Barcoding Turkish Culex mosquitoes to facilitate arbovirus vector incrimination studies reveals hidden diversity and new potential vectors

Acta Tropica

Volumn 143, Issue , 2015, Pages 112-120

  Gunay, Filiz ^a   Alten, Bulent ^a   Simsek, Fatih ^b   Aldemir, Adnan ^c   Linton, Yvonne Marie ^d,e,f,g  

^a HACETTEPE UNIVERSITY   (Turkey)

^b ADNAN MENDERES UNIVERSITY   (Turkey)

^c KAFKAS UNIVERSITY   (Turkey)

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

^e SMITHSONIAN INSTITUTION   (United States)

^f DEPARTMENT OF PALEOBIOLOGY   (United States)

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

Author keywords

Arbovirus; Culex; DNA barcoding; New records; Turkey; Vector

Indexed keywords

DNA; MITOCHONDRION; MORPHOLOGY; MOSQUITO; NEW RECORD; SPECIES INVENTORY; TAXONOMY;

ARBOVIRUS; ARTICLE; CULEX; CULEX EUROPAEUS; CULEX HORTENSIS; CULEX IMPUDICUS; CULEX LATICINCTUS; CULEX MARTINII; CULEX MIMETICUS; CULEX PEREXIGUUS; CULEX PIPIENS; CULEX PIPIENS MOLESTUS; CULEX QUINQUEFASCIATUS; CULEX TERRITANS; CULEX THEILERI; CULEX TORRENTIUM; CULEX TRITAENIORHYNCHUS; CYTOCHROME C OXIDASE I GENE; DNA BARCODING; GENETIC DISTANCE; MITOCHONDRIAL GENE; MORPHOLOGY; NONHUMAN; SPECIES IDENTIFICATION; TURKEY (REPUBLIC); ANIMAL; DISEASE CARRIER; GENETICS; ISOLATION AND PURIFICATION; POLYMERASE CHAIN REACTION; PROCEDURES; SPECIES DIFFERENCE; TURKEY; VIROLOGY; WEST NILE VIRUS;

TURKEY;

ARBOVIRUS; NEOCULEX; WEST NILE VIRUS;

ANIMALS; ARBOVIRUSES; CULEX; DNA BARCODING, TAXONOMIC; INSECT VECTORS; POLYMERASE CHAIN REACTION; SPECIES SPECIFICITY; TURKEY; WEST NILE VIRUS;

EID: 84922337042     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2014.10.013     Document Type: Article

References (84)

