Advertisement

Considerations for male fitness in successful genetic vector control programs

  • Michelle E. H. Helinski
  • Laura C. Harrington
Chapter
Part of the Ecology and control of vector-borne diseases book series (ECVD, volume 3)

Abstract

A number of genetic control strategies, including sterile, transgenic, and Wolbachia-based approaches, are under development to reduce mosquito vector populations and the impact of important diseases such as malaria and dengue. Fitness of released males is critically important for the success of these strategies. In order to understand how to optimise the success of released males, we need to determine how males behave in their natural environment and which factors contribute to their success. Male mosquito biology has received little attention, although recent contributions have advanced our knowledge in this area. These advances include the discovery of precopulatory acoustic interactions and the identification of seminal fluid proteins that may have profound effects on female physiology and behaviour. Gaps in our knowledge include detailed information on male survival, dispersal, and mating strategies in the field across a range of geographical and ecological settings in which genetic control strategies may be deployed. There is evidence from laboratory studies that age, body size, and conditions during larval development contribute to male mating success; however, verification of these findings in natural settings is lacking. Although fitness assessments of transgenic or sterile males in genetic control programs are often performed in the laboratory using laboratory-adapted colonies, we advocate that fitness studies are conducted in semi-field cages under ambient conditions where insects are challenged with wild-type mosquitoes to determine their true potential. Because of the considerable amount of time and costs involved with the execution of cage trials we recommend that researchers plan field cage studies as early as possible in the assessment process to prevent time delays.

Keywords

genetic control mosquitoes male fitness reproductive success field applications 

Notes

Acknowledgements

The authors wish to thank the members of the Harrington lab and reviewers for constructive comments during manuscript preparation. This study was supported by the NIH/NIAID grant 1R01AI095491.

