Modifying Insect Population Age Structure to Control Vector-Borne Disease

  • Peter E. Cook
  • Conor J. McMeniman
  • Scott L. O’Neill
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 627)


Age is a critical determinant of the ability of most arthropod vectors to transmit a range of human pathogens. This is due to the fact that most pathogens require a period of extrinsic incubation in the arthropod host before pathogen transmission can occur. This developmental period for the pathogen often comprises a significant proportion of the expected lifespan of the vector. As such, only a small proportion of the population that is oldest contributes to pathogen transmission. Given this, strategies that target vector age would be expected to obtain the most significant reductions in the capacity of a vector population to transmit disease. The recent identification of biological agents that shorten vector lifespan, such as Wolbachia, entomopathogenic fungi and densoviruses, offer new tools for the control of vector-borne diseases. Evaluation of the efficacy of these strategies under field conditions will be possible due to recent advances in insect age-grading techniques. Implementation of all of these strategies will require extensive field evaluation and consideration of the selective pressures that reductions in vector longevity may induce on both vector and pathogen.


Entomopathogenic Fungus Cuticular Hydrocarbon Pathogen Transmission Cytoplasmic Incompatibility Wolbachia Infection 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Macdonald G. The epidemiology and control of malaria. London: Oxford University Press, 1957.Google Scholar
  2. 2.
    Garrett-Jones C. Prognosis for interruption of malaria transmission through assessment of the mosquito’s vectorial capacity. Nature 1964; 204:1173–5.PubMedCrossRefGoogle Scholar
  3. 3.
    Garrett-Jones C. The human blood index of malaria vectors in relation to epidemiological assessment. Bull World Health Organ 1964; 30:241–61.PubMedGoogle Scholar
  4. 4.
    Gratz NG. Emerging and resurging vector-borne diseases. Annu Rev Entomol 1999; 44:51–75.PubMedCrossRefGoogle Scholar
  5. 5.
    Brownstein JS, Hett E, O’Neill SL. The potential of virulent Wolbachia to modulate disease transmission by insects. J Invertebr Pathol 2003; 84(l):24–9.PubMedCrossRefGoogle Scholar
  6. 6.
    Sinkins SP, O’Neill SL. Wolbachia as a vehicle to modify insect populations. In: Handler AM, James AA, eds. Insect Transgenesis: Methods and Applications. London: CRC Press, 2000:271–87.Google Scholar
  7. 7.
    Blanford S, Chan BH, Jenkins N et al. Fungal pathogen reduces potential for malaria transmission. Science 2005; 308(5728):l638–4l.CrossRefGoogle Scholar
  8. 8.
    Carlson J, Suchman E, Buchatsky L. Densoviruses for control and genetic manipulation of mosquitoes. Adv Virus Res 2006; 68:361–92.PubMedCrossRefGoogle Scholar
  9. 9.
    Siler JF, Hall MW, Hitchens AP. Dengue: Its history, epidemiology, mechanism of transmission, etiology, clinical manifestations, immunity and prevention. Philipp J Sci 1926; 29(l–2):l–304.Google Scholar
  10. 10.
    Gilles HM, Warrell DA. Essential malariology. 4th ed. London: Arnold, 2002.Google Scholar
  11. 11.
    Dye C. The analysis of parasite transmission by bloodsucking insects. Annu Rev Entomol 1992; 37:1–19.PubMedCrossRefGoogle Scholar
  12. 12.
    Garrett-Jones C, Grab B. Assessment of insecticidal impact on malaria mosquito’s vectorial capacity from data on proportion of parous females. Bull World Health Organ 1964; 31(l):71–86.PubMedGoogle Scholar
  13. 13.
    Black IVth WC, Moore CG. Population biology as a tool for studying vector-borne diseases. In: Marquardt WC, ed. Biology of Disease Vectors. 2nd ed. Boston: Elsevier Academic Press, 2005:187–206.Google Scholar
  14. 14.
    Edman JD, Strickman D, Kittayapong P et al. Female Aedes aegypti (Diptera: Culicidae) in Thailand rarely feed on sugar. J Med Entomol 1992; 29(6): 1035–8.PubMedGoogle Scholar
  15. 15.
