Multiplex Assay for Species Identification and Monitoring of Insecticide Resistance in Anopheles punctulatus Group Populations of Papua New Guinea

Cara N. Henry-Halldin Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by Cara N. Henry-Halldin in
Current site
Google Scholar
PubMed
Close
,
Kogulan Nadesakumaran Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by Kogulan Nadesakumaran in
Current site
Google Scholar
PubMed
Close
,
John Bosco Keven Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by John Bosco Keven in
Current site
Google Scholar
PubMed
Close
,
Allison M. Zimmerman Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by Allison M. Zimmerman in
Current site
Google Scholar
PubMed
Close
,
Peter Siba Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by Peter Siba in
Current site
Google Scholar
PubMed
Close
,
Ivo Mueller Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by Ivo Mueller in
Current site
Google Scholar
PubMed
Close
,
Manuel W. Hetzel Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by Manuel W. Hetzel in
Current site
Google Scholar
PubMed
Close
,
James W. Kazura Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by James W. Kazura in
Current site
Google Scholar
PubMed
Close
,
Edward Thomsen Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by Edward Thomsen in
Current site
Google Scholar
PubMed
Close
,
Lisa J. Reimer Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by Lisa J. Reimer in
Current site
Google Scholar
PubMed
Close
, and
Peter A. Zimmerman Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Papua New Guinea Institute of Medical Research, Madang, MADANG, Papua New Guinea; Papua New Guinea Institute of Medical Research, Goroka, EASTERN HIGHLANDS, Papua New Guinea; School of Population Health, University of Queensland, Brisbane, Australia

Search for other papers by Peter A. Zimmerman in
Current site
Google Scholar
PubMed
Close
Restricted access

Anopheles punctulatus sibling species (An. punctulatus s.s., Anopheles koliensis, and Anopheles farauti species complex [eight cryptic species]) are principal vectors of malaria and filariasis in the Southwest Pacific. Given significant effort to reduce malaria and filariasis transmission through insecticide-treated net distribution in the region, effective strategies to monitor evolution of insecticide resistance among An. punctulatus sibling species is essential. Mutations in the voltage-gated sodium channel (VGSC) gene have been associated with knock-down resistance (kdr) to pyrethroids and DDT in malarious regions. By examining VGSC sequence polymorphism we developed a multiplex assay to differentiate wild-type versus kdr alleles and query intron-based polymorphisms that enable simultaneous species identification. A survey including mosquitoes from seven Papua New Guinea Provinces detected no kdr alleles in any An. punctulatus species. Absence of VGSC sequence introgression between species and evidence of geographic separation within species suggests that kdr must be monitored in each An. punctulatus species independently.

Author Notes

*Address correspondence to Peter A. Zimmerman, Center for Global Health and Diseases, Case Western Reserve University School of Medicine, 10900 Euclid Avenue, Cleveland, OH 44106-7286. E-mail: paz@case.edu
†These authors contributed equally to this work.

Financial support: This study was supported by grants from National Institutes of Health (AI065717) and Fogarty International Center (TW007872, TW007377, and TW007735). Mosquito collection was also supported by the Global Fund to Fight Aids, Tuberculosis and Malaria Round 3 malaria grant to PNG.

Authors' addresses: Cara N. Henry-Halldin, Kogulan Nadesakumaran, Allison M. Zimmerman, James W. Kazura, and Peter A. Zimmerman, Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, OH, E-mails: vgx5@cdc.gov, kxn80@case.edu, amz23@case.edu, jxk14@case.edu, and paz@case.edu. John Bosco Keven, Edward Thomsen, and Lisa J. Reimer, Papua New Guinea Institute of Medical Research-Madang, Madang, Papua New Guinea, E-mails: jbkeven@gmail.com, edward.thomsen@case.edu, and lisa.reimer@case.edu. Peter Siba, Ivo Mueller, and Manuel W. Hetzel, Papua New Guinea Institute of Medical Research-Goroka, Eastern Highlands, Papua New Guinea, E-mails: peter.siba@pngimr.org.pg, ivomueller@fastmail.fm, and manuel.hetzel@pngimr.org.pg.