References

  1. Adlakha V and Pillai MK (1975) Involvement of male accessory gland substance in the fertility of mosquitoes. J Insect Physiol 21: 1453-1455.PubMedGoogle Scholar
  2. Aksoy S (ed.) (2008) Transgenesis and the management of vector-borne disease. Springer, Dordrecht, the Netherlands.Google Scholar
  3. Aksoy S, Weiss B and Attardo G (2008) Paratransgenesis applied for control of tsetse transmitted sleeping sickness. Adv Exp Med Biol 627: 35-48.PubMedGoogle Scholar
  4. Alphey L (2002) Re-engineering the sterile insect technique. Insect Biochem Mol Biol 32: 1243-1247.PubMedGoogle Scholar
  5. Alphey L, Beard CB, Billingsley P, Coetzee M, Crisanti A, Curtis C, Eggleston P, Godfray C, Hemingway J, Jacobs-Lorena M, James AA, Kafatos FC, Mukwaya LG, Paton M, Powell JR, Schneider W, Scott TW, Sina B, Sinden R, Sinkins S, Spielman A, Toure Y and Collins FH (2002) Malaria control with genetically manipulated insect vectors. Science 298: 119-121.PubMedGoogle Scholar
  6. Amenya DA, Bonizzoni M, Isaacs AT, Jasinskiene N, Chen H, Marinotti O, Yan G and James AA (2010) Comparative fitness assessment of Anopheles stephensi transgenic lines receptive to site-specific integration. Insect Mol Biol 19: 263-269.PubMedGoogle Scholar
  7. Asman SM, McDonald PT and Prout T (1981) Field studies of genetic control systems for mosquitoes. Annu Rev Entomol 26: 289-318.PubMedGoogle Scholar
  8. Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD and Wolfner MF (2010) Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56: 21-40.Google Scholar
  9. Bargielowski I, Nimmo D, Alphey L and Koella JC (2010) Comparison of life history characteristics of the genetically modified OX513A line and a wild type strain of Aedes aegypti. PLoS One 6: e20699.Google Scholar
  10. Beard CB, Cordon-Rosales C and Durvasula RV (2002) Bacterial symbionts of the triatominae and their potential use in control of Chagas disease transmission. Annu Rev Entomol 47: 123-141.PubMedGoogle Scholar
  11. Beard CB, Dotson EM, Pennington PM, Eichler S, Cordon-Rosales C and Durvasula RV (2001) Bacterial symbiosis and paratransgenic control of vector-borne Chagas disease. Int J Parasitol 31: 621-627.PubMedGoogle Scholar
  12. Bellini R, Albieri A, Balestrino F, Carrieri M, Porretta D, Urbanelli S, Calvitti M, Moretti R and Maini S (2010) Dispersal and survival of Aedes albopictus (Diptera: Culicidae) males in Italian urban areas and significance for sterile insect technique application. J Med Entomol 47: 1082-1091.PubMedGoogle Scholar
  13. Benedict M, D’Abbs P, Dobson S, Gottlieb M, Harrington L, Higgs S, James A, James S, Knols B, Lavery J, O’Neill S, Scott T, Takken W and Toure Y (2008) Guidance for contained field trials of vector mosquitoes engineered to contain a gene drive system: recommendations of a scientific working group. Vector Borne Zoonotic Dis 8: 127-166.PubMedGoogle Scholar
  14. Benedict MQ, Knols BG, Bossin HC, Howell PI, Mialhe E, Caceres C and Robinson AS (2009) Colonisation and mass rearing: learning from others. Malar J 8 Suppl 2: S4.Google Scholar
  15. Benedict MQ and Robinson AS (2003) The first releases of transgenic mosquitoes: an argument for the sterile insect technique. Trends Parasitol 19: 349-355.PubMedGoogle Scholar
  16. Boller E (1972) Behavioral aspects of mass rearing of insects. Entomophaga 17: 9-25.Google Scholar
  17. Brelsfoard CL, Sechan Y and Dobson SL (2008) Interspecific hybridization yields strategy for South Pacific filariasis vector elimination. PLoS Negl Trop Dis 2: e129.PubMedGoogle Scholar
  18. Briegel H (1990) Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J Insect Physiol 36: 165-172.Google Scholar
  19. Buonaccorsi JP, Harrington LC and Edman JD (2003) Estimation and comparison of mosquito survival rates with release-recapture-removal data. J Med Entomol 40: 6-17.PubMedGoogle Scholar
  20. Cabrera M and Jaffe K (2007) An aggregation pheromone modulates lekking behavior in the vector mosquito Aedes aegypti (Diptera: Culicidae). J Am Mosq Control Assoc 23: 1-10.PubMedGoogle Scholar
  21. Cáceres C, McInnis D, Shelly T, Jang E, Robinson A and Hendrichs J (2007) Quality management systems for fruit fly (Diptera: Tephritidae) sterile insect technique. Fla Entomol 90: 1-9.Google Scholar
  22. Caputo B, Dani FR, Horne GL, N’Fale S, Diabate A, Turillazzi S, Coluzzi M, Costantini C, Priestman AA, Petrarca V and della Torre A (2007) Comparative analysis of epicuticular lipid profiles of sympatric and allopatric field populations of Anopheles gambiae s.s. molecular forms and An. arabiensis from Burkina Faso (West Africa). Insect Biochem Mol Biol 37: 389-398.PubMedGoogle Scholar
  23. Carter V and Hurd H (2010) Choosing anti-Plasmodium molecules for genetically modifying mosquitoes: focus on peptides. Trends Parasitol 26: 582-590.PubMedGoogle Scholar
  24. Cator LJ, Arthur BJ, Harrington LC and Hoy RR (2009) Harmonic convergence in the love songs of the dengue vector mosquito. Science 323: 1077-1079.PubMedGoogle Scholar
  25. Cator LJ, Arthur BJ, Ponlawat A and Harrington LC (2011) Behavioral observations and sound recordings of free-flight mating swarms of Ae. aegypti in Thailand. J Med Entomol In Press.Google Scholar
  26. Cator LJ and Harrington LC (2011) The harmonic convergence of fathers predicts the mating success of sons in the yellow fever mosquito. Anim Behav In Press.Google Scholar
  27. Cator LJ, Ng’habi KR, Hoy RR and Harrington LC (2010) Sizing up a mate: variation in production of and response to acoustic signals in Anopheles gambiae. Behav Ecol 21: 1033-1039.Google Scholar