    Scott TW, Chow E, Strickman D et al. Blood-feeding patterns of Aedes aegypti (Diptera: Culicidae) collected in a rural Thai village. J Med Entomol 1993; 30(5):922–7.PubMedGoogle Scholar
  16. 16.
    Scott TW, Naksathit A, Day JF et al. A fitness advantage for Aedes aegypti and the viruses it transmits when females feed only on human blood. Am J Trop Med Hyg 1997; 57(2):235–9.PubMedGoogle Scholar
  17. 17.
    Olson KE, Adelman ZN, Travanty EA et al. Developing arbovirus resistance in mosquitoes. Insect Biochem Mol Biol 2002; 32(10): 1333–43.PubMedCrossRefGoogle Scholar
  18. 18.
    Alphey L, Beard CB, Billingsley P et al. Malaria control with genetically manipulated insect vectors. Science 2002; 298(5591):119–21.PubMedCrossRefGoogle Scholar
  19. 19.
    Kokoza V, Ahmed A, Cho WL et al. Engineering blood meal-activated systemic immunity in the yellow fever mosquito, Aedes aegypti. Proc Natl Acad Sci USA 2000; 97(16):9144–9.PubMedCrossRefGoogle Scholar
  20. 20.
    Aultman KS, Beaty BJ, Walker ED. Genetically manipulated vectors of human disease: A practical overview. Trends Parasitol 2001; 17(11):507–9.PubMedCrossRefGoogle Scholar
  21. 21.
    Land KM. Transgenic mosquitoes in controlling malaria transmission. Trends Parasitol 2002; 18(9):383.PubMedCrossRefGoogle Scholar
  22. 22.
    Jacobs-Lorena M. Interrupting malaria transmission by genetic manipulation of anopheline mosquitoes. J Vector Borne Dis 2003; 40(3–4):73–7.PubMedGoogle Scholar
  23. 23.
    Travanty EA, Adelman ZN, Franz AW et al. Using RNA interference to develop dengue virus resistance in genetically modified Aedes aegypti. Insect Biochem Mol Biol 2004; 34(7):607–13.PubMedCrossRefGoogle Scholar
  24. 24.
    Boete C, Koella JC. A theoretical approach to predicting the success of genetic manipulation of malaria mosquitoes in malaria control. Malar J 2002; 1(1):3.PubMedCrossRefGoogle Scholar
  25. 25.
    Hertig M, Wolbach SB. Studies on rickettsia-like micro-organisms in insects. J Med Res 1924; 44:329–74.PubMedGoogle Scholar
  26. 26.
    Hertig M. The rickettsia, Wolbachia pipientis (gen. et sp. n.) and associated inclusions in the mosquito, Culex pipiens. Parasitology 1936; 28(4):453–86.Google Scholar
  27. 27.
    Werren JH, Windsor D, Guo LR. Distribution of Wolbachia among neotropical arthropods. Proc R Soc Lond B Biol Sci 1995; 262:197–204.CrossRefGoogle Scholar
  28. 28.
    Jeyaprakash A, Hoy MA. Long PCR improves Wolbachia DNA amplification: Wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 2000; 9(4):393–405.PubMedCrossRefGoogle Scholar
  29. 29.
    Heath BD, Butcher RD, Whitfield WG et al. Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 1999; 9(6):313–6.PubMedCrossRefGoogle Scholar
  30. 30.
    Stouthamer R, Breeuwer JAJ, Luck RF et al. Molecular identification of microorganisms associated with parthenogenesis. Nature 1993; 361:66–8.PubMedCrossRefGoogle Scholar
  31. 31.
    Rousset F, Bouchon D, Pintureau B et al. Wolbachia endosymbionts responsible for various alterations of sexuality of arthropods. Proc R Soc Lond B Biol Sci 1992; 250:91–8.CrossRefGoogle Scholar
  32. 32.
    Hurst GD, Jiggins FM, Graf von der Schulenberg JH et al. Male killing Wolbachia in two species of insects. Proc R Soc Lond B Biol Sci 1999; 266:735–40.CrossRefGoogle Scholar
  33. 33.
    O’Neill SL, Giordano R, Colbert AM et al. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 1992; 89(7):2699–702.PubMedCrossRefGoogle Scholar
  34. 34.
