Genetic structure of Anopheles gambiae populations on islands in northwestern Lake Victoria, Uganda

Malaria Journal

Volumn 4, Issue , 2005, Pages

  Kayondo, Jonathan K ^a,b   Mukwaya, Louis G ^b   Stump, Aram ^a   Michel, Andrew P ^a   Coulibaly, Mamadou B ^a   Besansky, Nora J ^a   Collins, Frank H ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b UGANDA VIRUS RESEARCH INSTITUTE   (Uganda)

Author keywords

[No Author keywords available]

Indexed keywords

ANOPHELES GAMBIAE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; GENE FLOW; GENE LOCUS; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOME; GENOTYPE; GEOGRAPHY; HUMAN; MAJOR CLINICAL STUDY; MALARIA; MOSQUITO; POPULATION; SAMPLE; UGANDA; ANIMAL; CHROMOSOME INVERSION; CLASSIFICATION; DISEASE CARRIER; GENETIC POLYMORPHISM; GENETICS; METHODOLOGY; POLYMERASE CHAIN REACTION; POPULATION DENSITY; STATISTICAL MODEL; TIME;

MICROSATELLITE DNA;

ANIMALS; ANOPHELES GAMBIAE; CHROMOSOME INVERSION; GENE FLOW; GENETIC VARIATION; GENOTYPE; GEOGRAPHY; INSECT VECTORS; LINEAR MODELS; MICROSATELLITE REPEATS; POLYMERASE CHAIN REACTION; POLYMORPHISM, GENETIC; POPULATION DENSITY; TIME FACTORS; UGANDA;

EID: 30944467512     PISSN: 14752875     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-4-59     Document Type: Article

References (66)