1. Alten B., Caglar S.S., Özer N. Malaria and its vectors in Turkey. Eur. Mosq. Bull. 2000, 7:27-33.
2. Azari-Hamidian S., Yaghoobi-Ershadi M.R., Javadian E., Abai M.R., Mobedi I., Linton Y.-M., Harbach R.E. Distribution and ecology of mosquitoes in a focus of dirofilariasis in northwestern Iran, with the first finding of filarial larvae in naturally infected local mosquitoes. Med. Vet. Entomol. 2009, 23:111-121. 10.1111/j.1365-2915.2009.00802.x.
3. Bahnck C.M., Fonseca D.M. Rapid assay to identify the two genetic forms of Culex (Culex) pipiens L. (Diptera: Culicidae) and hybrid populations. Am. J. Trop. Med. Hyg. 2006, 75:251-255.
4. Balenghien T., Fouque F., Sabatier P., Bicout D.J. Horse, bird, and human-seeking behavior and seasonal abundance of mosquitoes in a West Nile virus focus of southern France. J. Med. Entomol. 2006, 43:936-946. 10.1603/0022-2585(2006)43[936:HBAHBA]2.0.CO;2.
5. Balenghien T., Vazeille M., Reiter P., Schaffner F., Zeller H., Bicout D.J. Evidence of laboratory vector competence of Culex modestus for West Nile Virus. J. Am. Mosq. Control Assoc. 2007, 23:233-236. 10.2987/8756-971X(2007)23[233:EOLVCO]2.0.CO;2.
6. Becker N., Petric D., Zgomba M., Boase C., Dahl C., Madon M., Kaiser A. Mosquitoes and Their Control 2010, 608. Springer Heidelberg, Dordrecht, London, New York. second ed.
7. Bickley W.E., Harrison B.A. Separation of variable Culex territans specimens from other Culex (Neoculex) in North America. Mosq. Syst. 1989, 21:188-196.
8. Bohart R.M. The subgenus Neoculex in America, north of Mexico (Diptera: Culicidae). Ann. Am. Entomol. Soc. 1948, 41:330-345.
9. Busquets N., Alba A., Allepuz A., Aranda C., Nuñez J.I. Usutu virus sequences in Culex pipiens (Diptera: Culicidae), Spain. Emerg. Infect. Dis. 2008, 14:861-862. 10.3201/eid1405.071577.
10. Calherios C.M.L., Fontes G., Williams P., Rocha E.M.M. Experimental infection of Culex (Culex) quinquefasciatus and Aedes (Stegomyia) aegypti with Wuchereria bancrofti. Mem. Inst. Oswaldo Cruz 1998, 93:855-860. 10.1590/S0074-02761998000600029.
11. Chaskopoulou A., Dovas C.I., Chaintoutis S.C., Kashefi J., Koehler P., Papanastassopoulou M. Detection and early warning of West Nile virus circulation in central Macedonia, Greece, using sentinel chickens and mosquitoes. Vector Borne Zoonotic Dis. 2013, 13:723-732. 10.1089/vbz.2012.1176.
12. Clary D.O., Wolstenholme D.R. The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J. Mol. Evol. 1985, 22:252-271.
13. da Cunha Ramos H., Ribeiro H., Harrison B.A. A new European mosquito species: Culex (Neoculex) europaeus (Diptera: Culicidae). Eur. Mosq. Bull. 2003, 15:6-11.
14. Danabalan R., Ponsonby D.J., Linton Y.-M. A critical assessment of available molecular identification tools for determining the status of Culex pipiens s.l. in the United Kingdom. J. Am. Mosq. Control Assoc. 2012, 28:68-74. 10.2987/8756-971X-28.0.68.
15. Dehghan H., Sadraei J., Moosa-Kazemi S.H., Baniani N.A., Nowruzi F. The molecular and morphological variations of Culex pipiens complex (Diptera: Culicidae) in Iran. J. Vector Borne Dis. 2013, 50:111-120.
16. Do Q.H., Vu T.Q., Huynh T.K., Dinh Q.T., Deubel V. Current situation of Japanese encephalitis in the south of Vietnam, 1976-1992. Trop. Med. 1994, 36:202-214.
17. Erel D. Sivrisineklerin morfolojisi ve biolojisi. T.C. Saglik ve Sosyal Yardim Bakanligi Hifzissihha Okulu Yayin No. 28 1967, Gursoy Basimevi, Ankara, [In Turkish].