  • 1.

    Rozeboom LE, Knight KL, 1946. The punctulatus complex of Anopheles (Diptera: Culicidae). J Parasitol 32: 95131.

  • 2.

    Bryan JH, 1974. Morphological studies on the Anopheles punctulatus Dönitz complex. Trans R Entomol Soc Lond 125: 413435.

  • 3.

    Charlwood JD, Dagoro H, Paru R, 1985. Blood-feeding and resting behavior in the Anopheles punctulatus Dönitz complex (Diptera: Culicidae) from coastal Papua New Guinea. Bull Entomol Res 75: 463476.

    • Search Google Scholar
    • Export Citation
  • 4.

    Cooper RD, Waterson DG, Frances SP, Beebe NW, Sweeney AW, 2002. Speciation and distribution of the members of the Anopheles punctulatus (Diptera: Culicidae) group in Papua New Guinea. J Med Entomol 39: 1627.

    • Search Google Scholar
    • Export Citation
  • 5.

    Foley DH, Paru R, Dagoro H, Bryan JH, 1993. Allozyme analysis reveals six species within the Anopheles punctulatus complex of mosquitoes in Papua New Guinea. Med Vet Entomol 7: 3748.

    • Search Google Scholar
    • Export Citation
  • 6.

    Beebe NW, Cooper RD, 2002. Distribution and evolution of the Anopheles punctulatus group (Diptera: Culicidae) in Australia and Papua New Guinea. Int J Parasitol 32: 563574.

    • Search Google Scholar
    • Export Citation
  • 7.

    Bockarie M, Tavul L, Kastens W, Michael E, Kazura J, 2002. Impact of untreated bednets on prevalence of Wuchereria bancrofti transmitted by Anopheles farauti in Papua New Guinea. Med Vet Entomol 16: 116119.

    • Search Google Scholar
    • Export Citation
  • 8.

    Bockarie MJ, Fischer P, Williams SA, Zimmerman PA, Griffin L, Alpers MP, Kazura JW, 2000. Application of a polymerase chain reaction-ELISA to detect Wuchereria bancrofti in pools of wild-caught Anopheles punctulatus in a filariasis control area in Papua New Guinea. Am J Trop Med Hyg 62: 363367.

    • Search Google Scholar
    • Export Citation
  • 9.

    Burkot TR, Molineaux L, Graves PM, Paru R, Battistutta D, Dagoro H, Barnes A, Wirtz RA, Garner P, 1990. The prevalence of naturally acquired multiple infections of Wuchereria bancrofti and human malarias in anophelines. Parasitology 100: 369375.

    • Search Google Scholar
    • Export Citation
  • 10.

    Benet A, Mai A, Bockarie F, Lagog M, Zimmerman P, Alpers MP, Reeder JC, Bockarie MJ, 2004. Polymerase chain reaction diagnosis and the changing pattern of vector ecology and malaria transmission dynamics in Papua New Guinea. Am J Trop Med Hyg 71: 277284.

    • Search Google Scholar
    • Export Citation
  • 11.

    Cooper RD, Waterson DG, Frances SP, Beebe NW, Pluess B, Sweeney AW, 2009. Malaria vectors of Papua New Guinea. Int J Parasitol 39: 14951501.

  • 12.

    Burkot TR, Graves PM, Paru R, Wirtz RA, Heywood PF, 1988. Human malaria transmission studies in the Anopheles punctulatus complex in Papua New Guinea: sporozoite rates, inoculation rates, and sporozoite densities. Am J Trop Med Hyg 39: 135144.

    • Search Google Scholar
    • Export Citation
  • 13.

    Black RH, 1955. Malaria in the South-west Pacific. South Pacific Commission Technical Paper 81, 156.

  • 14.

