Unexpected diversity of Anopheles species in Eastern Zambia: Implications for evaluating vector behavior and interventions using molecular tools

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Lobo, Neil F ^a   St Laurent, Brandyce ^a   Sikaala, Chadwick H ^b   Hamainza, Busiku ^b   Chanda, Javan ^b   Chinula, Dingani ^b   Krishnankutty, Sindhu M ^c   Mueller, Jonathan D ^a   Deason, Nicholas A ^a   Hoang, Quynh T ^a   Boldt, Heather L ^a   Thumloup, Julie ^a   Stevenson, Jennifer ^d,e   Seyoum, Aklilu ^f   Collins, Frank H ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b Chainama Hospital College Grounds   (Zambia)

^c MONTANA STATE UNIVERSITY   (United States)

^d JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^e Macha Research Trust   (Zambia)

^f ABT ASSOCIATES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SPACER DNA;

ANIMAL; ANIMAL BEHAVIOR; ANOPHELES; BIODIVERSITY; CLASSIFICATION; DNA SEQUENCE; DRUG EFFECTS; GENE; GENETICS; INSECT VECTOR; INSECTICIDE RESISTANCE; MOSQUITO CONTROL; PHYLOGENY; PROCEDURES; ZAMBIA;

ANIMALS; ANOPHELES; BEHAVIOR, ANIMAL; BIODIVERSITY; DNA, INTERGENIC; GENES, INSECT; INSECT VECTORS; INSECTICIDE RESISTANCE; MOSQUITO CONTROL; PHYLOGENY; SEQUENCE ANALYSIS, DNA; ZAMBIA;

EID: 84949603844     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17952     Document Type: Article

References (61)