18. Ergunay K., Whitehouse C.A., Ozkul A. Current status of human arboviral diseases. Vector Borne Zoonotic Dis. 2011, 11(6):731-741. 10.1089/vbz.2010.0162.
19. Ergunay K., Gunay F., Oter K., Kasap O.E., Orsten S., Akkutay A.Z., Erdem H., Ozkul A., Alten B. Arboviral surveillance of field-collected mosquitoes reveals circulation of West Nile virus lineage 1 strains in eastern Thrace, Turkey. Vector Borne Zoonotic Dis. 2013, 13:744-752. 10.1089/vbz.2012.1288.
20. Ergunay K., Gunay F., Kasap O.E., Oter K., Gargari S., Karaoglu T., Tezcan S., Cabalar M., Yildirim Y., Emekdas G., Alten B., Ozkul A. Serological, molecular and entomological surveillance demonstrates widespread circulation of West Nile virus in Turkey. PLoS Negl. Trop. Dis. 2014, 8(7):e3028. 10.1371/journal.pntd.0003028.
21. Felsenstein J. Phylogenies and the comparative method. Am. Nat. 1985, 125(1):1-15.
22. Flores F.S., Diaz L.A., Batallan G.P., Almiron W.R., Contigiani M.S. Vertical transmission of St. Louis encephalitis virus in Culex quinquefasciatus (Diptera: Culicidae) in Cordoba, Argentina. Vector Borne Zoonotic Dis. 2010, 10(10):999-1002. 10.1089/vbz.2009.0136.
23. Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit from diverse metazoan invertebrates. Mol. Mar. Biol. Biotech. 1994, 3:294-299.
24. Francy D.B., Jaenson T.G., Lundstrom J.O., Schildt E.B., Espmark A., Henriksson B., Niklasson B. Ecologic studies of mosquitoes and birds as hosts of Ockelbo virus in Sweden and isolation of Inkoo and Batai viruses from mosquitoes. Am. J. Trop. Med. Hyg. 1989, 41(3):355-363.
25. Gad A.M., Hassan A.N., Merdan A.I.H. Transmission of rift valley fever virus by different geographic strains of Culex pipiens in Egypt. J. Egypt. Public Health Assoc. 1989, 64:363-379.
26. Goddard L.B., Roth A.E., Reisen W.K., Scott T.W. Vertical transmission of West Nile virus by three California Culex (Diptera: Culicidae) species. J. Med. Entomol. 2003, 40:743-746. 10.1603/0022-2585-40.6.743.
27. Gutsevich A.V., Monchadskii A.S., Shtakelberg A.A. Fauna of the USSR Diptera Volume III No 4. Mosquitoes, Family Culicidae 1974, Akademii Nauk SSSR Zoologicheskogo Institute, Leningrad, Russia, [NS no 100; in Russian, English translation by R. Lavoott, Ed. O. Theodor, Israel Program for Scientific Translations, Jerusalem].
28. Hannoun C., Panthier R., Mouchet J., Eouzan J.P. Isolement en France du virus West-Nile partir de malades et du vecteur Culex modestus Ficalbi. Comptes Rendus Hebdomadaires des Séances de l'Académie des Sciences. Série D, Sciences naturelles 1964, 259:4170-4172.
29. Harbach R.E. The mosquitoes of the subgenus Culex in southwest Asia and Egypt (Diptera, Culicidae). Contrib. Am. Entomol. Inst. 1988, 24:1-240.
30. Harbach R.E. The identity of Culex perexiguus Theobald versus Cx. univittatus in southern Europe. Eur. Mosq. Bull. 1999, 4:7.
31. Hubálek Z., Halouzka J. West Nile fever-a reemerging mosquito-borne viral disease in Europe. Emerg. Infect. Dis. 1999, 5:643-650.
32. Irdem E. Biological research in Çiyenli and Belemedik. Saglik Dergisi 1939, 15:864-878. [In Turkish].
33. Jeanmougin F., Thompson J.D., Gouy M., Higgins D.G., Gibson T.J. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 1998, 23:403-405.
34. Jupp P.G. Culex theileri and Sindbis virus; Salivary gland infection in relation to transmission. J. Am. Mosq. Control Assoc. 1985, 1:374-376.