    Hoffmann AA, Turelli M. Cytoplasmic incompatibility in insects. In: O’Neill SL, Hoffmann AA, Werren JH, eds. Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford: Oxford University Press, 1997:42–80.Google Scholar
  35. 35.
    Turelli M, Hoffmann AA. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 1991; 353(6343):440–2.PubMedCrossRefGoogle Scholar
  36. 36.
    Turelli M, Hoffmann AA. Cytoplasmic incompatibility in Drosophila simulans: Dynamics and parameter estimates from natural populations. Genetics 1995; 140(4): 1319–38.PubMedGoogle Scholar
  37. 37.
    Dobson SL, Marsland EJ, Rattanadechakul W. Mutualistic Wolbachia infection in Aedes albopictus: Accelerating cytoplasmic drive. Genetics 2002; 160(3): 1087–94.PubMedGoogle Scholar
  38. 38.
    Dobson SL, Rattanadechakul W, Marsland EJ. Fitness advantage and cytoplasmic incompatibility in Wolbachia single-and superinfected Aedes albopictus. Heredity 2004; 93(2): 135–42.PubMedCrossRefGoogle Scholar
  39. 39.
    Hoffmann AA, Clancy D, Duncan J. Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity 1996; 76:1–8.PubMedCrossRefGoogle Scholar
  40. 40.
    Fleury F, Vavre F, Ris N et al. Physiological cost induced by the maternally-transmitted endosymbiont Wolbachia in the Drosophila parasitoid Leptopilina heterotoma. Parasitology 2000; 121(5):493–500.PubMedCrossRefGoogle Scholar
  41. 41.
    Min KT, Benzer S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad sci USA 1997; 94(20): 10792–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Hannah AM. Radiation-mutations involving the cut-locus in Drosophila. Proc 8th Intl Congr Genet 1948 Hereditas (Lund) 1949; 588–9.Google Scholar
  43. 43.
    McGraw EA, Merritt DJ, Droller JN et al. Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad sci USA 2002; 99(5):2918–23.PubMedCrossRefGoogle Scholar
  44. 44.
    Reynolds KT, Thomson LJ, Hoffmann AA. The effects of host age, host nuclear background and temperature on phenotypic effects of the virulent Wolbachia strain popcorn in Drosophila melanogaster. Genetics 2003; 164(3):1027–34.PubMedGoogle Scholar
  45. 45.
    McGraw EA, Merritt DJ, Droller JN et al. Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila. Proc R Soc Lond B Biol Sci 2001; 268(l485):2565–70.CrossRefGoogle Scholar
  46. 46.
    Rasgon JL, Styer LM, Scott TW. Wolbachia-induced mortality as a mechanism to modulate pathogen transmission by vector arthropods. J Med Entomol 2003; 40(2): 125–32.PubMedGoogle Scholar
  47. 47.
    Ono M, Braig HR, Munstermann LE et al. Wolbachia infections of Phlebotomine sand flies (Diptera: Psychodidae). J Med Entomol 2001; 38(2):237–4l.PubMedGoogle Scholar
  48. 48.
    Cheng Q, Ruel TD, Zhou W et al. Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp. Med Vet Entomol 2000; 14:44–50.PubMedCrossRefGoogle Scholar
  49. 49.
    Ruang-Areerate T, Kittayapong P, Baimai V et al. Molecular phylogeny of Wolbachia endosymbionts in Southeast Asian mosquitoes (Diptera: Culicidae) based on wsp gene sequences. J Med Entomol 2003; 40(1): 1–5.PubMedGoogle Scholar
  50. 50.
    Sinkins SP. Wolbachia and cytoplasmic incompatibility in mosquitoes. Insect Biochem Mol Biol 2004; 34(7):723–9.PubMedCrossRefGoogle Scholar
  51. 51.
    Kittayapong P, Baimai V, O’Neill SL. Field prevalence of Wolbachia in the mosquito vector Aedes albopictus. Am J Trop Med Hyg 2002; 66(l):108–11.Google Scholar
  52. 52.
    Dean JL, Dobson SL. Characterization of Wolbachia infections and interspecific crosses of Aedes (Stegomyia) polynesiensis and Ae. (Stegomyia) riversi (Diptera: Culicidae). J Med Entomol 2004; 4l(5):894–900.Google Scholar
  53. 53.
