Molecular Differentiation of the African Yellow Fever Vector Aedes bromeliae (Diptera: Culicidae) from Its Sympatric Non-vector Sister Species, Aedes lilii

PLoS Neglected Tropical Diseases

Volumn 9, Issue 12, 2015, Pages

  Bennett, Kelly Louise ^a   Linton, Yvonne Marie ^b,c,d,e   Shija, Fortunate ^a,f   Kaddumukasa, Martha ^g   Djouaka, Rousseau ^h   Misinzo, Gerald ^f   Lutwama, Julius ^g   Huang, Yiau Min ^b,e   Mitchell, Luke B ^b,e   Richards, Miriam ^f   Tossou, Eric ^h   Walton, Catherine ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b SMITHSONIAN INSTITUTION   (United States)

^c WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^d UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^e DEPARTMENT OF PALEOBIOLOGY   (United States)

^f SOKOINE UNIVERSITY OF AGRICULTURE   (Tanzania)

^g Emerging and Re emerging Infections Virus Research Institute   (Uganda)

^h Plant Health Management Division   (Benin)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; CYTOCHROME P450; INTERNAL TRANSCRIBED SPACER; INSECT PROTEIN; RIBOSOMAL SPACER DNA;

ADULT; AEDES; AEDES BROMELIAE; AEDES LILII; ARTICLE; GENETIC VARIABILITY; MOLECULAR GENETICS; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; YELLOW FEVER; ANIMAL; BENIN; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; ECOSYSTEM; EVALUATION STUDY; GENETICS; HUMAN; INSECT VECTOR; PHYLOGEOGRAPHY; PROCEDURES; TANZANIA; TRANSMISSION; UGANDA; ZOOLOGY;

AEDES; ANIMALS; BENIN; CLUSTER ANALYSIS; DNA, RIBOSOMAL SPACER; ECOSYSTEM; ENTOMOLOGY; HUMANS; INSECT PROTEINS; INSECT VECTORS; MOLECULAR SEQUENCE DATA; PHYLOGEOGRAPHY; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; TANZANIA; UGANDA; YELLOW FEVER;

EID: 84953238960     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004250     Document Type: Article

References (72)