1. Marshall E: Malaria. A renewed assault on an old and deadly foe. Science 2000, 290:428-430.
2. Wellems TE: Plasmodium chloroquine resistance and the search for a replacement antimalarial drug. Science 2002, 298:124-126.
3. Hemingway J, Field L, Vontas J: An overview of insecticide resistance. Science 2002, 298:96-97.
4. Weill M, Malcolm C, Chandre F, Mogensen K, Berthomieu A, Marquine M, Raymond M: The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Mol Biol 2004, 13:1-7.
5. James AA: Mosquito molecular genetics: the hands that feed bite back. Science 1992, 257:37-38.
6. James AA: Blocking malaria parasite invasion of mosquito salivary glands. J Exp Biol 2003, 206:3817-3821.
7. Collins FH, Besansky NJ: Vector biology and the control of malaria in Africa. Science 1994, 264:1874-1875.
8. Crampton JM, Warren A, Lycett GJ, Hughes MA, Comley IP, Eggleston P: Genetic manipulation of insect vectors as a strategy for the control of vector-borne disease. Ann Trop Med Parasitol 1994, 88:3-12.
9. 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, Collins FH: Malaria control with genetically manipulated insect vectors. Science 2002, 298:119-121.
10. Nirmala X, James AA: Engineering Plasmodium-refractory phenotypes in mosquitoes. Trends Parasitol 2003, 19:384-387.
11. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R, Salzberg SL, Loftus B, Yandell M, Majoros WH, Rusch DB, Lai Z, Kraft CL, Abril JF, Anthouard V, Arensburger P, Atkinson PW, Baden H, de Berardinis V, Baldwin D, Benes V, Biedler J, Blass C, Bolanos R, Boscus D, Barnstead M, Cai S, Center A, Chaturverdi K, Christophides GK, Chrystal MA, Clamp M, Cravchik A, Curwen V, Dana A, Delcher A, Dew I, Evans CA, Flanigan M, Grundschober-Freimoser A, Friedli L, Gu Z, Guan P, Guigo R, Hillenmeyer ME, Hladun SL, Hogan JR, Hong YS, Hoover J, Jaillon O, Ke Z, Kodira C, Kokoza E, Koutsos A, Letunic I, Levitsky A, Liang Y, Lin JJ, Lobo NF, Lopez JR, Malek JA, McIntosh TC, Meister S, Miller J, Mobarry C, Mongin E, Murphy SD, O'Brochta DA, Pfannkoch C, Qi R, Regier MA, Remington K, Shao H, Sharakhova MV, Sitter CD, Shetty J, Smith TJ, Strong R, Sun J, Thomasova D, Ton LQ, Topalis P, Tu Z, Unger MF, Walenz B, Wang A, Wang J, Wang M, Wang X, Woodford KJ, Wortman JR, Wu M, Yao A, Zdobnov EM, Zhang H, Zhao Q, Zhao S, Zhu SC, Zhimulev I, Coluzzi M, della Torre A, Roth CW, Louis C, Kalush F, Mural RJ, Myers EW, Adams MD, Smith HO, Broder S, Gardner MJ, Fraser CM, Birney E, Bork P, Brey PT, Venter JC, Weissenbach J, Kafatos FC, Collins FH, Hoffman SL: The genome sequence of the malaria mosquito Anopheles gambiae. Science 2002, 298:129-149.
12. Mongin E, Louis C, Holt RA, Birney E, Collins FH: The Anopheles gambiae genome: an update. Trends Parasitol 2004, 20:49-52.
13. Hill CA, Kafatos FC, Stansfield SK, Collins FH: Arthropod-borne diseases: vector control in the genomics era. Nat Rev Microbiol 2005, 3:262-268.
14. Collins FH, Zheng L, Paskewitz SM, Kafatos FC: Progress in the map-based cloning of the Anopheles gambiae genes responsible for the encapsulation of malarial parasites. Ann Trop Med Parasitol 1997, 91:517-521.
15. Zheng L, Cornel AJ, Wang R, Erfle H, Voss H, Ansorge W, Kafatos FC, Collins FH: Quantitative trait loci for refractoriness of Anopheles gambiae to Plasmodium cynomolgi B. Science 1997, 276:425-428.
16. Collins FH, Saunders RD, Kafatos FC, Roth C, Ke Z, Wang X, Dymbrowski K, Ton L, Hogan J: Genetics in the study of mosquito susceptibility to Plasmodium. Parassitologia 1999, 41:163-168.
17. de Lara Capurro M, Coleman J, Beerntsen BT, Myles KM, Olson KE, Rocha E, Krettli AU, James AA: Virus-expressed, recombinant single-chain antibody blocks sporozoite infection of salivary glands in Plasmodium gallinaceum-infected Aedes aegypti. Am J Trop Med Hyg 2000, 62:427-433.
18. Ito J, Ghosh A, Moreira LA, Wimmer EA, Jacobs-Lorena M: Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 2002, 417:452-455.
19. Catteruccia F, Nolan T, Loukeris TG, Blass C, Savakis C, Kafatos FC, Crisanti A: Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 2000, 405:959-962.
20. Collins FH, Kamau L, Ranson HA, Vulule JM: Molecular entomology and prospects for malaria control. Bull World Health Organ 2000, 78:1412-1423.
