Geographical distributions of African malaria vector sibling species and evidence for insecticide resistance
Open accessAbstract
BACKGROUND: Many of the mosquito species responsible for malaria transmission belong to a sibling complex; a taxonomic group of morphologically identical, closely related species. Sibling species often differ in several important factors that have the potential to impact malaria control, including their geographical distribution, resistance to insecticides, biting and resting locations, and host preference. The aim of this study was to define the geographical distributions of dominant malaria vector sibling species in Africa so these distributions can be coupled with data on key factors such as insecticide resistance to aid more focussed, species-selective vector control. RESULTS: Within the Anopheles gambiae species complex and the Anopheles funestus subgroup, predicted geographical distributions for Anopheles coluzzii, An. gambiae (as now defined) and An. funestus (distinct from the subgroup) have been produced for the first time. Improved predicted geographical distributions for Anopheles arabiensis, Anopheles melas and Anopheles merus have been generated based on records that were confirmed using molecular identification methods and a model that addresses issues of sampling bias and past changes to the environment. The data available for insecticide resistance has been evaluated and differences between sibling species are apparent although further analysis is required to elucidate trends in resistance. CONCLUSIONS: Sibling species display important variability in their geographical distributions and the most important malaria vector sibling species in Africa have been mapped here for the first time. This will allow geographical occurrence data to be coupled with species-specific data on important factors for vector control including insecticide resistance. Species-specific data on insecticide resistance is available for the most important malaria vectors in Africa, namely An. arabiensis, An. coluzzii, An. gambiae and An. funestus. Future work to combine these data with the geographical distributions mapped here will allow more focussed and resource-efficient vector control and provide information to greatly improve and inform existing malaria transmission models.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015
Bhatt, S., Weiss, D. J., Cameron, E., Bisanzio, D., Mappin, B., Dalrymple, U., Battle, K. E., Moyes, C. L., Henry, A., Eckhoff, P. A., et al. (2015) · Nature · doi:10.1038/nature15535 · Cited by 3,225 · see citing works
Self-citationSinka, M. E., Bangs, M. J., Manguin, S., Coetzee, M., Mbogo, C. M., Hemingway, J., Patil, A. P., Temperley, W. H., Gething, P. W., Kabaria, C. W., et al. (2010) · Parasites & Vectors · doi:10.1186/1756-3305-3-117 · Cited by 761 · see citing works
Self-citationCharacterizing, controlling and eliminating residual malaria transmission
Killeen, G. F. (2014) · Malaria Journal · doi:10.1186/1475-2875-13-330 · Cited by 506 · see citing works
On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms
della Torre, A., Tu, Z., & Petrarca, V. (2005) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2005.02.006 · Cited by 244 · see citing works
Mwangangi, J. M., Mbogo, C. M., Orindi, B. O., Muturi, E. J., Midega, J. T., Nzovu, J., Gatakaa, H., Githure, J., Borgemeister, C., Keating, J., et al. (2013) · Malaria Journal · doi:10.1186/1475-2875-12-13 · Cited by 242 · see citing works
Kelly-Hope, L. A., Hemingway, J., & McKenzie, F. E. (2009) · Malaria Journal · doi:10.1186/1475-2875-8-268 · Cited by 143 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 41
- [1]Battle KE Gething PW Elyazar IRF Moyes CL Sinka ME Howes RE The global public health significance of Plasmodium vivax Adv Parasitol 2012 80 1 111 10.1016/B978-0-12-397900-1.00001-3 23199486 · DOI