  28. Catteruccia F, Benton JP and Crisanti A (2005) An Anopheles transgenic sexing strain for vector control. Nat Biotechnol 23: 1414-1417.PubMedGoogle Scholar
  29. Catteruccia F, Crisanti A and Wimmer EA (2009) Transgenic technologies to induce sterility. Malar J 8 Suppl 2: S7.Google Scholar
  30. Catteruccia F, Godfray HC and Crisanti A (2003) Impact of genetic manipulation on the fitness of Anopheles stephensi mosquitoes. Science 299: 1225-1227.PubMedGoogle Scholar
  31. Chambers EW, Hapairai L, Peel BA, Bossin H and Dobson SL (2011) Male mating competitiveness of a Wolbachia-introgressed Aedes polynesiensis strain under semi-field conditions. PLoS Negl Trop Dis 5: e1271.PubMedGoogle Scholar
  32. Chapman T, Bangham J, Vinti G, Seifried B, Lung O, Wolfner MF, Smith HK and Partridge L (2003) The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference. Proc Natl Acad Sci USA 100: 9923-9928.PubMedGoogle Scholar
  33. Charlwood JD, Pinto J, Sousa CA, Ferreira C and do Rosario VE (2002a) Male size does not affect mating success (of Anopheles gambiae in Sao Tome). Med Vet Entomol 16: 109-111.PubMedGoogle Scholar
  34. Charlwood JD, Pinto J, Sousa CA, Madsen H, Ferreira C and do Rosario VE (2002b) The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera: Culicidae) from Sao Tome Island. J Vector Ecol 27: 178-183.PubMedGoogle Scholar
  35. Charlwood JD, Thompson R and Madsen H (2003) Observations on the swarming and mating behaviour of Anopheles funestus from southern Mozambique. Malaria J 2: 2.Google Scholar
  36. Chen CH, Huang H, Ward CM, Su JT, Schaeffer LV, Guo M and Hay BA (2007) A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 316: 597-600.PubMedGoogle Scholar
  37. Chen PS, Stumm-Zollinger E, Aigaki T, Balmer J, Bienz M and Bohlen P (1988) A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell 54: 291-298.PubMedGoogle Scholar
  38. Clements AN (1999) The biology of mosquitoes. CABI Publishing, Wallingford, UK.Google Scholar
  39. Coates CJ, Jasinskiene N, Miyashiro L and James AA (1998) Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc Natl Acad Sci USA 95: 3748-3751.PubMedGoogle Scholar
  40. Corby-Harris V, Drexler A, Watkins de Jong L, Antonova Y, Pakpour N, Ziegler R, Ramberg F, Lewis EE, Brown JM, Luckhart S and Riehle MA (2010) Activation of Akt signaling reduces the prevalence and intensity of malaria parasite infection and lifespan in Anopheles stephensi mosquitoes. PLoS Pathog 6: e1001003.PubMedGoogle Scholar
  41. Costero A, Attardo GM, Scott TW and Edman JD (1998) An experimental study on the detection of fructose in Aedes aegypti. J Am Mosq Control Assoc 14: 234-242.PubMedGoogle Scholar
  42. Craig G (1970) Genetic control of insect vectors of disease. Act IV Congr Latin Z 1: 15-28.Google Scholar
  43. Curtis CF (1985) Genetic control of insect pests: growth industry or lead balloon. Biol J Linn Soc 26: 359-374.Google Scholar
  44. Curtis CF (2006) Review of previous applications of genetics to vector control. In: Knols BGJ and Louis C (eds.) Bridging laboratory and field research for genetic control of disease vectors. Springer, Dordrecht, the Netherlands, pp. 33-43.Google Scholar
  45. Dadd R, Asman S and Kleinjan J (1989) Essential fatty acid status of laboratory-reared mosquitos improved by supplementing crude larval foods with fish oils. Entomol Exp Appl 52: 149-158.Google Scholar
  46. Dame DA, Lowe RE and Williamson DL (1981) Assessment of released sterile Anopheles albimanus and Glossina morsitans morsitans. In: Kitzmiller JB and Kanda T (eds.) Cytogenetics and genetics of vectors. Elsevier Biomedical, Amsterdam, the Netherlands.Google Scholar
  47. Dame DA, Woodard DB, Ford HR and Weidhaas DE (1964) Field behavior of sexually sterile Anopheles quadrimaculatus males. Mosq News 24: 6-14.Google Scholar
  48. Dao A, Adamou A, Yaro AS, Maiga HM, Kassogue Y, Traore SF and Lehmann T (2008) Assessment of alternative mating strategies in Anopheles gambiae: does mating occur indoors? J Med Entomol 45: 643-652.PubMedGoogle Scholar
  49. Diabate A, Dao A, Yaro AS, Adamou A, Gonzalez R, Manoukis NC, Traore SF, Gwadz RW and Lehmann T (2009) Spatial swarm segregation and reproductive isolation between the molecular forms of Anopheles gambiae. Proc Biol Sci 276: 4215-4222.PubMedGoogle Scholar
  50. Diabate A, Yaro AS, Dao A, Diallo M, Huestis DL and Lehmann T (2011) Spatial distribution and male mating success of Anopheles gambiae swarms. BMC Evol Biol 11: 184.PubMedGoogle Scholar
  51. Dobson SL, Fox CW and Jiggins FM (2002) The effect of Wolbachia-induced cytoplasmic incompatibility on host population size in natural and manipulated systems. Proc Biol Sci 269: 437-445.PubMedGoogle Scholar
  52. Dottorini T, Nicolaides L, Ranson H, Rogers DW, Crisanti A and Catteruccia F (2007) A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior. Proc Natl Acad Sci USA 104: 16215-16220.PubMedGoogle Scholar
  53. Downe AE (1975) Internal regulation of rate of digestion of blood meals in the mosquito, Aedes aegypti. J Insect Physiol 21: 1835-1839.PubMedGoogle Scholar
  54. Dyck A, Hendrichs J and Robinson AS (2005) The sterile insect technique: principles and practice in area-wide integrated pest management. Springer, Dordrecht, the Netherlands.Google Scholar
  55. Dye C (1984) Models for the population dynamics of the yellow fever mosquito, Aedes aegypti. J Anim Ecol 53: 247-268.Google Scholar
  56. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, NJ, USA.Google Scholar
  57. Edman JD (1970) Rate of digestion of vertebrate blood in Aedes aegypti (L.). Effect of age, mating, and parity. Am J Trop Med Hyg 19: 1031-1033.PubMedGoogle Scholar