    Behbahani A, Dutton TJ, Davies N et al. Population differentiation and Wolbachia phylogeny in mosquitoes of the Aedes scutellaris group. Med Vet Entomol 2005; 19(1):66–71.PubMedCrossRefGoogle Scholar
  54. 54.
    Dobson SL, Marsland EJ, Rattanadechakul W. Wolbachia-induced cytoplasmic incompatibility in single-and superinfected Aedes albopictus (Diptera: Culicidae). J Med Entomol 2001; 38(3):382–7.PubMedGoogle Scholar
  55. 55.
    Sinkins SP, Braig HR, O’Neill SL. Wolbachia pipientis: Bacterial density and unidirectional cytoplasmic incompatibility between infected populations of Aedes albopictus. Exp Parasitol 1995; 81(3):284–91.PubMedCrossRefGoogle Scholar
  56. 56.
    Sinkins SP, Braig HR, O’Neill SL. Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proc R Soc Lond B Biol Sci 1995; 261(1362):325–30.CrossRefGoogle Scholar
  57. 57.
    Kittayapong P, Baisley KJ, Sharpe RG et al. Maternal transmission efficiency of Wolbachia superinfections in Aedes albopictus populations in Thailand. Am J Trop Med Hyg 2002; 66(1): 103–7.PubMedGoogle Scholar
  58. 58.
    Kittayapong P, Mongkalangoon P, Baimai V et al. Host age effect and expression of cytoplasmic incompatibility in field populations of Wolbachia-superinfected Aedes albopictus. Heredity 2002; 88(4):270–4.PubMedCrossRefGoogle Scholar
  59. 59.
    Kittayapong P, Baisley KJ, Baimai V et al. Distribution and diversity of Wolbachia infections in Southeast Asian mosquitoes (Diptera: Culicidae). J Med Entomol 2000; 37(3):340–5.PubMedCrossRefGoogle Scholar
  60. 60.
    Rasgon JL, Scott TW. An initial survey for Wolbachia (Rickettsiales: Rickettsiaceae) infections in selected California mosquitoes (Diptera: Culicidae). J Med Entomol 2004; 4l(2):255–7.Google Scholar
  61. 61.
    Ricci I, Cancrini G, Gabrielli S et al. Searching for Wolbachia (Rickettsiales: Rickettsiaceae) in mosquitoes (Diptera: Culicidae): Large polymerase chain reaction survey and new identifications. J Med Entomol 2002; 39(4):562–7.PubMedGoogle Scholar
  62. 62.
    Boyle L, O’Neill SL, Robertson HM et al. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 1993; 260(5115):1796–9.PubMedCrossRefGoogle Scholar
  63. 63.
    Chang NW, Wade MJ. The transfer of Wolbachia pipientis and reproductive incompatibility between infected and uninfected strains of the flour beetle, Tribolium confusum, by microinjection. Can J Microbiol 1994; 40:978–81.CrossRefGoogle Scholar
  64. 64.
    Clancy DJ, Hoffmann AA. Behavior of Wolbachia endosymbionts from Drosophila simulans in Drosophila serrata, a novel host. Am Nat 1997; l49(5):975–88.CrossRefGoogle Scholar
  65. 65.
    Grenier S, Pintureau B, Heddi A et al. Successful horizontal transfer of Wolbachia symbionts between Trichogramma wasps. Proc R Soc Lond B 1998; 265:1441–5.CrossRefGoogle Scholar
  66. 66.
    Sasaki T, Kubo T, Ishikawa H. Interspecific transfer of Wolbachia between two lepidopteran insects expressing cytoplasmic incompatibility: A Wolbachia variant naturally infecting Cadra cautella causes male killing in Ephestia kuehniella. Genetics 2002; 162(3): 1313–9.PubMedGoogle Scholar
  67. 67.
    Xi Z, Khoo CCH, Dobson SL. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 2005; 310:326–8.PubMedCrossRefGoogle Scholar
  68. 68.
    Rigaud T, Juchault P. Success and failure of horizontal transfers of feminizing Wolbachia endosymbionts in woodlice. J Evol Biol 1995; 8:249–55.CrossRefGoogle Scholar
  69. 69.