21. Lehmann T, Hawley WA, Kamau L, Fontenille D, Simard F, Collins FH: Genetic differentiation of Anopheles gambiae populations from East and west Africa: comparison of microsatellite and allozyme loci. Heredity 1996, 77:192-200.
22. Besansky NJ, Lehmann T, Fahey GT, Fontenille D, Braack LE, Hawley WA, Collins FH: Patterns of mitochondrial variation within and between African malaria vectors, Anopheles gambiae and An. arabiensis, suggest extensive gene flow. Genetics 1997, 147:1817-1828.
23. Toure YT, Petrarca V, Traore SF, Coulibaly A, Maiga HM, Sankare O, Sow M, Di Deco MA, Coluzzi M: The distribution and inversion polymorphism of chromosomally recognized taxa of the Anopheles gambiae complex in Mali, West Africa. Parassitologia 1998, 40:477-511.
24. Gentile G, Slotman M, Ketmaier V, Powell JR, Caccone A: Attempts to molecularly distinguish cryptic taxa in Anopheles gambiae s.s. Insect Mol Biol 2001, 10:25-32.
25. Mukabayire O, Caridi J, Wang X, Toure YT, Coluzzi M, Besansky NJ: Patterns of DNA sequence variation in chromosomally recognized taxa of Anopheles gambiae: evidence from rDNA and single-copy loci. Insect Mol Biol 2001, 10:33-46.
26. Favia G, Lanfrancotti A, Spanos L, Siden-Kiamos I, Louis C: Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s. Insect Mol Biol 2001, 10:19-23.
27. Lehmann T, Hawley WA, Grebert H, Danga M, Atieli F, Collins FH: The Rift Valley complex as a barrier to gene flow for Anopheles gambiae in Kenya. J Hered 1999, 90:613-621.
28. Pinto J, Donnelly MJ, Sousa CA, Malta-Vacas J, Gil V, Ferreira C, Petrarca V, do Rosario VE, Charlwood JD: An island within an island: genetic differentiation of Anopheles gambiae in Sao Tome, West Africa, and its relevance to malaria vector control. Heredity 2003, 91:407-414.
29. Simard F, Fontenille D, Lehmann T, Girod R, Brutus L, Gopaul R, Dournon C, Collins FH: High amounts of genetic differentiation between populations of the malaria vector Anopheles arabiensis from West Africa and eastern outer islands. Am J Trop Med Hyg 1999, 60:1000-1009.
30. Donnelly MJ, Licht MC, Lehmann T: Evidence for recent population expansion in the evolutionary history of the malaria vectors Anopheles arabiensis and Anopheles gambiae. Mol Biol Evol 2001, 18:1353-1364.
31. Tripet F, Toure YT, Taylor CE, Norris DE, Dolo G, Lanzaro GC: DNA analysis of transferred sperm reveals significant levels of gene flow between molecular forms of Anopheles gambiae. Mol Ecol 2001, 10:1725-1732.
32. Tripet F, Toure YT, Dolo G, Lanzaro GC: Frequency of multiple inseminations in field-collected Anopheles gambiae females revealed by DNA analysis of transferred sperm. Am J Trop Med Hyg 2003, 68:1-5.
33. Chen H, Minakawa N, Beier J, Yan G: Population genetic structure of Anopheles gambiae mosquitoes on Lake Victoria islands, west Kenya. Malar J 2004, 3:48 [http://www.malariajour nal.com/content/3/1/48].
34. Gillies MT, De Meillon B: The Anophelinae of Africa south of the Sahara 2nd edition. Johannesburg: Publications of the South African Institute for Medical Research No 54; 1968.
35. Mukwaya LG, Kayondo JK, Crabtree MB, Savage HM, Biggerstaff BJ, Miller BR: 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 2000, 9:85-91.
36. Scott JA, Brogdon WG, Collins FH: Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 1993, 49:520-529.
37. Wang R, Kafatos FC, Zheng L: Microsatellite markers and genotyping procedures for Anopheles gambiae. Parasitol Today 1999, 15:33-37.
38. Zheng L, Benedict MQ, Cornel AJ, Collins FH, Kafatos FC: An integrated genetic map of the African human malaria vector mosquito, Anopheles gambiae. Genetics 1996, 143:941-952.
39. Raymond M, Rousset F: GENEPOP (Version 1.2): Population genetics software for exact tests and ecumenism. J Heredity 1995, 86:248-249.
40. Schneider S, Roessli D, Excoffier L: ARLEQUIN, Version 2.000: A software for population genetics data analysis Produced by the Genetics and Biometry Laboratory, University of Geneva, Switzerland; 2000.
41. Dieringer D, Schlotterer C: Microsatellite analyzer (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 2003, 3:167-169.
42. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P: MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 2004, 4:535-538.