  58. Enserink M (2010) GM mosquito trial alarms opponents, strains ties in gates-funded project. Science 330: 1030-1031.PubMedGoogle Scholar
  59. Enserink M (2011) GM mosquito release in Malaysia surprises opponents and scientists – again. Science 27 January 2011. Available at: http://news.sciencemag.org/scienceinsider/2011/01/gm-mosquito-release-in-malaysia.html.
  60. Facchinelli L, Valerio L, Bond JG, Wise de Valdez M, Harrington LC, Ramsey JM, Casas-Martinez M and Scott TW (2011) Development of a semi-field system for contained field trials with Aedes aegypti in Southern México. Am J Trop Med Hyg 58: 248-256.Google Scholar
  61. Fang W, Vega-Rodriguez J, Ghosh AK, Jacobs-Lorena M, Kang A and St Leger RJ (2011) Development of transgenic fungi that kill human malaria parasites in mosquitoes. Science 331: 1074-1077.PubMedGoogle Scholar
  62. Favia G, Ricci I, Damiani C, Raddadi N, Crotti E, Marzorati M, Rizzi A, Urso R, Brusetti L, Borin S, Mora D, Scuppa P, Pasqualini L, Clementi E, Genchi M, Corona S, Negri I, Grandi G, Alma A, Kramer L, Esposito F, Bandi C, Sacchi L and Daffonchio D (2007) Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci USA 104: 9047-9051.PubMedGoogle Scholar
  63. Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, Gimnig JE, Fish D and Killeen GF (2010) Ecology: a prerequisite for malaria elimination and eradication. PLoS Med 7: e1000303.PubMedGoogle Scholar
  64. Ferguson HM, John B, Ng’habi K and Knols BG (2005) Redressing the sex imbalance in knowledge of vector biology. Trends Ecol Evol 20: 202-209.PubMedGoogle Scholar
  65. Fornadel CM, Norris LC, Glass GE and Norris DE (2010) Analysis of Anopheles arabiensis blood feeding behavior in southern Zambia during the two years after introduction of insecticide-treated bed nets. Am J Trop Med Hyg 83: 848-853.PubMedGoogle Scholar
  66. Foster WA (1995) Mosquito sugar feeding and reproductive energetics. Annu Rev Entomol 40: 443-474.PubMedGoogle Scholar
  67. Foster WA and Lea AO (1975) Renewable fecundity of male Aedes aegypti following replenishment of seminal vesicles and accessory glands. J Insect Physiol 21: 1083-1090.Google Scholar
  68. Franz AW, Jasinskiene N, Sanchez-Vargas I, Isaacs AT, Smith MR, Khoo CC, Heersink MS, James AA and Olson KE (2011) Comparison of transgene expression in Aedes aegypti generated by mariner Mos1 transposition and PhiC31 site-directed recombination. Insect Mol Biol 20: 587-598.PubMedGoogle Scholar
  69. Franz AW, Sanchez-Vargas I, Adelman ZN, Blair CD, Beaty BJ, James AA and Olson KE (2006) Engineering RNA interference-based resistance to dengue virus type 2 in genetically modified Aedes aegypti. Proc Natl Acad Sci USA 103: 4198-4203.PubMedGoogle Scholar
  70. Franz AW, Sanchez-Vargas I, Piper J, Smith MR, Khoo CC, James AA and Olson KE (2009) Stability and loss of a virus resistance phenotype over time in transgenic mosquitoes harbouring an antiviral effector gene. Insect Mol Biol 18: 661-672.PubMedGoogle Scholar
  71. 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 and Alphey L (2010) Female-specific flightless phenotype for mosquito control. Proc Natl Acad Sci USA 107: 4550-4554.PubMedGoogle Scholar
  72. Fuchs MS, Craig GB and Despommier DD (1969) The protein nature of the substance inducing female monogramy in Aedes aegypti. J Insect Physiol 15: 701-709.Google Scholar
  73. Fuchs MS, Craig GB, Jr. and Hiss EA (1968) The biochemical basis of female monogamy in mosquitoes. I. Extraction of the active principle from Aedes aegypti. Life Sci 7: 835-839.PubMedGoogle Scholar
  74. Fuchs MS and Hiss EA (1970) The partial purification and separation of the protein components of matrone from Aedes aegypti. J Insect Physiol 16: 931-939.PubMedGoogle Scholar
  75. Gary RE, Jr, Cannon JW, 3rd and Foster WA (2009) Effect of sugar on male Anopheles gambiae mating performance, as modified by temperature, space, and body size. Parasit Vectors 2: 19.PubMedGoogle Scholar
  76. Gibson G (1985) Swarming behaviour of the mosquito Culex pipiens quinquefasciatus: a quantitative analysis. Physiol Entom 10: 283-296.Google Scholar
  77. Gillies MT (1961) Studies on the dispersion and survival of Anopheles gambiae Giles in East Africa, by means of marking and release experiments. Bull Entomol Res 52: 99-127.Google Scholar
  78. Gillott C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48: 163-184.PubMedGoogle Scholar
  79. Gubler DJ and Bhattacharya NC (1972) Swarming and mating of Aedes (S.) albopictus in nature. Mosq News 32: 219-223.Google Scholar
  80. Gwadz RW and Craig GB, Jr. (1970) Female polygamy due to inadequate semen transfer in Aedes aegypti. Mosq News 30: 355-360.Google Scholar
  81. Hancock RG, Foster WA and Yee WL (1990) Courtship behavior of the mosquito Sabethes cyaneus (Diptera: Culicidae). J Insect Behav 3: 401-416.Google Scholar
  82. Harrington LC, Scott TW, Lerdthusnee K, Coleman RC, Costero A, Clark GG, Jones JJ, Kitthawee S, Kittayapong P, Sithiprasasna R and Edman JD (2005) Dispersal of the dengue vector Aedes aegypti within and between rural communities. Am J Trop Med Hyg 72: 209-220.PubMedGoogle Scholar
  83. Harris AF, Nimmo D, McKemey AR, Kelly N, Scaife S, Donnelly CA, Beech C, Petrie WD and Alphey L (2011) Field performance of engineered male mosquitoes. Nat Biotechnol 29: 1034-1037.PubMedGoogle Scholar
  84. Hartberg WK (1971) Observations on the mating behaviour of Aedes aegypti in nature. Bull WHO 45: 847-850.PubMedGoogle Scholar