    Rigaud T, Pennings PS, Juchault P. Wolbachia bacteria effects after experimental interspecific transfers in terrestrial isopods. J Invertebr Pathol 2001; 77(4):251–7.PubMedCrossRefGoogle Scholar
  70. 70.
    Braig HR, Guzman H, Tesh RB et al. Replacement of the natural Wolbachia symbiont of Drosophila simulans with a mosquito counterpart. Nature 1994; 367(6462):453–5.PubMedCrossRefGoogle Scholar
  71. 71.
    Van Meer MM, Stouthamer R. Cross-order transfer of Wolbachia from Muscidifurax uniraptor (Hymenoptera: Pteromalidae) to Drosophila simulans (Diptera: Drosophilidae). Heredity 1999; 82(2): 163–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Xi Z, Dean JL, Khoo C et al. Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection. Insect Biochem Mol Biol 2005; 35(8):903–10.PubMedCrossRefGoogle Scholar
  73. 73.
    Zabalou S, Riegler M, Theodorakopoulou M et al. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc Natl Acad Sci USA 2004; 101(42): 15042–5.PubMedCrossRefGoogle Scholar
  74. 74.
    Xi Z, Dobson SL. Characterization of Wolbachia transfection efficiency by using microinjection of embryonic cytoplasm and embryo homogenate. Appl Environ Microbiol 2005; 71(6):3199–204.PubMedCrossRefGoogle Scholar
  75. 75.
    Frydman HM, Li JM, Robson DN et al. Somatic stem cell niche tropism in Wolbachia. Nature 2006; 44l(7092):509–12.CrossRefGoogle Scholar
  76. 76.
    Bouchon D, Rigaud T, Juchault P. Evidence for widespread Wolbachia infection in isopod crustaceans: Molecular identification and host feminization. Proc R Soc Lond B Biol Sci 1998; 265(l401):1081–90.CrossRefGoogle Scholar
  77. 77.
    Kang L, Ma X, Cai L et al. Superinfection of Laodelphax striatellus with Wolbachia from Drosophila simulans. Heredity 2003; 90(l):71–6.PubMedCrossRefGoogle Scholar
  78. 78.
    Ruang-Areerate T, Kittayapong P. Wolbachia transinfection in Aedes aegypti: A potential gene driver of dengue vectors. Proc Natl Acad Sci USA 2006; 103(33): 12534–9.PubMedCrossRefGoogle Scholar
  79. 79.
    Riegler M, Charlat S, Stauffer C et al. Wolbachia transfer from Rhagoletis cerasi to Drosophila simulans: Investigating the outcomes of host-symbiont coevolution. Appl Environ Microbiol 2004; 70(l):273–9.PubMedCrossRefGoogle Scholar
  80. 80.
    Noda H, Miyoshi T, Koizumi Y. In vitro cultivation of Wolbachia in insect and mammalian cell lines. In Vitro Cell Dev Biol Anim 2002; 38(7):423–7.CrossRefGoogle Scholar
  81. 81.
    Dobson SL, Marsland EJ, Veneti Z et al. Characterization of Wolbachia host cell range via the in vitro establishment of infections. Appl Environ Microbiol 2002; 68(2):656–60.PubMedCrossRefGoogle Scholar
  82. 82.
    O’Neill SL, Pettigrew MM, Sinkins SP et al. In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line. Insect Mol Biol 1997; 6(l):33–9.PubMedCrossRefGoogle Scholar
  83. 83.
    Kubota M, Morii T, Miura K. In vitro cultivation of parthenogenesis-inducing Wolbachia in an Aedes albopictus cell line. Entomol Exp Appl 2005; 117:83–7.CrossRefGoogle Scholar
  84. 84.
    Bartley LM, Donnelly CA, Garnett GP. The seasonal pattern of dengue in endemic areas: Mathematical models of mechanisms. Trans R Soc Trop Med Hyg 2002; 96(4):387–97.PubMedCrossRefGoogle Scholar
  85. 85.
    Wearing HJ, Rohani P. Ecological and immunological determinants of dengue epidemics. Proc Natl Acad Sci USA 2006; 103(31):11802–7.PubMedCrossRefGoogle Scholar
  86. 86.
