Outdoor malaria vector species profile in dryland ecosystems of Kenya

Abstract

Outdoor biting by anopheline mosquitoes is one of the contributors to residual malaria transmission, but the profile of vectors driving this phenomenon is not well understood. Here, we studied the bionomics and genetically characterized populations of An. gambiae and An. funestus complexes trapped outdoors in three selected dryland areas including Kerio Valley, Nguruman and Rabai in Kenya. We observed a higher abundance of Anopheles funestus group members (n = 639, 90.6%) compared to those of the An. gambiae complex (n = 66, 9.4%) with An. longipalpis C as the dominant vector species with a Plasmodium falciparum sporozoite rate (Pfsp) of 5.2% (19/362). The known malaria vectors including An. funestus s.s. (8.7%, 2/23), An. gambiae (14.3%, 2/14), An. rivulorum (14.1%, 9/64), An. arabiensis (1.9%, 1/52) occurred in low densities and displayed high Pfsp rates, which varied with the site. Additionally, six cryptic species found associated with the An. funestus group harbored Pf sporozoites (cumulative Pfsp rate = 7.2%, 13/181). We detected low frequency of resistant 119F-GSTe2 alleles in An. funestus s.s. (15.6%) and An. longipalpis C (3.1%) in Kerio Valley only. Evidence of outdoor activity, emergence of novel and divergent vectors and detection of mutations conferring metabolic resistance to pyrethroid/DDT could contribute to residual malaria transmission posing a threat to effective malaria control.

Figure 1

Map of Kenya showing the study areas and distribution of anopheline species found infected with Plasmodium falciparum sporozoites. Pie-chart indicating the relative abundance of the species infected based on actual numbers is shown for each study area. The map was designed using ArcMap 10.2.2 with the ocean and lakes base layer derived from Natural Earth (http://www.naturalearthdata.com/, a free GIS data source). The sample points were collected using a GPS gadget (garmin etrex 20, https://buy.garmin.com/en-US/US/p/518046), and the county boundaries for Kenya derived from Africa Open data (https://africaopendata.org/dataset/kenya-counties-shapefile, license Creative Commons).

Figure 2

(a) Outdoor mean catches/trap/day, (b) Species composition, in three study areas in dryland areas of Kenya. The number of trap nights were 44, 50 and 56 in Kerio Valley, Rabai and Nguruman, respectively.

Figure 3

Phylogenetic tree for represetative mosquitoes morphologically scored as An. funestus group infected with P. falciparum sprozoites. Few samples negative for the malaria parasite are also included. Bootstrap support values are indicated above the nodes from 1000 replicates. Highlighted in red are the infected samples.

Figure 4

Analysis of the polymorphism of a portion of the glutathione S-transferase epsilon 2 (GSTe2) gene. (a) Allele frequency distribution, (b) ML phylogenetic tree of GSTe2 gene fragment with previously recorded haplotypes in An. funestus s.s. across Africa, (c) Templeton-Crandall Sing (TCS) haplotype network. The rectangles and ovals represent haplotypes with the lines linking haplotypes showing a single mutation event. (d) Aligned sequence traces showing the mutational differences/polymorphic positions in the haplotypes detected in Kenyan An. longipalpis C/An. funestus s.s.* indicates polymorphic positions.