1. malERA Consultative Group on Vector Control. A research agenda for malaria eradication: vector control. PLoS Med 8 (1) (2011).
2. Killeen, G. F. Characterizing, controlling and eliminating residual malaria transmission. Malar J 13, 330, doi: 10.1186/1475-2875-13-330 (2014).
3. Bayoh, M. N. et al. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malaria Journal 9, 62, doi: 10.1186/1475-2875-9-62 (2010).
4. Elliott, R. The influence of vector behaviour on malaria transmission. Am J Trop Med Hyg 21, 755-763 (1972).
5. Mattingly, P. F. Mosquito behaviour in relation to disease eradication programmes. Annu Rev Entomol 7, 419-436, doi: 10.1146/annurev.en.07.010162.002223 (1962).
6. Gillies, M. T. The role of secondary vectors of malaria in north-east Tanganyika. Trans R Soc Trop Med Hyg 58, 154-158 (1964).
7. Antonio-Nkondjio, C. et al. Complexity of the malaria vectorial system in Cameroon: contribution of secondary vectors to malaria transmission. Journal of medical entomology 43, 1215-1221 (2006).
8. Killeen, G. F. et al. Eliminating malaria vectors. Parasit Vectors 6, 172, doi: 10.1186/1756-3305-6-172 (2013).
9. Reid, J. A. Secondary vectors, an obstacle to malaria eradication. Med J Malaya 14, 228-231 (1960).
10. Ranson, H. et al. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27, 91-98, doi: 10.1016/j.pt.2010.08.004 (2011).
11. Gatton, M. L. et al. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution 67, 1218-1230, doi: 10.1111/evo.12063 (2013).
12. Strode, C., Donegan, S., Garner, P., Enayati, A. A. & Hemingway, J. The impact of pyrethroid resistance on the efficacy of insecticidetreated bed nets against African anopheline mosquitoes: systematic review and meta-analysis. PLoS Med 11, e1001619, doi: 10.1371/journal.pmed.1001619 (2014).
13. Russell, T. L., Beebe, N. W., Cooper, R. D., Lobo, N. F. & Burkot, T. R. Successful malaria elimination strategies require interventions that target changing vector behaviours. Malar J 12, 56, doi: 10.1186/1475-2875-12-56 (2013).
14. Russell, T. L. et al. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J 10, 80, doi: 10.1186/1475-2875-10-80 (2011).
15. Taylor, B. Changes in the feeding behaviour of a malaria vector, Anopheles farauti Lav., following the use of DDT as a residual spray in houses in the British Solomon Islands Protectorate. Trans R Entomol Soc London 127 (1975).
16. Reddy, M. R. et al. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J 10, 184, doi: 10.1186/1475-2875-10-184 (2011).
17. Bayoh, M. N. et al. Persistently high estimates of late night, indoor exposure to malaria vectors despite high coverage of insecticide treated nets. Parasit Vectors 7, 380, doi: 10.1186/1756-3305-7-380 (2014).
18. Coetzee, M. et al. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 3619, 246-274 (2013).
19. Clarkson, C. S. et al. Adaptive introgression between Anopheles sibling species eliminates a major genomic island but not reproductive isolation. Nature communications 5, 4248, doi: 10.1038/ncomms5248 (2014).
20. Kawada, H. et al. Reconsideration of Anopheles rivulorum as a vector of Plasmodium falciparum in western Kenya: some evidence from biting time, blood preference, sporozoite positive rate, and pyrethroid resistance. Parasit Vectors 5, 230, doi: 10.1186/1756-3305-5-230 (2012).
21. Coetzee, M. Chromosomal and cross-mating evidence for two species within Anopheles (A.) coustani (Diptera: Culicidae). Syst Entomol. 8, 137-141 (1983).
22. Coetzee, M. Anopheles crypticus, new species from South Africa is distinguished from Anopheles coustani (Diptera: Culicidae) Mosq Syst. 26, 125-131 (1994).
23. Fornadel, C. M., Norris, L. C., Franco, V. & Norris, D. E. Unexpected anthropophily in the potential secondary malaria vectors Anopheles coustani s.l. and Anopheles squamosus in Macha, Zambia. Vector Borne Zoonotic Dis 11, 1173-1179, doi: 10.1089/vbz.2010.0082 (2011).
24. Stevenson, J. et al. Novel vectors of malaria parasites in the western highlands of Kenya. Emerg Infect Dis 18, 1547-1549, doi: 10.3201/eid1809.120283 (2012).
25. Besansky, N. J. Complexities in the analysis of cryptic taxa within the genus Anopheles. Parassitologia 41, 97-100 (1999).
26. Hackett, B. J. et al. Ribosomal DNA internal transcribed spacer (ITS2) sequences differentiate Anopheles funestus and An. rivulorum, and uncover a cryptic taxon. Insect Mol Biol 9, 369-374 (2000).
27. Koekemoer, L. L. et al. Cryptic species within Anopheles longipalpis from southern Africa and phylogenetic comparison with members of the An. funestus group. Bull Entomol Res 99, 41-49, doi: 10.1017/s0007485308006123 (2009).
28. Spillings, B. L. et al. A new species concealed by Anopheles funestus Giles, a major malaria vector in Africa. Am J Trop Med Hyg 81, 510-515 (2009).
29. Bigoga, J. D. et al. Seasonal prevalence of malaria vectors and entomological inoculation rates in the rubber cultivated area of Niete, South Region of Cameroon. Parasit Vectors 5, 197, doi: 10.1186/1756-3305-5-197 (2012).
30. Collins, F. H. & Paskewitz, S. M. A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Mol Biol 5, 1-9 (1996).
31. Scott, J. A., Brogdon, W. G. & Collins, F. H. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49, 520-529 (1993).