  85. Hay BA, Chen CH, Ward CM, Huang H, Su JT and Guo M (2010) Engineering the genomes of wild insect populations: challenges, and opportunities provided by synthetic Medea selfish genetic elements. J Insect Physiol 56: 1402-1413.PubMedGoogle Scholar
  86. Helinski ME and Knols BG (2008) Mating competitiveness of male Anopheles arabiensis mosquitoes irradiated with a partially or fully sterilizing dose in small and large laboratory cages. J Med Entomol 45: 698-705.PubMedGoogle Scholar
  87. Helinski ME and Knols BG (2009) Sperm quantity and size variation in un-irradiated and irradiated males of the malaria mosquito Anopheles arabiensis Patton. Acta Trop 109: 64-69.PubMedGoogle Scholar
  88. Helinski ME, Parker AG and Knols BG (2009) Radiation biology of mosquitoes. Malar J 8 Suppl 2: S6.Google Scholar
  89. Helinski MEH and Harrington LC (2011) Male mating history and body size influence female fecundity and longevity of the dengue vector Aedes aegypti. J Med Entomol 48: 202-211.PubMedGoogle Scholar
  90. Helinski MEH, Valerio L, Facchinelli L, Scott TW, Ramsey J and Harrington LC (2012) Evidence of polyandry in a natural population of Aedes aegypti under semi-field conditions. Am J Trop Med Hyg 86: 635-641.PubMedGoogle Scholar
  91. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, Greenfield M, Durkan M, Leong YS, Dong Y, Cook H, Axford J, Callahan AG, Kenny N, Omodei C, McGraw EA, Ryan PA, Ritchie SA, Turelli M and O’Neill SL (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476: 454-457.PubMedGoogle Scholar
  92. Howell PI and Knols BG (2009) Male mating biology. Malar J 8 Suppl 2: S8.Google Scholar
  93. Huho BJ, Ng’habi KR, Killeen GF, Nkwengulila G, Knols BG and Ferguson HM (2006) A reliable morphological method to assess the age of male Anopheles gambiae. Malar J 5: 62.PubMedGoogle Scholar
  94. Huho BJ, Ng’habi KR, Killeen GF, Nkwengulila G, Knols BG and Ferguson HM (2007) Nature beats nurture: a case study of the physiological fitness of free-living and laboratory-reared male Anopheles gambiae s.l. J Exp Biol 210: 2939-2947.PubMedGoogle Scholar
  95. Irvin N, Hoddle MS, O’Brochta DA, Carey B and Atkinson PW (2004) Assessing fitness costs for transgenic Aedes aegypti expressing the GFP marker and transposase genes. Proc Natl Acad Sci USA 101: 891-896.PubMedGoogle Scholar
  96. Ito J, Ghosh A, Moreira LA, Wimmer EA and Jacobs-Lorena M (2002) Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417: 452-455.PubMedGoogle Scholar
  97. James AA (2005) Gene drive systems in mosquitoes: rules of the road. Trends Parasitol 21: 64-67.PubMedGoogle Scholar
  98. Jones JC (1973) A study on the fecundity of male Aedes aegypti. J Insect Physiol 19: 435-439.PubMedGoogle Scholar
  99. Jones TM (1974) Sexual activities during single and multiple co-habitations in Aedes aegypti mosquitoes. J Ent 48: 185-194.Google Scholar
  100. Kambris Z, Blagborough AM, Pinto SB, Blagrove MS, Godfray HC, Sinden RE and Sinkins SP (2010) Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae. PLoS Pathog 6: e1001143.PubMedGoogle Scholar
  101. Kim W, Koo H, Richman AM, Seeley D, Vizioli J, Klocko AD and 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: 447-455.Google Scholar
  102. Klowden M and Chambers G (1991) Male accessory gland substances activate egg development in nutritionally stressed Ae. aegypti mosquitoes. J Insect Physiol 37: 721-726.Google Scholar
  103. Klowden MJ and Lea AO (1979) Humoral inhibition of host-seeking in Aedes aegypti during oocyte maturation. J Insect Physiol 25: 231-235.PubMedGoogle Scholar
  104. Knipling EF (1955) Possibilities of insect population control through the use of sexually sterile males. J Econ Entomol 48: 459-462.Google Scholar
  105. Knols BGJ, Bossin HC, Mukabana WR and Robinson AS (2007) Transgenic mosquitoes and the fight against malaria: managing technology push in a turbulent GMO world. Am J Trop Med Hyg 77: 232-242.PubMedGoogle Scholar
  106. Koenraadt CJ, Kormaksson M and Harrington LC (2010) Effects of inbreeding and genetic modification on Aedes aegypti larval competition and adult energy reserves. Parasit Vectors 3: 92.PubMedGoogle Scholar
  107. Koenraadt CJ and Takken W (2011) Viability of GM fungi crucial to malaria control. Science 332: 175.PubMedGoogle Scholar
  108. Labbe GM, Nimmo DD and Alphey L (2010) Piggybac- and PhiC31-mediated genetic transformation of the Asian tiger mosquito, Aedes albopictus (Skuse). PLoS Negl Trop Dis 4: e788.PubMedGoogle Scholar
  109. Lacroix R, Delatte H, Hue T and Reiter P (2009) Dispersal and survival of male and female Aedes albopictus (Diptera: Culicidae) on Reunion Island. J Med Entomol 46: 1117-1124.PubMedGoogle Scholar
  110. Laven H (1967) Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature 216: 383-384.PubMedGoogle Scholar
  111. Lavery JV, Harrington LC and Scott TW (2008) Ethical, social, and cultural considerations for site selection for research with genetically modified mosquitoes. Am J Trop Med Hyg 79: 312-318.PubMedGoogle Scholar
  112. Lavoipierre MM (1958) Biting behavior of mated and unmated females of an African strain of Aedes aegypti. Nature 181: 1781-1782.PubMedGoogle Scholar
  113. Leahy M and Craig G (1965) Accessory gland substance as a stimulant for oviposition in Aedes aegypti and Ae. albopictus. Mosq News 25: 448-452.Google Scholar
  114. Legros M, Lloyd AL, Huang Y and Gould F (2009) Density-dependent intraspecific competition in the larval stage of Aedes aegypti (Diptera: Culicidae): revisiting the current paradigm. J Med Entomol 46: 409-419.PubMedGoogle Scholar