35. Jupp G., Kemp A., Grobnelaar A., Leman P., Burt F.J., Alahmed A.M., Al Mujalli D., Al Khamees M., Swanepoel R. The 2000 epidemic of rift valley fever in Saudi Arabia: mosquito vector studies. Med. Vet. Entomol. 2002, 16:245-252. 10.1046/j.1365-2915.2002.00371.x.
36. Kirkpatrick T.W. The Mosquitoes of Egypt. Egyptian Government Anti-Malaria Commission 1925, 224. Government Printer, Cairo.
37. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980, 16:111-120.
38. Knight K.L., Stone A. A catalog of the mosquitoes of the world (Diptera: Culicidae) 1977, vol. VI. The Thomas Say Foundation, Entomological Society of America, College Park, MD. second ed.
39. Kolodziejek J., Pachler K., Bin H., Mendelson E., Shulman L., Orshan L., Nowotny N. Barkedji virus, a novel mosquito-borne flavivirus identified in Culex perexiguus mosquitoes, Israel, 2011. J. Gen. Virol. 2013, 94:2449-2457. 10.1099/vir.0.056200-0.
40. Kumari R., Kumar K., Rawat A., Singh G.R., Yadav N.K., Chauhan L.S. First indigenous transmission of Japanese encephalitis in urban areas of national capital territory of Delhi, India. Trop. Med. Int. Health 2013, 18:743-749. 10.1111/tmi.12104.
41. LaPointe D.A., Lee Goff M., Atkinson C.T. Comparative susceptibility of introduced forest-dwelling mosquitoes in Hawaii to avian malaria, Plasmodium relictum. J. Parasitol. 2005, 91:843-849. 10.1645/GE-3431.1.
42. Linton Y.-M., Pecor J.E., Porter C.H., Mitchell L.B., Garzon-Moreno A., Foley D.H., Pecor D.B., Wilkerson R.C. Mosquitoes of eastern Amazonian Ecuador: biodiversity, bionomics and barcodes. Mem. Inst. Oswaldo Cruz. 2013, 108:100-109.
43. Ludham K.W., Jachowsk L.A., Otto G.F. Potential vectors of Dirofilaria immitis. J. Am. Vet. Med. Assoc. 1970, 157:1354-1359.
44. Lundström J.O. Vector competence of western European mosquitoes for arboviruses: a review of field and experimental studies. Bull. Soc. Vector Ecol. 1994, 19:23-36.
45. McKeon S.N., Lehr M.A., Wilkerson R.C., Ruiz J.F., Sallum M.A., Lima J.B., Povoa M.M., Conn J.E. Lineage divergence detected in the malaria vector Anopheles marajoara (Diptera: Culicidae) in Amazonian Brazil. Malar. J. 2010, 9:271-284. 10.1186/1475-2875-9-271.
46. McIntosh B.M., Jupp P.G., Dickinson D.B., McGillivray G.M., Sweetnam J. Ecological studies on Sindbis and West Nile Viruses in South Africa, 1. Viral activity as revealed by infection of mosquitoes and sentinel fowls. S. Afr. J. Med. Sci. 1967, 32:1-14.
47. Meço O. Güneydoğu Anadolu bölgesi halkinda Bati Nil ateşi hemaglutinasyon-önlenim, antikorlarinin araştirilmasi. Mikrobiyol. Bul. 1977, 11:3-17. [in Turkish].
48. Mouchet J., Rageau J., Laumond C., Hannoun C., Beytout D., Oudar J., Corniou B., Chippaux A. Epidemiology of West Nile virus: study of a focus in Camargue, V. The vector: Culex modestus Ficalbi Diptera; Culicidae. Ann. Inst. Pasteur (Paris) 1970, 118:839-855. [in French].
49. Muñoz J., Ruiz S., Soriguer R., Alcaide M., Viana D.S., Roiz D., Vazquez A., Figuerola J. Feeding patterns of potential West Nile virus vectors in south-west Spain. PLoS One 2012, 7:e39549. 10.1371/journal.pone.0039549.
50. Orshan L., Bin H., Schnur H., Kaufman A., Valinsky A., Shulman L., Weiss L., Mendelson E., Pener H. Mosquito vectors of West Nile fever in Israel. Vector Borne Dis. Surveil. Prev. 2008, 45(5):939-947. 10.1603/0022-2585(2008)45[939:MVOWNF]2.0.CO;2.