1. Mutebi JP, Crabtree MB, Kading RC, Powers AM, Lutwama JJ, Miller BR, Mosquitoes of Western Uganda. J Med Entomol. 2012;49(6):1289–306. 23270157
2. Gubler DJ, Resurgent vector-borne diseases as a global health problem. Emerg Infect Dis. 1998 Jul-Sep;4(3):442–50. 9716967
3. Tomori O, Yellow fever in Africa: Public health impact and prospects for control in the 21st century. Biomedica. 2002;22(2):178–210. 12152484
4. Garske T, Van Kerkhove MD, Yactayo S, Ronveaux O, Lewis RF, Staples JE, et al. Yellow fever in Africa: Estimating the burden of disease and impact of mass vaccination from outbreak and serological data. PLoS Med. 2014;11(5):e1001638. doi: 10.1371/journal.pmed.1001638 24800812
5. WHO. Global alert and response: The West African situation. http://www.who.int/csr/disease/yellowfev/westafrica/en/ 2015.
6. Roberts L, Resurgence of yellow fever in Africa prompts a counterattack. Science. 2007;316(5828):1109–. 17525307
7. Ellis BR, Barrett ADT, The enigma of yellow fever in East Africa. Rev Med Virol. 2008;18(5):331–46. doi: 10.1002/rmv.584 18615782
8. Onyango CO, Grobbelaar AA, Gibson GVF, Sang RC, Sow A, Swanepoel R, et al. Yellow fever outbreak, Southern Sudan, 2003. Emerg Infect Dis. 2004;10(9):1668–70. 15498174
9. Gould LH, Osman MS, Farnon EC, Griffith KS, Godsey MS, Karch S, et al. An outbreak of yellow fever with concurrent chikungunya virus transmission in South Kordofan, Sudan, 2005. Trans R Soc Trop Med Hyg. 2008;102(12):1247–54. doi: 10.1016/j.trstmh.2008.04.014 18502458
10. Wamala JF, Malimbo M, Okot CL, Atai-Omoruto AD, Tenywa E, Miller JR, et al. Epidemiological and laboratory characterization of a yellow fever outbreak in northern Uganda, October 2010–January 2011. Int J Infect Dis. 2012;16(7):e536–e42. doi: 10.1016/j.ijid.2012.03.004 22575876
11. Barrett ADT, Higgs S, Yellow fever: A disease that has yet to be conquered. Annu Rev Entomol. 2006;52(1):209–29.
12. Theobald FV, A new Stegomyia from transvaal. Entomologist. 1905 (38):101–4.
13. Theobald FV, A monograph of the Culicidae or mosquitoes. British Museum of Natural History, London; 1910.
14. Theobald FV. Uganda Culicidae including thirteen new species. In Novae Culicidae, Part 1. Wye, Kent; 1915.
15. Haddow AJ, A note on the occurrence of Aedes (Stegomyia) simpsoni Theobald in the canopy of rain-forest in Bwamba County, Uganda. Ann Trop Med Parasitol. 1950 Oct;44(3):238–41. 24538825
16. Haddow AJ, The natural history of yellow fever in Africa. Proceedings of the Royal Society of Edinburgh Section B: Biological Sciences. 1969;70(03):191–227.
17. Gillett JD, The habits of the mosquito Aedes (Stegomyia) simpsoni (Theobald) in relation to the epidemiology of yellow fever in Uganda. Ann Trop Med Parasitol. 1951;45(2):110–21. 14878392
18. Gillett JD, Further studies on the biting behaviour of Aedes (Stegomyia) simpsoni Theobald in Uganda. Ann Trop Med Parasitol. 1955;49(2).
19. Mukwaya LG. Host preference in Aedes (Stegomyia) species mosquitoes with special preference to the anthropophilic forms of Ae. (Stegomyia) simpsoni Theo. (Diptera: Culicidae) in Uganda: PhD thesis. University of East Africa; 1971.
20. Mukwaya LG, Genetic control of feeding preferences in the mosquitoes Aedes (Stegomyia) simpsoni and aegypti. Physiol Entomol. 1977;2(2):133–45.
21. Mahaffy AF, Smithburn KC, Jacobs HR, Gillett JD, Yellow fever in Western Uganda. Trans R Soc Trop Med Hyg. 1942;36(1):9–20.
22. Huang Y-M, Aedes (Stegomyia) simpsoni complex in the Ethiopian region with lectotype designation for simpsoni (Theobald) (Diptera: Culicidae). Mosq Syst. 1979;11(3):221–34.
23. Huang YM, Aedes (Stegomyia) bromeliae (Diptera: Culicidae), the yellow fever virus vector in East Africa. J Med Entomol. 1986;23(2):196–200. 3701804
24. Jupp PG, Kemp A, Variation in tarsal claw morphology and the identification of Aedes (Stegomyia) demeilloni/segermanae and Aedes (Stegomyia) simpsoni/bromeliae (Diptera: Culicidae) in South Africa. J Am Mosq Control Assoc. 1999;15(1):86–8. 10342277