  115. Li C, Marrelli MT, Yan G and Jacobs-Lorena M (2008) Fitness of transgenic Anopheles stephensi mosquitoes expressing the SM1 peptide under the control of a vitellogenin promoter. J Hered 99: 275-282.PubMedGoogle Scholar
  116. Liedo P, Salgado S, Oropeza A and Toledo J (2007) Improving mating performance of mass-reared sterile mediterrenean fruit flies (Diptera: Tephritidae) through changes in adult holding conditions: demography and mating competitiveness. Fla Entomol 90: 33-40.Google Scholar
  117. Lofgren CS, Dame DA, Breeland SG, Weidhaas DE, Jeffery G, Kaiser R, Ford HR, Boston MD and Baldwin KF (1974) Release of chemosterilized males for the control of Anopheles albimanus in El Salvador. 3. Field methods and population control. Am J Trop Med Hyg 23: 288-297.PubMedGoogle Scholar
  118. Lyimo EO and Takken W (1993) Effects of adult body size on fecundity and the pre-gravid rate of Anopheles gambiae females in Tanzania. Med Vet Entomol 7: 328-332.PubMedGoogle Scholar
  119. Magori K, Legros M, Puente ME, Focks DA, Scott TW, Lloyd AL and Gould F (2009) Skeeter Buster: a stochastic, spatially explicit modeling tool for studying Aedes aegypti population replacement and population suppression strategies. PLoS NTD 3: e508.Google Scholar
  120. Mahmood F and Reisen WK (1994) Anopheles culicifacies: effects of age on the male reproductive system and mating ability of virgin adult mosquitoes. Med Vet Entomol 8: 31-37.PubMedGoogle Scholar
  121. Manoukis NC, Diabate A, Abdoulaye A, Diallo M, Dao A, Yaro AS, Ribeiro JM and Lehmann T (2009) Structure and dynamics of male swarms of Anopheles gambiae. J Med Entomol 46: 227-235.PubMedGoogle Scholar
  122. Marchand RP (1984) Field observations on swarming and mating in Anopheles gambiae mosquitoes in Tanzania. Neth J Zool 24: 367-387.Google Scholar
  123. Marrelli MT, Li C, Rasgon JL and Jacobs-Lorena M (2007) Transgenic malaria-resistant mosquitoes have a fitness advantage when feeding on Plasmodium-infected blood. Proc Natl Acad Sci USA 104: 5580-5583.PubMedGoogle Scholar
  124. Marrelli MT, Moreira CK, Kelly D, Alphey L and Jacobs-Lorena M (2006) Mosquito transgenesis: what is the fitness cost? Trends Parasitol 22: 197-202.PubMedGoogle Scholar
  125. McMeniman CJ, Lane RV, Cass BN, Fong AW, Sidhu M, Wang YF and O’Neill SL (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323: 141-144.PubMedGoogle Scholar
  126. Meredith JM, Basu S, Nimmo DD, Larget-Thiery I, Warr EL, Underhill A, McArthur CC, Carter V, Hurd H, Bourgouin C and Eggleston P (2011) Site-specific integration and expression of an anti-malarial gene in transgenic Anopheles gambiae significantly reduces Plasmodium infections. PLoS One 6: e14587.PubMedGoogle Scholar
  127. Merritt RW, Dadd RH and Walker ED (1992) Feeding behavior, natural food, and nutritional relationships of larval mosquitoes. Annu Rev Entomol 37: 349-376.PubMedGoogle Scholar
  128. Moreira LA, Ito J, Ghosh A, Devenport M, Zieler H, Abraham EG, Crisanti A, Nolan T, Catteruccia F and Jacobs-Lorena M (2002) Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes. J Biol Chem 277: 40839-40843.PubMedGoogle Scholar
  129. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, Rocha BC, Hall-Mendelin S, Day A, Riegler M, Hugo LE, Johnson KN, Kay BH, McGraw EA, Van den Hurk AF, Ryan PA and O’Neill SL (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139: 1268-1278.PubMedGoogle Scholar
  130. Moreira LA, Wang J, Collins FH and Jacobs-Lorena M (2004) Fitness of anopheline mosquitoes expressing transgenes that inhibit Plasmodium development. Genetics 166: 1337-1341.PubMedGoogle Scholar
  131. Morlan HB, Elmo M, McCray JR and Kilpatrick JW (1962) Field tests with sexually sterile males for control of Aedes aegypti. Mosq News 22: 295-300.Google Scholar
  132. Muir LE and Kay BH (1998) Aedes aegypti survival and dispersal estimated by mark-release-recapture in northern Australia. Am J Trop Med Hyg 58: 277-282.PubMedGoogle Scholar
  133. Ng’habi KR, John B, Nkwengulila G, Knols BG, Killeen GF and Ferguson HM (2005) Effect of larval crowding on mating competitiveness of Anopheles gambiae mosquitoes. Malar J 4: 49.PubMedGoogle Scholar
  134. Nijhout HF and Craig GB (1971) Reproductive isolation in Stegomyia mosquitoes. III Evidence for a sexual pheromone. Entomol Exp Appl 14: 399-412.Google Scholar
  135. Nimmo D, Alphey L, Meredith J and Eggleston P (2006) High efficiency site-specific genetic engineering of the mosquito genome. Insect Mol Biol 15: 129-136.PubMedGoogle Scholar
  136. Nolan T, Papathanos P, Windbichler N, Magnusson K, Benton J, Catteruccia F and Crisanti A (2011) Developing transgenic Anopheles mosquitoes for the sterile insect technique. Genetica 139: 33-39.PubMedGoogle Scholar
  137. Odiere M, Bayoh MN, Gimnig J, Vulule J, Irungu L and Walker E (2007) Sampling outdoor, resting Anopheles gambiae and other mosquitoes (Diptera: Culicidae) in western Kenya with clay pots. J Med Entomol 44: 14-22.PubMedGoogle Scholar
  138. Oxitec (2011) Field trials in Brazil: a progress report. Oxitec Newsletter September 2011. Available at: http://www.oxitec.com/september-2011-newsletter/.
  139. Parker AG and Mehta K (2007) Sterile insect technique: a model for dose optimization for improved sterile insect quality. Fla Entomol 90: 88-95.Google Scholar
  140. Patterson RS, Weidhaas DE, Ford HR and Lofgren CS (1970) Suppression and elimination of an island population of Culex pipiens quinquefasciatus with sterile males. Science 168: 1368-1370.PubMedGoogle Scholar
  141. Pennetier C, Warren B, Dabire KR, Russell IJ and Gibson G (2010) ‘Singing on the wing’ as a mechanism for species recognition in the malarial mosquito Anopheles gambiae. Curr Biol 20: 131-136.PubMedGoogle Scholar