    Vezzani D, Rubio A, Velazquez SM et al. Detailed assessment of microhabitat suitability for Aedes aegypti (Diptera: Culicidae) in Buenos Aires, Argentina. Acta Trop 2005; 95(2): 123–31.PubMedCrossRefGoogle Scholar
  87. 87.
    Wu M, Sun LV, Vamathevan J et al. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: A streamlined genome overrun by mobile genetic elements. PLoS Biol 2004; 2(3):E69.PubMedCrossRefGoogle Scholar
  88. 88.
    Sun LV, Riegler M, O’Neill SL. Development of a physical and genetic map of the virulent Wolbachia strain wMelPop. J Bacteriol 2003; 185(24):7077–84.PubMedCrossRefGoogle Scholar
  89. 89.
    Riegler M, Sidhu M, Miller WJ et al. Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol 2005; 15(15):1428–33.PubMedCrossRefGoogle Scholar
  90. 90.
    Valencia JI, Muller HJ. The mutational potentialities of some individual loci in Drosophila. Hereditas, Lund: Proc 8th Intl Congr Genet 1948 Hereditas (Lund) 1949:681–3.Google Scholar
  91. 91.
    Kaaya GP, Munyinyi DM. Biocontrol potential of the entomogenous fungi Beauveria bassiana and Metarhizium anisopliae for testse flies (Glossina spp.) at developmental sites. J Invertebr Pathol 1995; 66:237–41.PubMedCrossRefGoogle Scholar
  92. 92.
    Kaaya GP. Glossina morsitans morsitans: Mortalities caused in adults by experimental infection with entomopathogenic fungi. Acta Trop 1989; 46:107–14.PubMedCrossRefGoogle Scholar
  93. 93.
    Clark TB, Kellen W, Fukuda T et al. Field and laboratory studies on the pathogenicity of the fungus Beauveria bassiana to three genera of mosquitoes. J Invertebr Path 1968; 11:1–7.CrossRefGoogle Scholar
  94. 94.
    Soares Jr GG. Pathogenesis of infection by the hyphomycetous fungus Tolypldadium cylindrosporum in Aedes sierrensis and Culex tarsalis (Dipt.: Culicidae). Entomophaga 1982; 27:283–300.CrossRefGoogle Scholar
  95. 95.
    Scholte EJ, Njiru BN, Smallegange RC et al. Infection of malaria (Anopheles gambiae s.s.) and filariasis (Culex quinquefasciatus) vectors with the entomopathogenic fungus Metarhizium anisopliae. Malar J 2003; 2:29.PubMedCrossRefGoogle Scholar
  96. 96.
    Scholte EJ, Takken W, Knols BGJ. Pathogenicity of six East African entomopathogenic fungi to adult Anopheles gambiae s.s. (Diptera: Culicidae) mosquitoes. Proc Exp Appl Entomol NEV Amsterdam 2003; 14:25–9.Google Scholar
  97. 97.
    Scholte EJ, Ng’habi K, Kihonda J et al. An entomopathogenic fungus for control of adult African malaria mosquitoes. Science 2005; 308(5728):1641–2.PubMedCrossRefGoogle Scholar
  98. 98.
    Scholte EJ, Knols BG, Takken W. Infection of the malaria mosquito Anopheles gambiae with the entomopathogenic fungus Metarhizium anisopliae reduces blood reeding and fecundity. J Invertebr Pathol 2006; 91(l):43–9.PubMedCrossRefGoogle Scholar
  99. 99.
    Barreau C, Jousset FX, Bergoin M. Pathogenicity of the Aedes albopictus parvovirus (AaPV), a denso-like virus, for Aedes aegypti mosquitoes. J Invertebr Pathol 1996; 68(3):299–309.PubMedCrossRefGoogle Scholar
  100. 100.
    Kittayapong P, Baisley KJ, O’Neill SL. A mosquito densovirus infecting Aedes aegypti and Aedes albopictus from Thailand. Am J Trop Med Hyg 1999; 61(4):612–7.PubMedGoogle Scholar
  101. 101.
    Ledermann JP, Suchman EL, Black WC et al. Infection and pathogenicity of the mosquito densoviruses AeDNV, HeDNV, and APeDNV in Aedes aegypti mosquitoes (Diptera: Culicidae). J Econ Entomol 2004; 97(6): 1828–35.PubMedGoogle Scholar
  102. 102.