25. Lutwama JJM, Louis Godfrey, Variation in morphological characters of adults of the Aedes (Stegomyia) simpsoni complex from Uganda, Kenya and South Africa (Dipteria: Culicidae). Mosq Syst. 1994;26(3):145–57.
26. Huang Y-M, The subgenus Stegomyia of Aedes in the Afrotropical region with keys to the species (Diptera: Culicidae). Zootaxa. 2004;700:1–120.
27. Mukwaya LG, Kayondo J. K., Crabtree M. B., Savage H. M., Biggerstaff B. J., Miller B. R., 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(1):85–91. 10672075
28. Walter KS, Brown J. E., Powell J. R., Microhabitat partitioning of Aedes simpsoni (Diptera: Culicidae). J Med Entomol. 2014;51(3):596–604. 24897852
29. Hebert PDN, Cywinska A, Ball SL, deWaard JR, Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B: Biological Sciences. 2003;270(1512):313–21.
30. Hebert PDN, Ratnasingham S, de Waard JR, Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London B: Biological Sciences. 2003;270(Suppl 1):S96–S9.
31. Linton Y-M, Pecor JE, Porter CH, Mitchell LB, Garzón-Moreno A, Foley DH, et al. Mosquitoes of eastern Amazonian Ecuador: Biodiversity, bionomics and barcodes. Mem Inst Oswaldo Cruz. 2013;108(Suppl 1):100–9. doi: 10.1590/0074-0276130440 24473809
32. Funk DJ, Omland KE, Species-level paraphyly: Frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics. 2003;34(1):397–423.
33. Walton C, Sharpe RG, Pritchard SJ, Thelwell NJ, Butlin RK, Molecular identification of mosquito species. Biol J Linn Soc. 1999;68(1–2):241–56.
34. Huelsenbeck JP, Bull JJ, Cunningham CW, Combining data in phylogenetic analysis. Trends Ecol Evol. 1996;11(4):152–8. 21237790
35. Collins FH, Paskewitz SM, A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Mol Biol. 1996;5(1):1–9. 8630529
36. Arnheim N, Krystal M, Schmickel R, Wilson G, Ryder O, Zimmer E, Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proceedings of the National Academy of Sciences. 1980;77(12):7323–7.
37. Liao D, Concerted evolution: Molecular mechanism and biological implications. Am J Hum Genet. 1999;64(1):24–30. 9915939
38. Yao H, Song J, Liu C, Luo K, Han J, Li Y, et al. Use of ITS2 region as the universal DNA barcode for plants and animals. PLoS ONE. 2010;5(10):e13102. doi: 10.1371/journal.pone.0013102 20957043
39. Kress WJ, Wurdack KJ, Zimmer EA, Weigt LA, Janzen DH, Use of DNA barcodes to identify flowering plants. Proc Natl Acad Sci U S A. 2005;102(23):8369–74. 15928076
40. Walton C, Somboon P, O’Loughlin SM, Zhang S, Harbach RE, Linton YM, et al. Genetic diversity and molecular identification of mosquito species in the Anopheles maculatus group using the ITS2 region of rDNA. Infect, Genet Evol. 2007;7(1):93–102.
41. Prakash A, Walton C, Bhattacharyya DR, Loughlin SO, Mohapatra PK, Mahanta J, Molecular characterization and species identification of the Anopheles dirus and An. minimus complexes in north-east India using r-DNA ITS-2. Acta Trop. 2006;100(1–2):156–61. 17118324
42. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proceedings of the National Academy of Sciences. 2012;109(16):6241–6.
43. Le Goff G, Brengues C, Robert V, Stegomyia mosquitoes in Mayotte, taxonomic study and description of Stegomyia pia n. sp. Parasite. 2013;20:31. doi: 10.1051/parasite/2013030 24025625
44. Surendran S, Sarma D, Jude P, Kemppainen P, Kanthakumaran N, Gajapathy K, et al. Molecular characterization and identification of members of the Anopheles subpictus complex in Sri Lanka. Malar J. 2013;12(1):304.
45. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R, DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3(5):294–9. 7881515
46. Crabtree MB, Savage HM, Miller BR, 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. 1995;53(1):105–9. 7625528
47. Brown JE, Evans BR, Zheng W, Obas V, Barrera-Martinez L, Egizi A, et al. Human impacts have shaped historical and recent evolution in Aedes aegypti, the dengue and yellow fever mosquito. Evolution. 2014;68(2):514–25. doi: 10.1111/evo.12281 24111703