  142. Polerstock AR, Eigenbrode SD and Klowden MJ (2002) Mating alters the cuticular hydrocarbons of female Anopheles gambiae sensu stricto and Aedes aegypti (Diptera: Culicidae). J Med Entomol 39: 545-552.PubMedGoogle Scholar
  143. Ponlawat A and Harrington LC (2007) Age and body size influence male sperm capacity of the dengue vector Aedes aegypti (Diptera: Culicidae). J Med Entomol 44: 422-426.PubMedGoogle Scholar
  144. Ponlawat A and Harrington LC (2009) Factors associated with male mating success of the dengue vector mosquito, Aedes aegypti. Am J Trop Med Hyg 80: 395-400.PubMedGoogle Scholar
  145. Reisen W, Milby M, Asman S, Bock M, Meyer R, McDonald P and Reeves W (1982) Attempted suppression of a semi-isolated Culex tarsalis population by the release of irradiated males: a second experiment using males from a recently colonized strain. Mosq News 42: 565-575.Google Scholar
  146. Reisen WK and Aslamkhan M (1979) A release-recapture experiment with the malaria vector, Anopheles stephensi Liston, with observations on dispersal, survivorship, population size, gonotrophic rhythm and mating behaviour. Ann Trop Med Parasitol 73: 251-269.PubMedGoogle Scholar
  147. Reisen WK, Mahmood F and Parveen T (1980) Anopheles culicifacies Giles: a release-recapture experiment with cohorts of known age with implications for malaria epidemiology and genetical control in Pakistan. Trans R Soc Trop Med Hyg 74: 307-317.PubMedGoogle Scholar
  148. Ren X, Hoiczyk E and Rasgon JL (2008) Viral paratransgenesis in the malaria vector Anopheles gambiae. PLoS Pathog 4: e1000135.PubMedGoogle Scholar
  149. Riehle MM, Guelbeogo WM, Gneme A, Eiglmeier K, Holm I, Bischoff E, Garnier T, Snyder GM, Li X, Markianos K, Sagnon N and Vernick KD (2011) A cryptic subgroup of Anopheles gambiae is highly susceptible to human malaria parasites. Science 331: 596-598.PubMedGoogle Scholar
  150. Ritchie SA, Johnson PH, Freeman AJ, Odell RG, Graham N, Dejong PA, Standfield GW, Sale RW and O’Neill SL (2011) A secure semi-field system for the study of Aedes aegypti. PLoS Negl Trop Dis 5: e988.PubMedGoogle Scholar
  151. Robinson AS and Franz G (2000) The application of transgenic insect technology in the sterile insect technique. In: Handler M and James AA (eds.) Insect transgenesis:methods and applications. CRC Press, Baton Rouge, FL, USA, pp. 307-319.Google Scholar
  152. Rodrigues FG, Santos MN, De Carvalho TX, Rocha BC, Riehle MA, Pimenta PF, Abraham E, Jacobs-Lorena M, Alves de Brito CF and Moreira LA (2008) Expression of a mutated phospholipase A2 in transgenic Aedes fluviatilis mosquitoes impacts Plasmodium gallinaceum development. Insect Mol Biol 17: 175-183.PubMedGoogle Scholar
  153. Rogers DW, Baldini F, Battaglia F, Panico M, Dell A, Morris HR and Catteruccia F (2009) Transglutaminase-mediated semen coagulation controls sperm storage in the malaria mosquito. PLoS Biol 7: e1000272.PubMedGoogle Scholar
  154. Roth LM (1948) A study of mosquito behavior. An experimental laboratory study of the sexual behavior of Aedes aegypti (Linnaeus). Am Midl Nat 40: 265-352.Google Scholar
  155. Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP and Killeen GF (2011) Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J 10: 80.PubMedGoogle Scholar
  156. Santos MN, Nogueira PM, Dias FB, Valle D and Moreira LA (2010) Fitness aspects of transgenic Aedes fluviatilis mosquitoes expressing a Plasmodium-blocking molecule. Transgenic Res 19: 1129-1135.PubMedGoogle Scholar
  157. Schetelig MF, Scolari F, Handler AM, Kittelmann S, Gasperi G and Wimmer EA (2009) Site-specific recombination for the modification of transgenic strains of the Mediterranean fruit fly Ceratitis capitata. Proc Natl Acad Sci USA 106: 18171-18176.PubMedGoogle Scholar
  158. Scolari F, Siciliano P, Gabrieli P, Gomulski LM, Bonomi A, Gasperi G and Malacrida AR (2011) Safe and fit genetically modified insects for pest control: from lab to field applications. Genetica 139: 41-52.PubMedGoogle Scholar
  159. Scott TW, Takken W, Knols BG and Boëte C (2002) The ecology of genetically modified mosquitoes. Science 298: 117-119.PubMedGoogle Scholar
  160. Searcy WA and Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton, NJ, USA.Google Scholar
  161. Seawright JA, Kaiser PE and Dame DA (1977) Mating competitiveness of chemosterilized hybrid males of Aedes aegypti (L.) in field tests. Mosq News 37: 615-619.Google Scholar
  162. Service MW (1993) Mosquito ecology: field sampling methods. Chapman and Hall, London, UK.Google Scholar
  163. Service MW (1997) Mosquito (Diptera: Culicidae) dispersal – the long and short of it. J Med Entomol 34: 579-588.PubMedGoogle Scholar
  164. Sheppard PM, MacDonald WW, Tonn RJ and Grab B (1969) The dynamics of an adult population of Aedes aegypti in relation to dengue haemorrhagic fever in Bangkok. J Anim Ecol 38: 661-702.Google Scholar
  165. Shutt B, Stables L, Aboagye-Antwi F, Moran J and Tripet F (2010) Male accessory gland proteins induce female monogamy in anopheline mosquitoes. Med Vet Entomol 24: 91-94.PubMedGoogle Scholar
  166. Sinkins SP and Gould F (2006) Gene drive systems for insect disease vectors. Nat Rev Genet 7: 427-435.PubMedGoogle Scholar
  167. Sinkins SP and O’Neill SL (2000) Wolbachia as a vehicle to modify insect populations. In: Handler M and James AA (eds.) Insect transgenesis: methods and applications. CRC Press, Boca Raton, FL, USA, pp. 271-287.Google Scholar