    Heydon GA, 1923. Malaria at Rabaul. Med J Aust 2: 625633.

  • 15.

    Coates J, Boyd J, 1955. Malaria. Preventive Medicine in World War II: Communicable Diseases, Volume 6. Washington, DC: Office of the Surgeon General.

    • Search Google Scholar
    • Export Citation
  • 16.

    Joy RJ, 1999. Malaria in American troops in the South and Southwest Pacific in World War II. Med Hist 43: 192207.

  • 17.

    Russell PF, 1946. Lessons in malariology from World War II. Am J Trop Med Hyg 26: 513.

  • 18.

    WHO, 1957. Malaria: Sixth Report of the Expert Committee. World Health Organ Tech Rep Ser. Geneva: World Health Organization.

  • 19.

    Pampana E, 1969. A Textbook of Malaria Eradication. London: Oxford University Press.

  • 20.

    Laird M, 1946. Observations on Anopheles punctulatus Donitz 1901 and Anopheles farauti Laveran 1902 at Palmalmal and Manginuna, New Britian, during July and August 1945. Trans R Soc NZ 76: 148157.

    • Search Google Scholar
    • Export Citation
  • 21.

    Laird M, 1952. Notes on the mosquitoes of Nissan Island, Territory of New Guinea. Pac Sci 6: 151156.

  • 22.

    Mackerras I, Ratcliffe F, Gilmour D, Mules M, 1950. Dispersal of DDT from Aircraft for Mosquito Control. CSIRO Bulletin. Melbourne: Commonwealth Scientific and Industrial Research Organization, 164.

    • Search Google Scholar
    • Export Citation
  • 23.

    Bang FB, Hairston NG, Maier J, Roberts FH, 1947. DDT spraying inside houses as a means of malaria control in New Guinea. Trans R Soc Trop Med Hyg 40: 809822.

    • Search Google Scholar
    • Export Citation
  • 24.

    Metselaar D, 1956. A pilot project of residual-insecticide spraying to control malaria transmitted by the Anopheles punctulatus group in Netherlands New Guinea. Am J Trop Med Hyg 5: 977987.

    • Search Google Scholar
    • Export Citation
  • 25.

    Peters W, 1959. Malaria control in Papua and New Guinea. P N G Med J 3: 6675.

  • 26.

    Spencer M, 1965. Malaria in the d'Entrecasteaux Islands, with particular reference to Anopheles farauti Laveran. Proc Linn Soc N S W 90: 115127.

    • Search Google Scholar
    • Export Citation
  • 27.

    Spencer M, 1992. The history of malaria control in the southwest Pacific region, with particular reference to Papua New Guinea and the Solomon Islands. P N G Med J 35: 3366.

    • Search Google Scholar
    • Export Citation
  • 28.

    Avery J, 1974. A review of the malaria eradication programme in the British Solomon Islands 1970–1972. P N G Med J 17: 5060.

  • 29.

    Parkinson A, 1974. Malaria in Papua New Guinea 1973. P N G Med J 17: 816.

  • 30.

    Peters W, 1960. Studies on the epidemiology of malaria in New Guinea Part I. Holoendemic Malaria–The Clinical Picture. Trans R Soc Trop Med Hyg 54: 242249.

    • Search Google Scholar
    • Export Citation
  • 31.

    Spencer T, Spencer M, Venters D, 1974. Malaria vectors in Papua New Guinea. P N G Med J 7: 2230.

  • 32.

    Health PNGDo, 1986. Papua New Guinea National Health Plan 1986–1900. Port Moresby: Papua New Guinea Department of Health.

  • 33.

    Opeskin B, 2009. Malaria in Pacific populations: seen but not heard? J Popul Res 26: 175199.

  • 34.

    PMISG, 2010. Malaria on isolated Melanesian islands prior to the initiation of malaria elimination activities from The Pacific Malaria Initiative Survey Group on behalf of the Ministries of Health of Vanuatu and Solomon Islands. Malar J 9: 218.