- [2]Sinka ME Bangs MJ Manguin S Rubio-Palis Y Chareonviriyaphap T Coetzee M A global map of dominant malaria vectors Parasit Vectors 2012 5 69 10.1186/1756-3305-5-69 22475528 PMC3349467 · DOI
- [3]Coetzee M Hunt RH Wilkerson R Della Torre A Coulibaly MB Besansky NJ Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex Zootaxa 2013 3619 246 274 10.11646/zootaxa.3619.3.2 26131476 · DOI
- [4]Kipyab PC Khaemba BM Mwangangi JM Mbogo CM The bionomics of Anopheles merus (Diptera: Culicidae) along the Kenyan coast Parasit Vectors 2013 6 37 10.1186/1756-3305-6-37 23410133 PMC3584914 · DOI
- [5]Ebenezer A Noutcha AEM Okiwelu SN Relationship of annual entomological inoculation rates to malaria transmission indices, Bayelsa State, Nigeria J Vector Borne Dis. 2016 53 46 53 27004578
- [7]Hemingway J Ranson H Magill A Kolaczinski J Fornadel C Gimnig J Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet 2016 387 1785 1788 10.1016/S0140-6736(15)00417-1 26880124 PMC6215693 · DOI · Paper page
- [8]Massey NC Garrod G Wiebe A Henry AJ Huang Z Moyes CL A global bionomic database for the dominant vectors of human malaria Sci Data 2016 3 160014 10.1038/sdata.2016.14 26927852 PMC4772652 · DOI
- [9]Moyes CL Temperley WH Henry AJ Burgert CR Hay SI Providing open access data online to advance malaria research and control Malar J 2013 12 161 10.1186/1475-2875-12-161 23680401 PMC3662599 · DOI
- [10]Phillips SJ Dudik M Elith J Graham CH Lehmann A Leathwick J Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data Ecol Appl 2009 19 181 197 10.1890/07-2153.1 19323182 · DOI · Paper page
- [14]Weiss DJ Mappin B Dalrymple U Bhatt S Cameron E Hay SI Re-examining environmental correlates of Plasmodium falciparum malaria endemicity: a data-intensive variable selection approach Malar J 2015 14 68 10.1186/s12936-015-0574-x 25890035 PMC4333887 · DOI
- [15]De’ath G Boosted trees for ecological modeling and prediction Ecology 2007 88 243 251 10.1890/0012-9658(2007)88[243:BTFEMA]2.0.CO;2 17489472 · DOI
- [16]Elith J Graham CH Anderson RP Dudik M Ferrier S Guisan A Novel methods improve prediction of species’ distributions from occurrence data Ecography 2006 29 129 151 10.1111/j.2006.0906-7590.04596.x · DOI · Paper page
- [17]Elith J Leathwick JR Hastie T A working guide to boosted regression trees J Anim Ecol 2008 77 802 813 10.1111/j.1365-2656.2008.01390.x 18397250 · DOI · Paper page
- [18]Moyes CL Shearer FM Huang Z Wiebe A Gibson HS Nijman V Predicting the geographical distributions of the macaque hosts and mosquito vectors of Plasmodium knowlesi malaria in forested and non-forested areas Parasit Vectors 2016 9 242 10.1186/s13071-016-1527-0 27125995 PMC4850754 · DOI
- [19]Shearer FM Huang Z Weiss DJ Wiebe A Gibson HS Battle KE Estimating geographical variation in the risk of zoonotic Plasmodium knowlesi infection in countries eliminating malaria PLoS Negl Trop Dis 2016 10 e0004915 10.1371/journal.pntd.0004915 27494405 PMC4975412 · DOI
- [20]Fleiss J Levin B Paik M Statistical methods for rates and proportions 2003 Hoboken Wiley
- [21]Drake JM Beier JC Ecological niche and potential distribution of Anopheles arabiensis in Africa in 2050 Malar J 2014 13 213 10.1186/1475-2875-13-213 24888886 PMC4066281 · DOI
- [22]Fossog BT Ayala D Acevedo P Kengne P Mebuy INA Makanga B Habitat segregation and ecological character displacement in cryptic African malaria mosquitoes Evol Appl 2015 8 326 345 10.1111/eva.12242 25926878 PMC4408144 · DOI · Paper page
- [23]Adamou A Dao A Timbine S Kassogue Y Yaro AS Diallo M The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel Malar J 2011 10 151 10.1186/1475-2875-10-151 21645385 PMC3123247 · DOI