  168. Sirot LK, Hardstone MC, Helinski MEH, Kimura M, Deewathanawong P, Wolfner MF and Harrington LC (2011) Towards a semen proteome of the dengue vector mosquito: protein identification and potential functions. Plos NTD 5: e989.Google Scholar
  169. Sirot LK, Poulson RL, McKenna MC, Girnary H, Wolfner MF and Harrington LC (2008) Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochem Mol Biol 38: 176-189.PubMedGoogle Scholar
  170. Snow JW (1988) Radiation, insects and eradication in North America. An overview from screwworm to bollworm. In: Modern Insect control: nuclear techniques and biotechnology. Proceedings of a symposium jointly organized by IAEA/FAO, Vienna, November 1987, IAEA-SM-301/29, pp. 8-10.Google Scholar
  171. Spencer CY, Pendergast IV TH and Harrington LC (2005) Fructose variation in the dengue vector, Aedes aegypti, during high and low transmission seasons in the Mae Sot region of Thailand. J Am Mosq C Assoc 21: 177-181.Google Scholar
  172. Takken W and Knols BG (1999) Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44: 131-157.PubMedGoogle Scholar
  173. Thailayil J, Magnusson K, Godfray HC, Crisanti A and Catteruccia F (2011) Spermless males elicit large-scale female responses to mating in the malaria mosquito Anopheles gambiae. Proc Natl Acad Sci USA 108: 13677-13681.PubMedGoogle Scholar
  174. Thomas DD, Donnelly CA, Wood RJ and Alphey LS (2000) Insect population control using a dominant, repressible, lethal genetic system. Science 287: 2474-2476.PubMedGoogle Scholar
  175. Touré YT and Manga L (2000) Ethical, legal and social issues in the use of genetically modified vectors for disease control. In: Knols BGJ and Louis C (eds.), Bridging laboratory and field research for genetic control of disease vectors. Springer, Dordrecht, the Netherlands, pp. 221-225.Google Scholar
  176. Tripet F, Toure YT, Dolo G and Lanzaro GC (2003) Frequency of multiple inseminations in field-collected Anopheles gambiae females revealed by DNA analysis of transferred sperm. Am J Trop Med Hyg 68: 1-5.PubMedGoogle Scholar
  177. Verhoek BA and Takken W (1994) Age effects on the insemination rate of Anopheles gambiae s.l. in the laboratory. Entomol Exp Appl 72: 167-172.Google Scholar
  178. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ, Leong YS, Dong Y, Axford J, Kriesner P, Lloyd AL, Ritchie SA, O’Neill SL and Hoffmann AA (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476: 450-453.PubMedGoogle Scholar
  179. Ward TW, Jenkins MS, Afanasiev BN, Edwards M, Duda BA, Suchman E, Jacobs-Lorena M, Beaty BJ and Carlson JO (2001) Aedes aegypti transducing densovirus pathogenesis and expression in Aedes aegypti and Anopheles gambiae larvae. Insect Mol Biol 10: 397-405.PubMedGoogle Scholar
  180. Warren B, Gibson G and Russell IJ (2009) Sex recognition through midflight mating duets in Culex mosquitoes is mediated by acoustic distortion. Curr Biol 19: 485-491.PubMedGoogle Scholar
  181. Weidhaas DE, Schmidt CH and Seabrook EL (1962) Field studies on the release of sterile males for the control of Anopheles quadrimaculatus. Mosq News 22: 283-291.Google Scholar
  182. Windbichler N, Menichelli M, Papathanos PA, Thyme SB, Li H, Ulge UY, Hovde BT, Baker D, Monnat RJ, Jr, Burt A and Crisanti A (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473: 212-215.PubMedGoogle Scholar
  183. Wise de Valdez MR, Nimmo D, Betz J, Gong HF, James AA, Alphey L and Black WCt (2011) Genetic elimination of dengue vector mosquitoes. Proc Natl Acad Sci USA 108: 4772-4775.PubMedGoogle Scholar
  184. Wise de Valdez MR, Suchman EL, Carlson JO and Black WC (2010) A large scale laboratory cage trial of Aedes densonucleosis virus (AeDNV). J Med Entomol 47: 392-399.PubMedGoogle Scholar
  185. Wolfner MF (2007) ‘S.P.E.R.M.’ (seminal proteins (are) essential reproductive modulators): the view from Drosophila. Soc Reprod Fertil Suppl 65: 183-199.PubMedGoogle Scholar
  186. Xi Z, Dean JL, Khoo C and Dobson SL (2005a) Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection. Insect Biochem Mol Biol 35: 903-910.PubMedGoogle Scholar
  187. Xi Z, Khoo CC and Dobson SL (2005b) Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310: 326-328.PubMedGoogle Scholar
  188. Xi Z, Khoo CC and Dobson SL (2006) Interspecific transfer of Wolbachia into the mosquito disease vector Aedes albopictus. Proc Biol Sci 273: 1317-1322.PubMedGoogle Scholar
  189. Yohannes M and Boelee E (2012) Early biting rhythm in the afro-tropical vector of malaria, Anopheles arabiensis, and challenges for its control in Ethiopia. Med Vet Entomol 26: 103-105.PubMedGoogle Scholar
  190. Yuval B (2006) Mating systems of blood-feeding flies. Ann Rev Entomol 51: 413-440.Google Scholar
  191. Yuval B and Bouskila A (1993) Temporal dynamics of mating and predation in mosquito swarms. Oecologia 95: 65-69.Google Scholar
  192. Yuval B and Fritz GN (1994) Multiple mating in female mosquitoes? Evidence from a field population of Anopheles freeborni (Diptera: Culicidae). BullEntomol Res 84: 137-139.Google Scholar
  193. Yuval B, Holliday-Hanson L and Washino RK (1994) Energy budget of swarming male mosquitoes. Ecol Entomol 19: 74-78.Google Scholar
  194. Yuval B, Wekesa JW and Washino RK (1993) Effects of body size on swarming behavior and mating success of male Anopheles freeborni (Diptera: Culicidae). J Insect Behav 6: 333-342.Google Scholar

Copyright information

© Wageningen Academic Publishers The Netherlands 2013

Authors and Affiliations

  • Michelle E. H. Helinski
    • 1
  • Laura C. Harrington
    • 2
  1. 1.Malaria Consortium Regional OfficeKampalaUganda
  2. 2.Department of EntomologyCornell UniversityIthacaUSA

Personalised recommendations