    • Search Google Scholar
    • Export Citation
  • 35.

    Cattani JA, Tulloch JL, Vrbova H, Jolley D, Gibson FD, Moir JS, Heywood PF, Alpers MP, Stevenson A, Clancy R, 1986. The epidemiology of malaria in a population surrounding Madang, Papua New Guinea. Am J Trop Med Hyg 35: 315.

    • Search Google Scholar
    • Export Citation
  • 36.

    Genton B, Al-Yaman F, Beck H, Hii J, Mellor S, Narara A, Gibson N, Smith T, Alpers M, 1995. The epidemiology of malaria in the Wosera area, East Sepik Province, Papua New Guinea in preparation for vaccine trials. I: malariometric indices and immunity. Ann Trop Med Parasitol 89: 359376.

    • Search Google Scholar
    • Export Citation
  • 37.

    Muller I, Bockarie M, Alpers M, Smith T, 2003. The epidemiology of malaria in Papua New Guinea. Trends Parasitol 19: 253259.

  • 38.

    Genton B, Hii J, al-Yaman F, Paru R, Beck HP, Ginny M, Dagoro H, Lewis D, Alpers MP, 1994. The use of untreated bednets and malaria infection, morbidity and immunity. Ann Trop Med Parasitol 88: 263270.

    • Search Google Scholar
    • Export Citation
  • 39.

    Hii JL, Smith T, Vounatsou P, Alexander N, Mai A, Ibam E, Alpers MP, 2001. Area effects of bednet use in a malaria-endemic area in Papua New Guinea. Trans R Soc Trop Med Hyg 95: 713.

    • Search Google Scholar
    • Export Citation
  • 40.

    Graves PM, Brabin BJ, Charlwood JD, Burkot TR, Cattani JA, Ginny M, Paino J, Gibson FD, Alpers MP, 1987. Reduction in incidence and prevalence of Plasmodium falciparum in under-5-year-old children by permethrin impregnation of mosquito nets. Bull World Health Organ 65: 869877.

    • Search Google Scholar
    • Export Citation
  • 41.

    Genton B, Hii J, Al-Yaman F, Paru R, Beck H, Ginny M, Dagoro H, Lewis D, Alpers M, 1994. The use of untreated bednets and malaria infection, morbidity and immunity. Ann Trop Med Parasitol 88: 263270.

    • Search Google Scholar
    • Export Citation
  • 42.

    Hetzel MW, 2009. An integrated approach to malaria control in Papua New Guinea. P N G Med J 52: 17.

  • 43.

    Keven JB, Henry-Halldin CN, Thomsen EK, Mueller I, Siba PM, Zimmerman PA, Reimer LJ, 2010. Pyrethroid susceptibility in natural populations of the Anopheles punctulatus group (Diptera: Culicidae) in Papua New Guinea. Am J Trop Med Hyg 83: 12591261.

    • Search Google Scholar
    • Export Citation
  • 44.

    Vais H, Williamson M, Devonshire A, Usherwood P, 2001. The molecular interactions of pyrethroid insecticides with insect and mammalian sodium channels. Pest Manag Sci 57: 877888.

    • Search Google Scholar
    • Export Citation
  • 45.

    Williamson M, Martinez-Torres D, Hick C, Devonshire A, 1996. Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol Gen Genet 252: 5160.

    • Search Google Scholar
    • Export Citation
  • 46.

    Martinez-Torres DC, Williamson MS, Darriet F, Berge JB, Devonshire AL, Guillet P, Pasteur N, Pauron D, 1998. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol 7: 179184.

    • Search Google Scholar
    • Export Citation
  • 47.

    Soderlund DM, 2008. Pyrethroids, knockdown resistance and sodium channels. Pest Manag Sci 64: 610616.

  • 48.

    Ranson H, Jensen B, Vulule J, Wang X, Hemingway J, Collins F, 2000. Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Mol Biol 9: 491497.