51. Oter K., Gunay F., Tüzer E., Linton Y.-M., Bellini R., Alten B. First record of Stegomyia albopicta in Turkey determined by active ovitrap surveillance and DNA barcoding. Vector Borne Zoonotic Dis. 2013, 13:753-761. 10.1089/vbz.2012.1093.
52. Özkul A., Yìldìrìm Y., Pìnar D., Akcalì A., Yìlmaz V., Colak D. Serological evidence of West Nile virus (WNv) in mammalian species in Turkey. Epidemiol. Infect. 2005, 134:826-829. 10.1017/S0950268805005492.
53. Özkul A., Ergunay K., Koysuren A., Alkan F., Arsava E.M., Tezcan S., Emekdas G., Hacioglu S., Turan M., Us D. Concurrent occurrence of human and equine West Nile virus infections in Central Anatolia, Turkey: the first evidence for circulation of lineage 1 viruses. Int. J. Infect. Dis. 2013, 17:e546-e551. 10.1016/j.ijid.2013.02.005.
54. Özer N., Ergünay K., Şimşek F., Kaynaş S., Alten B., Çağlar S.S., Ustaçelebi S. West Nile virus studies in the Şanliurfa province of Turkey. J. Vect. Ecol. 2007, 32:202-206. 10.3376/1081-1710(2007)32[202:WNVSIT]2.0.CO;2.
55. Pandey B.D., Karabatsos N., Cropp B., Tagaki M., Tsuda Y., Ichinose A., Igarashi A. Identification of a flavivirus isolated from mosquitoes in Chiang Mai Thailand. Southeast Asian J. Trop. Med. Public Health 1999, 30:161-165.
56. Parrish D.W. The mosquitoes of Turkey. Mosq. News 1959, 19:264-266.
57. Parreira R., Cook S., Lopes A., de Matos A.P., de Almeida A.P., Piedade J., Esteves A. Genetic characterization of an insect-specific flavivirus isolated from Culex theileri mosquitoes collected in southern Portugal. Virus Res. 2012, 167:152-161. 10.1016/j.virusres.2012.04.010.
58. Pradeep Kumar N.P., Rajavel A.R., Natarajan R., Jambulingam P. DNA barcodes can distinguish species of Indian mosquitoes (Diptera: Culicidae). J. Med. Entomol. 2007, 44:1-7. 10.1603/0022-2585(2007)44[1:DBCDSO]2.0.CO.
59. Ramsdale C.D., Alten B., Çaglar S.S., Özer N. A revised, annotated checklist of the mosquitoes (Diptera, Culicidae) of Turkey. Eur. Mosq. Bull. 2001, 9:18-27.
60. Ratnasingham S., Hebert P.D.N. BOLD: the barcode of life data system. Mol. Ecol. Notes 2007, 7:355-364. DOI: 10.1111/j.1471-8286.2007.01678.x. (www.barcodinglife.org).
61. Ribeiro H., Pires C., Capela R. An annotated checklist of the mosquitoes of continental Portugal (Diptera, Culicidae). Actas do III Congresso Ibérico de Entomologia 1988, 233-253.
62. Rios J., Hacker C.S., Hailey C.A., Parsons R.E. Demographic and spatial analysis of West Nile virus and St. Louis encephalitis in Houston, Texas. J. Am. Mosq. Control Assoc. 2006, 22:254-263.
63. Roiz D., Vazquez A., Rosà R., Muñoz J., Arnoldi D., Rosso F., Figuerola J., Tenorio A., Rizzoli A. Blood meal analysis, flavivirus screening, and influence of meteorological variables on the dynamics of potential mosquito vectors of West Nile virus in northern Italy. J. Vector. Ecol. 2012, 37:20-28. 10.1111/j.1948-7134.2012.00196.x.
64. Rosen L., Shroyer D.A., Lien J.C. Transovarial transmission of Japanese encephalitis virus by Culex tritaeniorhynchus mosquitoes. Am. J. Trop. Med. Hyg. 1980, 29:711-712.
65. Rossi L., Pollono F., Meneguez P.G., Cancrini G. Quattro specie di culicidi come possibili vettori di Dirofilaria immitis nella risaia piemontese. Parassitologia 1999, 41:537-542. [in Italian with English abstract].
66. Ruiz-Lopez F., Wilkerson R.C., Conn J.E., McKeon S.N., Levin D.M., Quiñones M.L., Póvoa M.M., Linton Y.-M. DNA barcoding reveals both known and novel taxa in the albitarsis group (Anopheles: Nyssorhynchus) of neotropical malaria vectors. Parasites Vectors 2012, 5:44-56. 10.1186/1756-3305-5-44.