48. Messing J, New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. 6310323
49. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28(12):1647–9. doi: 10.1093/bioinformatics/bts199 22543367
50. Flot JF, Seqphase: A web tool for interconverting phase input/output files and fasta sequence alignments. Molecular Ecology Resources. 2010;10(1):162–6. doi: 10.1111/j.1755-0998.2009.02732.x 21565002
51. Stephens M, Smith NJ, Donnelly P, A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 2001;68(4):978–89. 11254454
52. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9. doi: 10.1093/molbev/mst197 24132122
53. Darriba D, Taboada GL, Doallo R, Posada D, jModelTest 2: More models, new heuristics and parallel computing. Nat Methods. 2012;9(8):772. doi: 10.1038/nmeth.2109 22847109
54. Guindon S, Gascuel O, A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52(5):696–704. 14530136
55. Excoffier L, Lischer HE, Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources. 2010;10(3):564–7. doi: 10.1111/j.1755-0998.2010.02847.x 21565059
56. Maddison WP, Gene trees in species trees. Syst Biol. 1997;46(3):523–36.
57. Hlaing T, Tun-Lin W, Somboon P, Socheat D, Setha T, Min S, et al. Mitochondrial pseudogenes in the nuclear genome of Aedes aegypti mosquitoes: Implications for past and future population genetic studies. BMC Genetics. 2009;10:11. doi: 10.1186/1471-2156-10-11 19267896
58. Lyimo IN, Ferguson HM, Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends Parasitol. 2009;25(4):189–96. doi: 10.1016/j.pt.2009.01.005 19269900
59. Mutebi J-P, Barrett ADT, The epidemiology of yellow fever in Africa. Microb Infect. 2002;4(14):1459–68.
60. Ellis BR, Sang RC, Horne KM, Higgs S, Wesson DM, Yellow fever virus susceptibility of two mosquito vectors from Kenya, East Africa. Trans R Soc Trop Med Hyg. 2012;106(6):387–9. doi: 10.1016/j.trstmh.2012.02.007 22521217
61. Sérié C, Andral L, Poirier A, Lindrec A, Neri P, Etudes sur la fièvre jaune en Ethiopie. 6. Etude épidémiologique. Bull W H O. 1968;38(6):879–84. 5303663
62. Germain M, Monath P, Bryan J, Salaun JJ, Renaudet J, Yellow fever virus in the Gambia, 1978–1979: Entomological aspects and epidemiological correlations. Am J Trop Med Hyg. 1980;29(5):929–40. 7435794
63. Lee VH, Moore DL, Vectors of the 1969 yellow fever epidemic on the Jos Plateau, Nigeria. Bull W H O. 1972;46(5):669–73. 4403105
64. Port GR, Wilkes TJ, Aedes (Diceromyia) furcifer/taylori and a yellow fever outbreak in the Gambia. Trans R Soc Trop Med Hyg. 1979;73(3):341–4. 473332
65. Germain M, Cornet M, Mouchet J, Monath TP, Hervé J-P, Salaün JJ, et al. Recent advances in research regarding sylvatic yellow fever in West and Central Africa. Bulletin de L'Institut Pasteur. 1982;80(4):315–30.
66. Weaver SC, Reisen WK, Present and future arboviral threats. Antiviral Res. 2010;85(2):328–45. doi: 10.1016/j.antiviral.2009.10.008 19857523
67. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, et al. Infection with Chikungunya virus in Italy: An outbreak in a temperate region. The Lancet. 2007;370(9602):1840–6.
68. Thiboutot MM, Kannan S, Kawalekar OU, Shedlock DJ, Khan AS, Sarangan G, et al. Chikungunya: A potentially emerging epidemic? PLoS Negl Trop Dis. 2010;4(4):e623. doi: 10.1371/journal.pntd.0000623 20436958
69. Pialoux G, Gaüzère B-A, Jauréguiberry S, Strobel M, Chikungunya, an epidemic arbovirosis. The Lancet Infectious Diseases. 2007;7(5):319–27. 17448935
70. Josseran L, Paquet C, Zehgnoun A, Caillere N, Le Tertre A, Solet J-L, et al. Chikungunya disease outbreak, Reunion Island. Emerg Infect Dis. 2006;12(12):1994–5. 17354339
71. Van-Mai C-L, Claudine R, Anita T, Emilie R, Anne-Laure B, Henri-Pierre M, et al. Zika virus, French Polynesia, South Pacific, 2013. Emerging Infectious Disease Journal. 2014;20(6):1084.
72. Vireak H, Chadwick YY, Ly S, Andrew DH, Amelia PTdR, Robert BT, et al. Zika virus infection, Cambodia, 2010. Emerging Infectious Disease Journal. 2012;18(2):349.