    • Search Google Scholar
    • Export Citation
  • 49.

    Nwane P, Etang J, Chouaibou M, Toto JC, Kerah-Hinzoumbe C, Mimpfoundi R, Awono-Ambene HP, Simard F, 2009. Trends in DDT and pyrethroid resistance in Anopheles gambiae s.s. populations from urban and agro-industrial settings in southern Cameroon. BMC Infect Dis 9: 163.

    • Search Google Scholar
    • Export Citation
  • 50.

    Reimer L, Fondjo E, Patchok ÈS, Diallo B, Lee Y, Ng A, Ndjemai H, Atangana J, Traore S, Lanzaro G, 2008. Relationship between kdr mutation and resistance to pyrethroid and DDT insecticides in natural populations of Anopheles gambiae. J Med Entomol 45: 260266.

    • Search Google Scholar
    • Export Citation
  • 51.

    Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, Caccone A, Donnelly MJ, Petrarca V, Simard F, Pinto J, della Torre A, 2008. Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J 7: 74.

    • Search Google Scholar
    • Export Citation
  • 52.

    Singh O, Dykes C, Das M, Pradhan S, Bhatt R, Agrawal O, Adak T, 2010. Presence of two alternative kdr-like mutations, L1014F and L1014S, and a novel mutation, V1010L, in the voltage gated Na+ channel of Anopheles culicifacies from Orissa, India. Malar J 9: 146.

    • Search Google Scholar
    • Export Citation
  • 53.

    Verhaeghen K, Van Bortel W, Trung H, Sochantha T, Keokenchanh K, Coosemans M, 2010. Knockdown resistance in Anopheles vagus, An. sinensis, An. paraliae and An. peditaeniatus populations of the Mekong region. Parasit Vectors 3: 5970.

    • Search Google Scholar
    • Export Citation
  • 54.

    Singh OP, Dykes CL, Lather M, Agrawal OP, Adak T, 2011. Knockdown resistance (kdr)-like mutations in the voltage-gated sodium channel of a malaria vector Anopheles stephensi and PCR assays for their detection. Malar J 10: 59.

    • Search Google Scholar
    • Export Citation
  • 55.

    Syafruddin D, Hidayati A, Asih P, Hawley W, Sukowati S, Lobo N, 2010. Detection of 1014 F kdr mutation in four major anopheline malaria vectors in Indonesia. Malar J 9: 315.

    • Search Google Scholar
    • Export Citation
  • 56.

    Guerrero F, Jamroz R, Kammlah D, Kunz S, 1997. Toxicological and molecular characterization of pyrethroid-resistant horn flies, Haematobia irritans: identification of kdr and super-kdr point mutations. Insect Biochem Mol Biol 27: 745755.

    • Search Google Scholar
    • Export Citation
  • 57.

    Hii J, Smith T, Mai A, Ibam E, Alpers M, 2000. Comparison between anopheline mosquitoes (Diptera: Culicidae) caught using different methods in a malaria endemic area of Papua New Guinea. Bull Entomol Res 90: 211219.

    • Search Google Scholar
    • Export Citation
  • 58.

    Belkin J, 1962. The Mosquitoes of the South Pacific (Diptera: Culicidae). Berkeley, CA: University of California Press.

  • 59.

    Henry-Halldin CN, Reimer L, Thomsen EK, Koimbu G, Zimmerman AM, Keven JB, Dagoro H, Hetzel M, Mueller I, Siba P, Zimmerman P, 2011. High throughput multiplex assay for species identification of Papua New Guinea malaria vectors: members of the Anopheles punctulatus (Diptera: Culicidae) species group. Am J Trop Med Hyg 84: 166173.

    • Search Google Scholar
    • Export Citation
  • 60.

    Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, Devonshire AL, Guillet P, Pasteur N, Pauron D, 1998. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol 7: 179184.