32. Beebe, N. W. & Saul, A. Discrimination of all members of the Anopheles punctulatus complex by polymerase chain reaction - restriction fragment length polymorphism analysis. Am J Trop Med Hyg 53, 478-481 (1995).
33. Kumar, N. P., Rajavel, A. R., Natarajan, R. & Jambulingam, P. DNA barcodes can distinguish species of Indian mosquitoes (Diptera: Culicidae). Journal of medical entomology 44, 1-7 (2007).
34. Dusfour, I. et al. Polymerase chain reaction identification of three members of the Anopheles sundaicus (Diptera: Culicidae) complex, malaria vectors in Southeast Asia. Journal of medical entomology 44, 723-731 (2007).
35. Riehle, M. M. et al. A cryptic subgroup of Anopheles gambiae is highly susceptible to human malaria parasites. Science 331, 596-598, doi: 10.1126/science.1196759 (2011).
36. Tainchum, K. et al. Diversity of Anopheles species and trophic behavior of putative malaria vectors in two malaria endemic areas of northwestern Thailand. J Vector Ecol 39, 424-436, doi: 10.1111/jvec.12118 (2014).
37. Fanello, C. et al. The pyrethroid knock-down resistance gene in the Anopheles gambiae complex in Mali and further indication of incipient speciation within An. gambiae s.s. Insect Mol Biol 12, 241-245 (2003).
38. Singh, B. et al. A genus-and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg 60, 687-692 (1999).
39. Sikaala, C. H. et al. A cost-effective, community-based, mosquito-trapping scheme that captures spatial and temporal heterogeneities of malaria transmission in rural Zambia. Malar J 13, 225, doi: 10.1186/1475-2875-13-225 (2014).
40. Sikaala, C. H. et al. Evaluation of alternative mosquito sampling methods for malaria vectors in Lowland South - East Zambia. Parasit Vectors 6, 91, doi: 10.1186/1756-3305-6-91 (2013).
41. Chanda, E. et al. Integrated vector management: the Zambian experience. Malar J 7, 164, doi: 10.1186/1475-2875-7-164 (2008).
42. Kent, R. J., Thuma, P. E., Mharakurwa, S. & Norris, D. E. Seasonality, blood feeding behavior, and transmission of Plasmodium falciparum by Anopheles arabiensis after an extended drought in southern Zambia. Am J Trop Med Hyg 76, 267-274 (2007).
43. Norris, L. C. & Norris, D. E. Efficacy of long-lasting insecticidal nets in use in Macha, Zambia, against the local Anopheles arabiensis population. Malar J 10, 254, doi: 10.1186/1475-2875-10-254 (2011).
44. Carrara, G. C., Petrarca, V., Niang, M. & Coluzzi, M. Anopheles pharoensis and transmission of Plasmodium falciparum in the Senegal River delta, West Africa. Med Vet Entomol 4, 421-424 (1990).
45. Okara, R. M. et al. Distribution of the main malaria vectors in Kenya. Malar J 9, 69, doi: 10.1186/1475-2875-9-69 (2010).
46. Pates, H. V. et al. Unexpected anthropophagic behaviour in Anopheles quadriannulatus. Med Vet Entomol 15, 293-298 (2001).
47. Pates, H. V., Takken, W., Curtis, C. F. & Jamet, H. Zoophilic Anopheles quadriannulatus species B found in a human habitation in Ethiopia. Ann Trop Med Parasitol 100, 177-179, doi: 10.1179/136485906× 86374 (2006).
48. Carnevale, P., Le Goff, G., Toto, J. C. & Robert, V. Anopheles nili as the main vector of human malaria in villages of southern Cameroon. Med Vet Entomol 6, 135-138 (1992).
49. Gillies, M. & DeMeillon, B. The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical Region). Second edition. Johannesburg: South African Institute for Medical Research (1968).
50. Seyoum, A. et al. Human exposure to anopheline mosquitoes occurs primarily indoors, even for users of insecticide-treated nets in Luangwa Valley, South-east Zambia. Parasit Vectors 5, 101, doi: 10.1186/1756-3305-5-101 (2012).
51. Chaki, P. P. et al. An affordable, quality-assured community-based system for high-resolution entomological surveillance of vector mosquitoes that reflects human malaria infection risk patterns. Malar J 11, 172, doi: 10.1186/1475-2875-11-172 (2012).
52. Govella, N. J. et al. A new tent trap for sampling exophagic and endophagic members of the Anopheles gambiae complex. Malaria Journal 8, 157, doi: 10.1186/1475-2875-8-157 (2009).
53. Govella, N. J., Moore, J. D. & Killeen, G. F. An Exposure-Free Tool for Monitoring Adult Malaria Mosquito Populations. American Journal of Tropical Medicine and Hygiene 83, 596-600, doi: 10.4269/ajtmh.2010.09-0682 (2010).
54. Gillies, M. T. & Coetzee, M. A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical Region). South African Institute for Medical Research, Johannesburg, 1-139 (1987).
55. 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 3, 294-299 (1994).
56. Ratnasingham, S. & Hebert, P. D. bold: The Barcode of Life Data System (http://www.barcodinglife.org). Mol Ecol Notes 7, 355-364, doi: 10.1111/j.1471-8286.2007.01678.x (2007).
57. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30, 772-780, doi: 10.1093/molbev/mst010 (2013).
58. Katoh, K. & Toh, H. Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics 9, 212, doi: 10.1186/1471-2105-9-212 (2008).
59. Wheeler, T. J. & Kececioglu, J. D. Multiple alignment by aligning alignments. Bioinformatics 23, i559-568, doi: 10.1093/bioinformatics/btm226 (2007).
60. Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis Version 3.0.4 http://mesquiteproject.org. (2015) Date of access:01/03/2015.
61. Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574 (2003).