The Anopheles coluzzii range extends into Kenya: detection, insecticide resistance profiles and population genetic structure in relation to conspecific populations in West and Central Africa

Abstract

Background: Anopheles coluzzii is a primary vector of malaria found in West and Central Africa, but its presence has hitherto never been documented in Kenya. A thorough understanding of vector bionomics is important as it enables the implementation of targeted and effective vector control interventions. Malaria vector surveillance efforts in the country have tended to focus on historically known primary vectors. The current study sought to determine the taxonomic status of samples collected from five different malaria epidemiological zones in Kenya as well as describe the population genetic structure and insecticide resistance profiles in relation to other An. coluzzii populations.

Methods: Mosquitoes were sampled as larvae from Busia, Kwale, Turkana, Kirinyaga and Kiambu counties, representing the range of malaria endemicities in Kenya, in 2019 and 2021 and emergent adults analysed using Whole Genome Sequencing (WGS) data processed in accordance with the Anopheles gambiae 1000 Genomes Project phase 3. Where available, historical samples from the same sites were included for WGS. Comparisons were made with An. coluzzii cohorts from West and Central Africa.

Results: This study reports the detection of An. coluzzii for the first time in Kenya. The species was detected in Turkana County across all three time points from which samples were analyzed and its presence confirmed through taxonomic analysis. Additionally, there was a lack of strong population genetic differentiation between An. coluzzii from Kenya and those from the more northerly regions of West and Central Africa, suggesting they represent a connected extension to the known species range. Mutations associated with target-site resistance to DDT and pyrethroids and metabolic resistance to DDT were found at high frequencies up to 64%. The profile and frequencies of the variants observed were similar to An. coluzzii from West and Central Africa but the ace-1 mutation linked to organophosphate and carbamate resistance present in An. coluzzii from coastal West Africa was absent in Kenya.

Conclusions: These findings emphasize the need for the incorporation of genomics in comprehensive and routine vector surveillance to inform on the range of malaria vector species, and their insecticide resistance status to inform the choice of effective vector control approaches.

Keywords: Anopheles coluzzii; Insecticide resistance; Kenya; Malaria vectors; Population structure.

Fig. 1

Map of Kenya showing the study sites. The figure shows the sampling locations in Kenya in relation to Plasmodium falciparum prevalence rate in 2015 standardized to the age group 2 to 10 years using data obtained from the malariaAtlas R package [27]

Fig. 2

Taxon confirmation of Kenya An. coluzzii. Confirmation of taxon assignment using principal components analysis (PCA) and neighbour-joining tree (NJT) analysis, comparing samples in this study with reference samples from the Anopheles gambiae 1000 genomes project from inland West Africa (Burkina Faso, Mali), coastal West Africa (Cote d’Ivoire, Ghana), Central Africa (Cameroon, the Central African Republic, Angola) and the study of Fontaine et al. [31]. a PCA. b NJT

Fig. 3

Population genetic structure of Kenyan An. coluzzii. The figure shows the analysis of geographical population structure within An. coluzzii, comparing samples from Turkana, Kenya collected in this study with reference samples from the Ag1000G project and Fontaine et al. [31]. Kenyan An. coluzzii are most closely related to An. coluzzii from inland West Africa (Mali, Burkina Faso) and Northern Cameroon. a PCA. b NJT

Fig. 4

Insecticide resistance profiles of Kenyan An. coluzzii. The figure shows amino acid substitution frequencies in genes associated with target-site resistance to DDT and pyrethroids. a Vgsc (AGAP004707). b Gste2 (AGAP009194)