    • Search Google Scholar
    • Export Citation
  • 61.

    Drummond AJ, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Stones-Havas S, Thierer T & Wilson A 2009. Geneious Pro v 5.0. Available at: http://www.geneious.com. Accessed March 15, 2011.

    • Search Google Scholar
    • Export Citation
  • 62.

    Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG, 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 29472948.

    • Search Google Scholar
    • Export Citation
  • 63.

    McNamara DT, Kasehagen LJ, Grimberg BT, Cole-Tobian J, Collins WE, Zimmerman PA, 2006. Diagnosing infection levels of four human malaria parasite species by a polymerase chain reaction/ligase detection reaction fluorescent microsphere-based assay. Am J Trop Med Hyg 74: 413421.

    • Search Google Scholar
    • Export Citation
  • 64.

    Beebe NW, Cooper RD, Foley DH, Ellis JT, 2000. Populations of the south-west Pacific malaria vector Anopheles farauti s.s. revealed by ribosomal DNA transcribed spacer polymorphisms. Heredity 84: 244253.

    • Search Google Scholar
    • Export Citation
  • 65.

    Beebe NW, Cooper RD, Morrison DA, Ellis JT, 2000. A phylogenetic study of the Anopheles punctulatus group of malaria vectors comparing rDNA sequence alignments derived from the mitochondrial and nuclear small ribosomal subunits. Mol Phylogenet Evol 17: 430436.

    • Search Google Scholar
    • Export Citation
  • 66.

    Beebe NW, Ellis JT, Cooper RD, Saul A, 1999. DNA sequence analysis of the ribosomal DNA ITS2 region for the Anopheles punctulatus group of mosquitoes. Insect Mol Biol 8: 381390.

    • Search Google Scholar
    • Export Citation
  • 67.

    Bower JE, Cooper RD, Beebe NW, 2009. Internal repetition and intraindividual variation in the rDNA ITS1 of the Anopheles punctulatus group (Diptera: Culicidae): multiple units and rates of turnover. J Mol Evol 68: 6679.

    • Search Google Scholar
    • Export Citation
  • 68.

    Hasan AU, Suguri S, Fujimoto C, Itaki RL, Harada M, Kawabata M, Bugoro H, Albino B, Tsukahara T, Hombhanje F, Masta A, 2008. Phylogeography and dispersion pattern of Anopheles farauti senso stricto mosquitoes in Melanesia. Mol Phylogenet Evol 46: 792800.

    • Search Google Scholar
    • Export Citation
  • 69.

    Davies TG, Field LM, Usherwood PN, Williamson MS, 2007. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 59: 151162.

  • 70.

    Keohavong P, Thilly W, 1989. Fidelity of DNA polymerases in DNA amplification. Proc Natl Acad Sci USA 86: 92539257.

  • 71.

    Lundberg K, Shoemaker D, Adams M, Short J, Sorge J, Mathur E, 1991. High-fidelity amplification using a thermostable DNA polymerase isolated from Pyrococcus furiosus. Gene 108: 16.

    • Search Google Scholar
    • Export Citation
  • 72.

    McDonald JH, Kreitman M, 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652654.

  • 73.

    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 27312739.

    • Search Google Scholar
    • Export Citation
  • 74.

    Diabate A, Baldet T, Chandre F, Dabire KR, Simard F, Ouedraogo JB, Guillet P, Hougard JM, 2004. First report of a kdr mutation in Anopheles arabiensis from Burkina Faso, West Africa. J Am Mosq Control Assoc 20: 195196.

    • Search Google Scholar
    • Export Citation
  • 75.

    Enayati AA, Vatandoost H, Ladonni H, Townson H, Hemingway J, 2003. Molecular evidence for a kdr-like pyrethroid resistance mechanism in the malaria vector mosquito Anopheles stephensi. Med Vet Entomol 17: 138144.

    • Search Google Scholar
    • Export Citation
  • 76.