    Suchman E, Carlson J. Production of mosquito densonucleosis viruses by Aedes albopictus C6/36 cells adapted to suspension culture in serum-free protein-free media. In Vitro Cell Dev Biol Anim 2004; 40(3–4):74–5.CrossRefGoogle Scholar
  103. 103.
    Suchman E, Kononko A, Plake E et al. Effects of AeDNV infection on Aedes aegypti lifespan and reproduction. Biol Control 2006; 39(3):456–473.CrossRefGoogle Scholar
  104. 104.
    Barreau C, Jousset FX, Bergoin M. Venereal and vertical transmission of the Aedes albopictus parvovirus in Aedes aegypti mosquitoes. Am J Trop Med Hyg 1997; 57(2): 126–31.PubMedGoogle Scholar
  105. 105.
    Jousset FX, Baquerizo E, Bergoin M. A new densovirus isolated from the mosquito Culex pipiens (Diptera: Culicidae). Virus Res 2000; 67(l):11–6.PubMedCrossRefGoogle Scholar
  106. 106.
    Jousset FX, Barreau C, Boublik Y et al. A parvo-like virus persistently infecting a C6/36 clone of Aedes albopictus mosquito cell-line and pathogenic for Aedes aegypti larvae. Virus Res 1993; 29(2):99–114.PubMedCrossRefGoogle Scholar
  107. 107.
    O’Neill SL, Kittayapong P, Braig HR et al. Insect densoviruses may be widespread in mosquito cell lines. J Gen Virol 1995; 76(Pt 8):2067–74.PubMedCrossRefGoogle Scholar
  108. 108.
    Rwegoshora RT, Baisley KJ, Kittayapong P. Seasonal and spatial variation in natural densovirus infection in Anopheles minimus S.L. in Thailand. Southeast Asian J Trop Med Public Health 2000; 31(l):3–9.PubMedGoogle Scholar
  109. 109.
    Service MW. Mosquito ecology: Field sampling methods. 2nd ed. London: Elsevier Applied Science Publishers, 1993.Google Scholar
  110. 110.
    Hagler JR, Jackson CG. Methods for marking insects: Current techniques and future prospects. Annu Rev Entomol 2001; 46:511–43.PubMedCrossRefGoogle Scholar
  111. 111.
    Muir LE, Kay BH. Aedes aegypti survival and dispersal estimated by mark-release-recapture in northern Australia. Am J Trop Med Hyg 1998; 58(3):277–82.PubMedGoogle Scholar
  112. 112.
    Gillies MT. Methods for assessing the density and survival of blood-sucking Diptera. Annu Rev Entomol 1974; 19:345–62.PubMedCrossRefGoogle Scholar
  113. 113.
    Detinova TS. Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria. WHO Monograph No 47. Geneva: World Health Organization, 1962:216.Google Scholar
  114. 114.
    Tyndale-Biscoe M. Age-grading methods in adult insects: A review. Bull Entomol Res 1984; 74:341–77.CrossRefGoogle Scholar
  115. 115.
    Hoc TQ, Charlwood JD. Age determination of Aedes can tans using the ovarian oil injection technique. Med Vet Entomol 1990; 4(2):227–33.PubMedCrossRefGoogle Scholar
  116. 116.
    Hoc TQ, Schaub GA. Improvement of techniques for age grading hematophagous insects: Ovarian oil-injection and ovariolar separation techniques. J Med Entomol 1996; 33(3):286–9.PubMedGoogle Scholar
  117. 117.
    Mondet B. Application of the Polovodova’s method to the determination of the physiological age of Aedes (Diptera: Culicidae) transmitting yellow fever. Ann Soc Entomol Fr 1993; 29(l):61–76.Google Scholar
  118. 118.
    Lardeux F, Ung A, Chebret M. Spectrofluorometers are not adequate for aging Aedes and Culex (Diptera: Culicidae) using pteridine fluorescence. J Med Entomol 2000; 37(5):769–73.PubMedCrossRefGoogle Scholar
  119. 119.
    Penilla RP, Rodriguez MH, Lopez AD et al. Pteridine concentrations differ between insectary-reared and field-collected Anopheles albimanus mosquitoes of the same physiological age. Med Vet Entomol 2002; 16(3):225–34.PubMedCrossRefGoogle Scholar
  120. 120.