43. Wang J, Whitlock MC: Estimating effective population size and migration rates from genetic samples over space and time. Genetics 2003, 163:429-446.
44. Waples RS: A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 1989, 121:379-391.
45. Lehmann T, Hawley WA, Grebert H, Collins FH: The effective population size of Anopheles gambiae in Kenya: implications for population structure. Mol Biol Evol 1998, 15:264-276.
46. Nei M, Tajima F: Genetic drift and estimation of effective population size. Genetics 1981, 98:625-640.
47. Tajima F, Nei M: Note on genetic drift and estimation of effective population size. Genetics 1984, 106:569-574.
48. Slatkin M: A measure of population subdivision based on microsatellite allele frequencies. Genetics 1995, 139:457-462.
49. Hartl DL, Clark AG: Principles of Population Genetics Sunderland, MA: Sinauer Associates, Inc; 1997.
50. Colluzi M, Sabatini A, Petrarca V, Di Deco MA: Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans R Soc Trop Med Hyg 1979, 73:483-497.
51. Petrarca V, Beier JC: Intraspecific chromosomal polymorphism in the Anopheles gambiae complex as a factor affecting malaria transmission in the Kisumu area of Kenya. Am J Trop Med Hyg 1992, 46:229-237.
52. Mnzava AE, Rwegoshora RT, Wilkes TJ, Tanner M, Curtis CF: Anopheles arabiensis and An. gambiae chromosomal inversion polymorphism, feeding and resting behaviour in relation to insecticide house-spraying in Tanzania. Med Vet Entomol 1995, 9:316-324.
53. Smits A, Roelants P, Van Bortel W, Coosemans M: Enzyme polymorphisms in the Anopheles gambiae (Diptera:Culicidae) complex related to feeding and resting behavior in the Imbo Valley, Burundi. J Med Entomol 1996, 33:545-553.
54. Garcia De Leon FJ, Chikhi L, Bonhomme F: Microsatellite polymorphism and population subdivision in natural populations of European Sea Bass (Dicentrarchus labrax Linnaeus, 1758). Mol Ecol 1997, 6:51-62.
55. Callen DF, Thompson AD, Shen Y, Phillips HA, Richards RI, Mulley JC, Sutherland GR: Incidence and origin of "null" alleles in the (AC)n microsatellite markers. Am J Hum Genet 1993, 52:922-927.
56. Paetkau D, Strobeck C: The molecular basis and evolutionary history of a microsatellite null allele in bears. Mol Ecol 1995, 4:519-520.
57. Donnelly MJ, Cuamba N, Charlwood JD, Collins FH, Townson H: Population structure in the malaria vector, Anopheles arabiensis Patton, in East Africa. Heredity 1999, 83:408-417.
58. Lehmann T, Licht M, Gimnig JE, Hightower A, Vulule JM, Hawley WA: Spatial and temporal variation in kinship among Anopheles gambiae (Diptera: Culicidae) mosquitoes. J Med Entomol 2003, 40:421-429.
59. Coluzzi M, Sabatini A, Petrarca V, DiDeco MA: Chromosomal differentiation and adpatation to human environments in the Anopheles gambiae complex. Trans R Soc Trop Med Hyg 1979, 73:483-497.
60. Coluzzi M, Petrarca V, Di Deco MA: Chromosomal inversion intergradation and incipient speciation in Anopheles gambiae. Boll Zool 1985, 52:45-63.
61. Coluzzi M, Sabatini A, Petrarca V, Di Deco MA: Behavioural divergences between mosquitoes with different inversion karyotypes in polymorphic populations of the Anopheles gambiae complex. Nature 1977, 266:832-833.
62. Costantini C, Li SG, Della Torre A, Sagnon N, Coluzzi M, Taylor CE: Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a west African Sudan savanna village. Med Vet Entomol 1996, 10:203-219.
63. Whitlock MC, McCauley DE: Indirect measures of gene flow and migration: FST not equal to 1/(4Nm + 1). Heredity 1999, 82:117-125.
64. Kamau L, Lehmann T, Hawley WA, Orago AS, Collins FH: Microgeographic genetic differentiation of Anopheles gambiae mosquitoes from Asembo Bay, western Kenya: a comparison with Kilifi in coastal Kenya. Am J Trop Med Hyg 1998, 58:64-69.
65. Lehmann T, Besansky NJ, Hawley WA, Fahey TG, Kamau L, Collins FH: Microgeographic structure of Anopheles gambiae in western Kenya based on mtDNA and microsatellite loci. Mol Ecol 1997, 6:243-253.
66. Lehmann T, Licht M, Elissa N, Maega BT, Chimumbwa JM, Watsenga FT, Wondji CS, Simard F, Hawley WA: Population structure of Anopheles gambiae in Africa. J Hered 2003, 94:133-147.