- [24]Lee Y Meneses CR Fofana A Lanzaro GC Desiccation resistance among subpopulations of Anopheles gambiae s.s. from Selinkenyi, Mali J Med Entomol 2009 46 316 320 10.1603/033.046.0216 19351082 · DOI
- [25]Lyons CL Coetzee M Chown SL Stable and fluctuating temperature effects on the development rate and survival of two malaria vectors, Anopheles arabiensis and Anopheles funestus Parasit Vectors 2013 6 104 10.1186/1756-3305-6-104 23590860 PMC3637585 · DOI
- [26]de Souza D Kelly-Hope L Lawson B Wilson M Boakye D Environmental factors associated with the distribution of Anopheles gambiae s.s in Ghana; an important vector of lymphatic filariasis and malaria PLoS ONE 2010 5 e9927 10.1371/journal.pone.0009927 20360950 PMC2847902 · DOI
- [27]Huestis DL Yaro AS Traore AI Adamou A Kassogue Y Diallo M Variation in metabolic rate of Anopheles gambiae and A. arabiensis in a Sahelian village J Exp Biol 2011 214 2345 2353 10.1242/jeb.054668 21697426 PMC3120220 · DOI
- [29]Kipyab PC Khaemba BM Mwangangi JM Mbogo CM The physicochemical and environmental factors affecting the distribution of Anopheles merus along the Kenyan coast Parasit Vectors 2015 8 221 10.1186/s13071-015-0819-0 25889775 PMC4396831 · DOI
- [30]Kirby MJ Lindsay SW Effect of temperature and inter-specific competition on the development and survival of Anopheles gambiae sensu stricto and An. arabiensis larvae Acta Trop 2009 109 118 123 10.1016/j.actatropica.2008.09.025 19013420 · DOI
- [31]Lyons CL Coetzee M Terblanche JS Chown SL Thermal limits of wild and laboratory strains of two African malaria vector species, Anopheles arabiensis and Anopheles funestus Malar J 2012 11 226 10.1186/1475-2875-11-226 22770378 PMC3507762 · DOI
- [32]Paaijmans KP Huijben S Githeko AK Takken W Competitive interactions between larvae of the malaria mosquitoes Anopheles arabiensis and Anopheles gambiae under semi-field conditions in western Kenya Acta Trop 2009 109 124 130 10.1016/j.actatropica.2008.07.010 18760989 · DOI
- [33]Afrane YA Zhou G Lawson BW Githeko AK Yan G Life-table analysis of Anopheles arabiensis in western Kenya highlands: effects of land covers on larval and adult survivorship Am J Trop Med Hyg 2007 77 660 666 17978067
- [34]Minakawa N Dida GO Sonye GO Futami K Njenga SM Malaria vectors in Lake Victoria and adjacent habitats in Western Kenya PLoS ONE 2012 7 e32725 10.1371/journal.pone.0032725 22412913 PMC3297610 · DOI
- [35]Dery DB Brown C Asante KP Adams M Dosoo D Amenga-Etego S Patterns and seasonality of malaria transmission in the forest-savannah transitional zones of Ghana Malar J 2010 9 314 10.1186/1475-2875-9-314 21054895 PMC2989982 · DOI
- [36]Guelbeogo WM Sagnon N Grushko O Yameogo MA Boccolini D Besansky NJ Seasonal distribution of Anopheles funestus chromosomal forms from Burkina Faso Malar J 2009 8 239 10.1186/1475-2875-8-239 19857258 PMC2775746 · DOI
- [38]Simard F Lehmann T Lemasson JJ Diatta M Fontenille D Persistence of Anopheles arabiensis during the severe dry season conditions in Senegal: an indirect approach using microsatellite loci Insect Molec Biol 2000 9 467 479 10.1046/j.1365-2583.2000.00210.x 11029665 · DOI
- [39]Athrey G Hodges TK Reddy MR Overgaard HJ Matias A Ridl FC The effective population size of malaria mosquitoes: large impact of vector control PLoS Genet 2012 8 e1003097 10.1371/journal.pgen.1003097 23271973 PMC3521722 · DOI
- [41]Crook SE Baptista A The effect of permethrin-impregnated wall-curtains on malaria transmission and morbidity in the suburbs of Maputo, Mozambique Trop Geogr Med 1995 47 64 67 8592765
- [42]Gimnig JE Vulule JM Lo TQ Kamau L Kolczak MS Phillips-Howard PA Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission Am J Trop Med Hyg 2003 68 16 22 12749481
- [43]Govella NJ Chaki PP Killeen GF Entomological surveillance of behavioural resilience and resistance in residual malaria vector populations Malar J 2013 12 124 10.1186/1475-2875-12-124 23577656 PMC3637503 · DOI
