1921
Volume 77, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

The feeding behavior of vectors influences the likelihood of pathogen invasion and the exposure of humans to vector-borne zoonotic pathogens. We used multilocus microsatellite genetic typing of an introduced mosquito vector and DNA sequencing of mosquito blood meals to determine the impact of hybrid ancestry on feeding behavior and the emergence of West Nile virus (WNV). The probability of ancestry of mosquitoes from two bionomically divergent forms, form molestus and form pipiens, influenced the probability that they fed on humans but did not explain a late summer feeding shift from birds to humans. We used a simple model to show that the occurrence of pure form molestus mosquitoes would have decreased the likelihood of WNV invasion ( in bird populations) 3- to 8-fold, whereas the occurrence of pure forms pipiens mosquitoes would have halved human exposure compared with the hybrids that are present. Data and modeling suggest that feeding preferences may be influenced by genetic ancestry and contribute to the emergence of vector-borne pathogens transmitted by introduced species, including malaria, and dengue, Chikungunya, yellow fever, and West Nile viruses.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.2007.77.667
2007-10-01
2017-09-19
Loading full text...

Full text loading...

/deliver/fulltext/14761645/77/4/0770667.html?itemId=/content/journals/10.4269/ajtmh.2007.77.667&mimeType=html&fmt=ahah

