Siciliano P, Gomulski LM, Karam N, Wimmer EA, Malacrida AR, Gasperi G (2008a) Insect transgenesis applied to tephritid pest control. J Appl Entomol 132:820–831CrossRefGoogle Scholar
  82. Scolari F, Schetelig MF, Bertin B, Malacrida AR, Gasperi G, Wimmer EA (2008b) Fluorescent sperm marking to improve the fight against the pest insect Ceratitis capitata (Wiedemann; Diptera: Tephritidae). N Biotechnol 25:76–84CrossRefPubMedGoogle Scholar
  83. Scott TW, Takken W, Knols BGJ, Boëte C (2002) The ecology of genetically modified mosquitoes. Science 298:117–119CrossRefPubMedGoogle Scholar
  84. Scott TW, Rasgon JL, Black WC IV, Gould F (2005) Fitness studies: developing a consensus methodology. In: Knols BGJ, Louis C (eds) Strategic plan to bridge laboratory and field research in disease vector control. Frontis, Dordrecht, pp 171–181Google Scholar
  85. Simmons GM (1992) Horizontal transfer of hobo transposable elements within the Drosophila melanogaster species complex: evidence from DNA sequencing. Mol Biol Evol 9:1050–1060PubMedGoogle Scholar
  86. Sinkins SP, Godfray HC (2004) Use of Wolbachia to drive nuclear transgenes through insect populations. Proc Biol Sci 271:1421–1426CrossRefPubMedGoogle Scholar
  87. Sinkins SP, Gould F (2006) Gene drive systems for insect disease vectors. Nat Rev Genet 7:427–435CrossRefPubMedGoogle Scholar
  88. Sundararajan P, Atkinson PW, O’Brochta DA (1999) Transposable element interactions in insects: crossmobilization of hobo and Hermes. Insect Mol Biol 8:359–368CrossRefPubMedGoogle Scholar
  89. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, Buchholz R, Demsky M, Fawcett R, Francis-Lang HL, Ryner L, Cheung LM, Chong A, Erickson C, Fisher WW, Greer K, Hartouni SR, Howie E, Jakkula L, Joo D, Killpack K, Laufer A, Mazzotta J, Smith RD, Stevens LM, Stuber C, Tan LR, Ventura R, Woo A, Zakrajsek I, Zhao L, Chen F, Swimmer C, Kopczynski C, Duyk G, Winberg ML, Margolis J (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36:283–287CrossRefPubMedGoogle Scholar
  90. Thomas DD, Donnelly CA, Wood RJ, Alphey LS (2000) Insect population control using a dominant, repressible, lethal genetic system. Science 287:2474–2476CrossRefPubMedGoogle Scholar
  91. Venken KJT, Bellen HJ (2005) Emerging technologies for gene manipulation in Drosophila melanogaster. Nat Rev Genet 6:167–178CrossRefPubMedGoogle Scholar
  92. Vreysen JB (2006) Prospects for area-wide integrated control of tsetse flies (Diptera:Glossinidae) and trypanosomosis in sub-Saharan Africa. Rev Soc Entomol Argent 65:1–21Google Scholar
  93. Wilke ABB, Nimmo DD, St John O, Burini Kojin B, Capurro ML, Marrelli MT (2009) Mini-review: genetic enhancements to the sterile insect technique to control mosquito populations. AsPac J Mol Biol Biotechnol 17:65–74Google Scholar
  94. Williams A, Harker N, Ktistaki E, Veiga-Fernandes H, Roderick K, Tolaini M, Norton T, Williams K, Kioussis D (2008) Position effect variegation and imprinting of transgenes in lymphocytes. Nucleic Acids Res 36:2320–2329CrossRefPubMedGoogle Scholar
  95. Windbichler N, Papathanos PA, Catteruccia F, Ranson H, Burt A, Crisanti A (2007) Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucleic Acids Res 35:5922–5933CrossRefPubMedGoogle Scholar
  96. Wyss JH (2000) Screwworm eradication in the Americas. Ann NY Acad Sci 916:186–193CrossRefPubMedGoogle Scholar
  97. Yakob L, Kiss IZ, Bonsall MB (2008) A network approach to modeling population aggregation and genetic control of pest insects. Theor Popul Biol 74:324–331CrossRefPubMedGoogle Scholar
  98. Zwiebel LJ, Saccone G, Zacharopoulou A, Besansky NJ, Favia G, Collins FH, Louis C, Kafatos FC (1995) The white gene of Ceratitis capitata: a phenotypic marker for germline transformation. Science 270:2005–2008CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • F. Scolari
    • 1
  • P. Siciliano
    • 1
  • P. Gabrieli
    • 1
  • L. M. Gomulski
    • 1
  • A. Bonomi
    • 1
  • G. Gasperi
    • 1
  • A. R. Malacrida
    • 1
  1. 1.Department of Animal BiologyUniversity of PaviaPaviaItaly

Personalised recommendations