    Luleyap HU, Alptekin D, Kasap H, Kasap M, 2002. Detection of knockdown resistance mutations in Anopheles sacharovi (Diptera: Culicidae) and genetic distance with Anopheles gambiae (Diptera: Culicidae) using cDNA sequencing of the voltage-gated sodium channel gene. J Med Entomol 39: 870874.

    • Search Google Scholar
    • Export Citation
  • 77.

    Pinto J, Lynd A, Elissa N, Donnelly MJ, Costa C, Gentile G, Caccone A, do Rosario VE, 2006. Co-occurrence of East and West African kdr mutations suggests high levels of resistance to pyrethroid insecticides in Anopheles gambiae from Libreville, Gabon. Med Vet Entomol 20: 2732.

    • Search Google Scholar
    • Export Citation
  • 78.

    Verhaeghen K, Van Bortel W, Roelants P, Backeljau T, Coosemans M, 2006. Detection of the East and West African kdr mutation in Anopheles gambiae and Anopheles arabiensis from Uganda using a new assay based on FRET/Melt Curve analysis. Malar J 5: 16.

    • Search Google Scholar
    • Export Citation
  • 79.

    Etang J, Fondjo E, Chandre F, Morlais I, Brengues C, Nwane P, Chouaibou M, Ndjemai H, Simard F, 2006. First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon. Am J Trop Med Hyg 74: 795797.

    • Search Google Scholar
    • Export Citation
  • 80.

    Martinez-Torres D, Chevillon C, Brun-Barale A, Bergé JB, Pasteur N, Pauron D, 1999. Voltage-dependent Na+ channels in pyrethroid-resistant Culex pipiens L. mosquitoes. Pestic Sci 55: 10121020.

    • Search Google Scholar
    • Export Citation
  • 81.

    Xu Q, Liu H, Zhang L, Liu N, 2005. Resistance in the mosquito, Culex quinquefasciatus, and possible mechanisms for resistance. Pest Manag Sci 61: 10961102.

    • Search Google Scholar
    • Export Citation
  • 82.

    Williamson M, Martinez-Torres D, Hick C, Devonshire A, 1996. Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol Gen Genet 252: 5160.

    • Search Google Scholar
    • Export Citation
  • 83.

    Miyazaki M, Ohyama K, Dunlap DY, Matsumura F, 1996. Cloning and sequencing of the para-type sodium channel gene from susceptible and kdr-resistant German cockroaches (Blattella germanica) and house fly (Musca domestica). Mol Gen Genet 252: 6168.

    • Search Google Scholar
    • Export Citation
  • 84.

    Pridgeon JW, Appel AG, Moar WJ, Liu N, 2002. Variability of resistance mechanisms in pyrethroid resistant German cockroaches (Dictyoptera: Blattellidae). Pestic Biochem Physiol 73: 149156.

    • Search Google Scholar
    • Export Citation
  • 85.

    Saitou N, Nei M, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406425.

  • 86.

    Felsenstein J, 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783791.

  • 87.

    Kelly GC, Hii J, Batarii W, Donald W, Hale E, Nausien J, Pontifex S, Vallely A, Tanner M, Clements A, 2010. Modern geographical reconnaissance of target populations in malaria elimination zones. Malar J 9: 289.

    • Search Google Scholar
    • Export Citation
  • 88.

    Hemingway J, Ranson H, 2000. Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45: 371391.

  • 89.

    Lawniczak M, Emrich S, Holloway A, Regier A, Olson M, White B, Redmond S, Fulton L, Appelbaum E, Godfrey J, 2010. Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330: 512.

    • Search Google Scholar
    • Export Citation
  • 90.

    Neafsey D, Lawniczak M, Park D, Redmond S, Coulibaly M, Traore S, Sagnon N, Costantini C, Johnson C, Wiegand R, 2010. SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science 330: 514.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 50 50 8
Full Text Views 291 92 0
PDF Downloads 53 13 0
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save