- [44]Sinka ME Golding N Massey NC Wiebe A Huang Z Hay SI Modelling the relative abundance of the primary African vectors of malaria before and after the implementation of indoor, insecticide-based vector control Malar J 2016 15 142 10.1186/s12936-016-1187-8 26945997 PMC4779559 · DOI
- [45]Killeen GF, Kiware SS, Okumu FO, Sinka ME, Moyes CL, Massey NC, et al. Going beyond personal protection against mosquito bites to eliminate malaria transmission: population suppression of malaria vectors that exploit both human and animal blood. BMJ Glob Health. http://archive.lstmed.ac.uk/6378/ (in press). PMC5444054 28589015
- [47]Chanda E Thomsen EK Musapa M Kamuliwo M Brogdon WG Norris DE An operational framework for insecticide resistance management planning Emerg Infect Dis 2016 22 773 779 10.3201/eid2205.150984 27089119 PMC4861508 · DOI · Paper page
- [48]Coetzee M Koekemoer LL Molecular systematics and insecticide resistance in the major African malaria vector Anopheles funestus An Rev Entomol 2013 58 393 412 10.1146/annurev-ento-120811-153628 23317045 · DOI
- [49]Coleman M, Hemingway J, Gleave K, Wiebe A, Gething PW, Moyes CL. Developing global maps of insecticide resistance risk to improve vector control. Malar J. doi:10.1186/s12936-017-1733-z. PMC5320685 28222727 · DOI
Cited by
Sorted by citations
Yokoly, F. N., Zahouli, J. B. Z., Small, G., Ouattara, A. F., Opoku, M., de Souza, D. K., & Koudou, B. G. (2021) · Malaria Journal · doi:10.1186/s12936-021-03938-1 · Cited by 24 · see citing works
Kroko-Djahouri, N. W. M., Guindo-Coulibaly, N., Assouho, K. F., Zoh, D. D., Tia, E., Sadia-Kacou, A. M. C., Azongnibo, K. R. M., Kpan, M. D. S., Kouadio, A. M. N., & Adja, A. M. (2024) · International Journal of Tropical Insect Science · doi:10.1007/s42690-024-01351-0 · Cited by 1 · see citing works
“In this continent, the parasites responsible for human malaria are mainly transmitted by primary vector species such as Anopheles gambiae sensulato ( s.l. ) Giles, An. funestus s.l. Giles and An. nili s.l. Theobald (Wiebe et al. 2017; Ossè et al. 2019).”
- Authors
- Wiebe, A., Longbottom, J., Gleave, K., Shearer, F. M., Sinka, M. E., Massey, N. C., Cameron, E., Bhatt, S., Gething, P. W., Hemingway, J., Smith, D. L., Coleman, M., & Moyes, C. L.
- Affiliations
- University of Oxford (GB)
- Liverpool School of Tropical Medicine (GB)
- St Mary's Hospital (GB)
- University of Washington (US)
- Corresponding author
- Moyes, Catherine L.
- ORCID
- Venue
- Malaria Journal
- Published
- 2017-02-20
- Volume
- 16
- Issue
- 1
- Pages
- 85-85
- ISSN
- 1475-2875 (ISSN-L)
- PMC
- PMC5319841
- OpenAlex
- W2591407193
- Cited by
- 160
- References
- 6
- Citations by year
- 2026: 14 · 2025: 12 · 2024: 20 · 2023: 12 · 2022: 18 · 2021: 24 · 2020: 26 · 2019: 15 · 2018: 13 · 2017: 6
- FWCI
- 15.41
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Malaria Journal (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- LSTM Online Archive (Liverpool School of Tropical Medicine) (acceptedVersion)
- LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- Spiral (Imperial College London) (submittedVersion, other-oa)
- Funders
- Wellcome Trust (108440/Z/15/Z)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
- Life Sciences › Immunology and Microbiology › Parasitology › Vector-borne infectious diseases
- Keywords
- malaria vectors, cryptic species, geographic distribution, insecticide resistance, Anopheles gambiae species complex, Anopheles funestus, Anopheles coluzzii, Anopheles arabiensis, Anopheles melas, Anopheles merus, malaria transmission model, Africa
- MeSH terms
- Mosquito Vectors, Africa, Animals, Anopheles, Insecticide Resistance, Phylogeography
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review