    Wu D, Lehane MJ. Pteridine fluorescence for age determination of Anopheles mosquitoes. Med Vet Entomol 1999; 13(l):48–52.PubMedCrossRefGoogle Scholar
  121. 121.
    Brei B, Edman JD, Gerade B et al. Relative abundance of two cuticular hydrocarbons indicates whether a mosquito is old enough to transmit malaria parasites. J Med Entomol 2004; 41(4):807–9.PubMedGoogle Scholar
  122. 122.
    Desena ML, Clark JM, Edman JD et al. Potential for aging female Aedes aegypti (Diptera: Culicidae) by gas Chromatographic analysis of cuticular hydrocarbons, including a field evaluation. J Med Entomol 1999; 36(6):811–23.PubMedGoogle Scholar
  123. 123.
    Desena ML, Edman JD, Clark JM et al. Aedes aegypti (Diptera: Culicidae) age determination by cuticular hydrocarbon analysis of female legs. J Med Entomol 1999; 36(6):824–30.PubMedGoogle Scholar
  124. 124.
    Gerade BB, Lee SH, Scott TW et al. Field validation of Aedes aegypti (Diptera: Culicidae) age estimation by analysis of cuticular hydrocarbons. J Med Entomol 2004; 4l(2):231–8.Google Scholar
  125. 125.
    Hayes EJ, Wall R. Age-grading adult insects: A review of techniques. Physiol Entomol 1999; 24(l):1–10.CrossRefGoogle Scholar
  126. 126.
    Caputo B, Dani FR, Home GL et al. Identification and composition of cuticular hydrocarbons of the major Afrotropical malaria vector Anopheles gambiae s.s. (Diptera: Culicidae): Analysis of sexual dimorphism and age-related changes. J Mass Spectrom 2005; 40(12): 1595–604.PubMedCrossRefGoogle Scholar
  127. 127.
    Hugo LE, Kay BH, Eaglesham GK et al. Investigation of cuticular hydrocarbons for determining the age and survivorship of Australasian mosquitoes. Am J Trop Med Hyg 2006; 74(3):462–74.PubMedGoogle Scholar
  128. 128.
    Cook PE, Hugo LE, Iturbe-Ormaetxe I et al. The use of transcriptional profiles to predict adult mosquito age under field conditions. Proc Natl Acad Sci USA 2006; 103(48): 108060–5.CrossRefGoogle Scholar
  129. 129.
    Marinotti O, Calvo E, Nguyen QK et al. Genome-wide analysis of gene expression in adult Anopheles gambiae. Insect Mol Biol 2006; 15(1):1–12.PubMedCrossRefGoogle Scholar
  130. 130.
    Arbeitman MN, Furlong EEM, Imam F et al. Gene expression during the life cycle of Drosophila melanogaster. Science 2002; 297(5590):2270–5.PubMedCrossRefGoogle Scholar
  131. 131.
    Pletcher SD, Macdonald SJ, Marguerie R et al. Genome-wide transcript profiles in aging and calorically restricted Drosophila melanogaster. Curr Biol 2002; 12(9):712–23.PubMedCrossRefGoogle Scholar
  132. 132.
    Kanzok SM, Jacobs-Lorena M. Entomopathogenic fungi as biological insecticides to control malaria. Trends Parasitol 2006; 22(2):49–51.PubMedCrossRefGoogle Scholar
  133. 133.
    Scholte EJ, Knols BGJ, Samson RA et al. Entomopathogenic fungi for mosquito control: A review. J Insect Sci 2004; 4.Google Scholar
  134. 134.
    Paul REL, Ariey F, Robert V. The evolutionary ecology of Plasmodium. Ecol Lett 2003; 6(9):866–80.CrossRefGoogle Scholar
  135. 135.
    Mackinnon MJ, Bell A, Read AF. The effects of mosquito transmission and population bottlenecking on virulence, multiplication rate and rosetting in rodent malaria. Int J Parasitol 2005; 35(2): 145–53.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  • Peter E. Cook
    • 1
  • Conor J. McMeniman
    • 1
  • Scott L. O’Neill
    • 1
  1. 1.School of Integrative BiologyThe University of QueenslandBrisbaneAustralia

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