References

  1. Weaver SC, 2005. Host range, amplification and arboviral disease emergence. Arch Virol Suppl: 33–44.
  2. Tempelis CH, 1974. Host-feeding patterns of mosquitoes with a review of advances in analysis of blood meals by serology. J Med Entomol 11 : 635–653.
  3. Turell MJ, Sardelis MR, O’Guinn ML, Dohm DJ, 2002. Potential vectors of West Nile virus in North America. Mackenzie J, Barrett A, Deubel V, eds. Japanese Encephalitis and West Nile Viruses. Vol. 267 Current Topics in Microbiology and Immunology. Berlin: Springer-Verlag, 241–252.
  4. Mukwaya LG, Kayondo JK, Crabtree MB, Savage HM, Bigger-staff BJ, Miller BR, 2000. Genetic differentiation in the yellow fever virus vector, Aedes simpsoni complex, in Africa: sequence variation in the ribosomal DNA internal transcribed spacers of anthropophilic and non-anthropophilic populations. Insect Mol Biol 9 : 85–91.
  5. Arredondojimenez JI, Bown DN, Rodriguez MH, Villarreal C, Loyola EG, Frederickson CE, 1992. Tests for the existence of genetic determination or conditioning in host selection by Anopheles albimanus (Diptera, Culicidae). J Med Entomol 29 : 894–897.
  6. Hii JLK, Chew M, Sang VY, Munstermann LE, Tan SG, Panyim S, Yasothornsrikul S, 1991. Population genetic-analysis of host seeking and resting behaviors in the malaria vector, Anopheles balabacensis (Diptera, Culicidae). J Med Entomol 28 : 675–684.
  7. Powell JR, Tabachnick WJ, Arnold J, 1980. Genetics and the origin of a vector population-Aedes aegypti, a case study. Science 208 : 1385–1387.
  8. Tabachnick WJ, Black WC, 1995. Making a case for molecular population genetic-studies of arthropod vectors. Parasitol Today 11 : 27–30.
  9. Killeen GF, Fillinger U, Kiche I, Gouagna LC, Knols BGJ, 2002. Eradication of Anopheles gambiae from Brazil: lessons for malaria control in Africa? Lancet Infect Dis 2 : 618–627.
  10. Tatem AJ, Hay SI, Rogers DJ, 2006. Global traffic and disease vector dispersal. Proc Natl Acad Sci USA 103 : 6242–6247.
  11. Kilpatrick AM, Kramer LD, Campbell S, Alleyne EO, Dobson AP, Daszak P, 2005. West Nile virus risk assessment and the bridge vector paradigm. Emerg Infect Dis 11 : 425–429.
  12. Kramer LD, Bernard KA, 2001. West Nile virus infection in birds and mammals. Ann N Y Acad Sci 951 : 84–93.
  13. Hubalek Z, Halouzka J, 1999. West Nile fever—a reemerging mosquito-borne viral disease in Europe. Emerg Infect Dis 5 : 643–650.
  14. Fonseca DM, Keyghobadi N, Malcolm CA, Mehmet C, Schaffner F, Mogi M, Fleischer RC, Wilkerson RC, 2004. Emerging vectors in the Culex pipiens complex. Science 303 : 1535–1538.
  15. Harbach RE, Harrison BA, Gad AM, 1984. Culex (Culex) molestus Forskal (Diptera: Culicidae): neotype designation, description, variation, and taxonomic status. Proc Entomol Soc Wash 86 : 521–542.
  16. Spielman A, 2001. Structure and seasonality of nearctic Culex pipiens populations. Ann N Y Acad Sci 951 : 220–234.
  17. Fonseca DM, Keyghobadi N, Malcolm CA, Schaffner F, Mogi M, Fleischer RC, Wilkerson RC, 2004. Outbreak of West Nile virus in North America—response. Science 306 : 1473–1475.
  18. Urbanelli S, Silvestrini F, Reisen WK, De Vito E, Bullini L, 1997. Californian hybrid zone between Culex pipiens pipiens and Cx. p. quinquefasciatus revisited (Diptera:Culicidae). J Med Entomol 34 : 116–127.
  19. Samuel PP, Arunachalam N, Hiriyan J, Thenmozhi V, Gajanana A, Satyanarayana K, 2004. Host-feeding pattern of Culex quinquefasciatus Say and Mansonia annulifera (Theobald) (Diptera: Culicidae), the major vectors of filariasis in a rural area of south India. J Med Entomol 41 : 442–446.
  20. Zinser M, Ramberg F, Willott E, 2004. Culex quinquefasciatus (Diptera: Culicidae) as a potential West Nile virus vector in Tucson, Arizona: blood meal analysis indicates feeding on both humans and birds. J Insect Sci 4 : 20.
  21. Apperson CS, Hassan HK, Harrison BA, Savage HM, Aspen SE, Farajollahi A, Crans W, Daniels TJ, Falco RC, Benedict M, Anderson M, McMillen L, Unnasch TR, 2004. Host feeding patterns of established and potential mosquito vectors of West Nile virus in the eastern United States. Vector Borne Zoonotic Dis 4 : 71–82.
  22. Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD, 2006. Host heterogeneity dominates West Nile virus transmission. Proceedings of the Royal Society B: Biological Sciences 273 : 2327–2333.
  23. Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P, 2006. West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol 4 : 606–610.
  24. Crabtree MB, Savage HM, Miller BR, 1995. Development of a species-diagnostic polymerase chain reaction assay for the identification of Culex vectors of St. Louis encephalitis virus based on interspecies sequence variation in ribosomal DNA spacers. Am J Trop Med Hyg 53 : 105–109.
  25. Barr AR, 1957. The distribution of Culex p. pipiens and Culex p. quinquefasciatus in North America. Am J Trop Med Hyg 6 : 153–165.
  26. Fonseca DM, Atkinson CT, Fleischer RC, 1998. Microsatellite primers for Culex pipiens quinquefasciatus, the vector of avian malaria in Hawaii. Mol Ecol 7 : 1617–1619.
  27. Keyghobadi N, Matrone MA, Ebel GD, Kramer LD, Fonseca DM, 2004. Microsatellite loci from the northern house mosquito (Culex pipiens), a principal vector of West Nile virus in North America. Mol Ecol Notes 4 : 20–22.
  28. Smith JL, Fonseca DM, 2004. Rapid assays for identification of members of the Culex (Culex) pipiens complex, their hybrids, and other sibling species (Diptera: culicidae). Am J Trop Med Hyg 70 : 339–345.
  29. Pritchard JK, Stephens M, Donnelly P, 2000. Inference of population structure using multilocus genotype data. Genetics 155 : 945–959.
  30. Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, Zhivotovsky LA, Feldman MW, 2002. Genetic structure of human populations. Science 298 : 2381–2385.
  31. Bahnck CM, Fonseca DM, 2006. Rapid assay to identify the two genetic forms of Culex (Culex) pipiens L. (Diptera: culicidae) and hybrid populations. Am J Trop Med Hyg 75 : 251–255.
  32. Dobson AP, Foufopoulos J, 2001. Emerging infectious pathogens of wildlife. Philos Trans R Soc Lond B Biol Sci 356 : 1001–1012.
  33. Wonham MJ, de-Camino-Beck T, Lewis MA, 2004. An epidemiological model for West Nile virus: invasion analysis and control applications. Proc R Soc Lond B Biol Sci 271 : 501–507.
  34. Biggerstaff B, Petersen L, 2002. Estimated risk of West Nile virus transmission through blood transfusion during an epidemic in Queens, New York City. Transfusion 42 : 1019–1026.
  35. Anderson RM, May RM, 1991. Infectious diseases of humans. Dynamics and control. London: Oxford University Press.
  36. Woolhouse MEJ, Dye C, Etard JF, Smith T, Charlwood JD, Garnett GP, Hagan P, Hii JLK, Ndhlovu PD, Quinnell RJ, Watts CH, Chandiwana SK, Anderson RM, 1997. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci USA 94 : 338–342.
  37. Dye C, Hasibeder G, 1986. Population dynamics of mosquito-borne disease—effects of flies which bite some people more frequently than others. Trans R Soc Trop Med Hyg 80 : 69–77.
  38. Hasibeder G, Dye C, 1988. Population-dynamics of mosquito-borne disease—persistence in a completely heterogeneous environment. Theor Popul Biol 33 : 31–53.
  39. Besansky NJ, Hill CA, Costantini C, 2004. No accounting for taste: host preference in malaria vectors. Trends Parasitol 20 : 249–251.
  40. Ulloa A, Arredondo-Jimenez JI, Rodriguez MH, Fernandez-Salas I, Gonzalez-Ceron L, 2004. Innate host selection in Anopheles vestitipennis from southern Mexico. J Am Mosq Control Assoc 20 : 337–341.
  41. La Deau SL, Kilpatrick AM, Marra PP, 2007. West Nile virus emergence and large-scale declines of North American bird populations. Nature 447 : 710–713.
  42. Kilpatrick AM, Daszak P, Goodman SJ, Rogg H, Kramer LD, Cedeno V, Cunningham AA, 2006. Predicting pathogen introduction: West Nile virus spread to Galapagos. Conserv Biol 20 : 1224–1231.
  43. Kilpatrick AM, Gluzberg Y, Burgett J, Daszak P, 2004. A quantitative risk assessment of the pathways by which West Nile virus could reach Hawaii. Ecohealth 1 : 205–209.
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.2007.77.667
Loading
/content/journals/10.4269/ajtmh.2007.77.667
Loading

Data & Media loading...

  • Received : 14 Mar 2007
  • Accepted : 02 Jul 2007

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error