67. Saitou N., Nei M. The neighbour-joining method: a new method for reconstructing phylogenetic tress. Mol. Biol. Evol. 1987, 4:406-425.
68. Santa-Ana M., Khadem M., Capela R. Natural infection of Culex theileri (Diptera: Culicidae) with Dirofilaria immitis (Nematoda: Filarioidea) on Madeira Island, Portugal. J. Med. Entomol. 2006, 43:104-106. 10.1603/0022-2585(2006)043[0104:NIOCTD]2.0.CO;2.
69. Samanidou-Voyadjoglou A., Harbach R.E. Keys to the adult female mosquitoes (Culicidae) of Greece. Eur. Mosq. Bull. 2001, 10:13-20.
70. Samanidou A., Harbach R.E. Culex (Culex) tritaeniorhynchus Giles, a newly discovered potential vector of arboviruses in Greece. Eur. Mosq. Bull. 2003, 16:15-17.
71. Samina I., Margalit J., Peleg J. Isolation of viruses from mosquitoes in the Negev, Israel. Trans. R. Soc. Trop. Med. Hyg. 1986, 80:471-472. 10.1016/0035-9203(86)90348-2.
72. Schaffner E., Angel G., Geoffroy B., Hervy J.P., Rhaiem A., Brunhes J. The Mosquitoes of Europe 2001, Institute de Recherche pour le Développement (IRD), Montpellier, France. CD-Rom.
73. Shaikevich E.V. PCR-RFLP of the COI gene reliably differentiates Cx. pipiens, Cx. pipiens f. molestus and Cx. torrentium of the Pipiens Complex. Eur. Mosq. Bull. 2007, 23:25-30.
74. Shaikevich E.V., Vinogradova E.B. The discovery of a hybrid population of mosquitoes of the Culex pipiens L. complex (Diptera, Culicidae) on the Kos Island (Greece) by means of molecular markers. Entomol. Rev. 2014, 94:35-39.
75. Snow K.R. Mosquitoes. Naturalists' Handbook 1990, 14. Richmond Publishing, England.
76. Süyev M. Sitma Savasi Çalismalari Albümü. Türkiye Cumhuriet Saglik ve Sosyal Yardim Vekaleti Yayinlardan 1953, 162. Hüsnütabiat Matbaasi, Istanbul, 248pp, [in Turkish].
77. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
78. Takashima I., Hashimoto N. Getah virus in several species of mosquitoes. Trans. R. Soc. Trop. Med. Hyg. 1985, 79:546-550. 10.1016/0035-9203(85)90091-4.
79. Takashima I., Hashimoto N., Arikawa J., Matusumoto K. Getah virus in Aedes vexans nipponii and Culex tritaeniorhynchus: vector susceptibility and ability to transmit. Arch. Virol. 1983, 76:299-305. 10.1007/BF01311197.
80. Takashima I., Hashimoto N., Matsumoto K. Multiplication of several arboviruses isolated in Japan in Culex tritaeniorhynchus. Microbiol. Immunol. 1983, 27:561-563. 10.1111/j.1348-0421.1983.tb00608.x.
81. Turell M.J., Presley S.M., Gad A.M., Cope S.E., Dohm D.J., Morrill J.C., Arthur R.R. Vector competence of Egyptian mosquitoes for rift valley fever virus. Am. J. Trop. Med. Hyg. 1996, 54:136-139. 10.1603/0022-2585(2008)45[102:VCOSAM]2.0.CO;2.
82. Vazquez A., Ruiz S., Herrero L., Moreno J., Molero F., Magallanes A., Sanchez-Seco M.P., Figuerola J., Tenorio A. West Nile and Usutu viruses in mosquitoes in Spain, 2008-2009. Am. J. Trop. Med. Hyg. 2011, 85(1):178-181. 10.4269/ajtmh.2011.11-0042.
83. Votýpka J., Šeblová V., Rádrová J. Spread of the West Nile virus vector Culex modestus and the potential malaria vector Anopheles hyrcanus in central Europe. J. Vect. Ecol. 2008, 33:269-277. 10.3376/1081-1710-33.2.269.
84. Wills W.M., Jakob W.L., Francy D.B., Oertley R.E., Ananõ E., Calisher C.H., Monath T.P. Trans. R. Soc. Trop. Med. Hyg. 1985, 79:63-66. 10.1016/0035-9203(85)90238-X.