Population genomic evidence of a putative 'far-west' African cryptic taxon in the Anopheles gambiae complex

Abstract

The two main Afrotropical malaria vectors - Anopheles coluzzii and An. gambiae - are genetically distinct and reproductively isolated across West Africa. However, populations at the western extreme of their range are assigned as "intermediate" between the two species by whole genome sequence (WGS) data, and as hybrid forms by conventional molecular diagnostics. By exploiting WGS data from 1190 specimens collected across west Africa via the Anopheles gambiae 1000 Genomes network, we identified a putative taxon in the far-west (provisionally named Bissau molecular form), which did not arise by admixture but rather may have originated at the same time as the split between An. coluzzii and An. gambiae. Intriguingly, this taxon lacks insecticide resistance mechanisms commonly observed in the two main species. These findings lead to a change of perspective on malaria vector species in the far-west region with potential for epidemiological implications, and a new challenge for genetic-based mosquito control approaches.

Fig. 1. Genomic structure of Ag1000G Ag3.0 Anopheles gambiae s.l. from West and Far-West Africa.

A Distribution and numbers of 1190 Ag1000G Ag3.0 individuals included in the analysis (right) with focus on the Far-West region (left), according to the Ag1000G Consortium^,. B Principal component analysis based on SNPs on chromosome-X, -3 and -2. Circles = Anopheles coluzzii and Anopheles gambiae; crosses = Far-West individuals. C ADMIXTURE Bayesian ancestry most parsimonious models for chromosome-X (K = 3) and chromosome-3 (K = 3). Anopheles coluzzii: BFcol (Burkina Faso), CIcol (Côte d’Ivoire), GHcol (Ghana), GNcol (Guinea), MAcol (Mali); An. gambiae: BFgam (Burkina Faso), GHgam (Ghana), GNgam (Guinea), GWgam (Guinea-Bissau), MAgam (Mali).

Fig. 2. Genetic divergence and diversity among Far-West populations (gcx1-GM, gcx1-GW, gcx2; Ag1000G, Ag3.0) and western Anopheles gambiae (GA) and An. coluzzii (CO) populations in the euchromatic region of chromosome-3.

Each population was randomly downsampled to 30 individuals (GNcol and GWgam populations were omitted owing to small sampling size). A Pairwise F_ST matrix; B Genetic diversity statistics: π, Tajima’s D, Watterson theta.

Fig. 3. Patterns of west-African Ag1000G (Ag3.0) Anopheles gambiae s.l. population splits and mixtures as inferred by TreeMix based on SNPs in the euchromatic region of chromosome-3.

Branch lengths are proportional to the evolutionary change (the drift parameter) and terminal nodes were labelled with clusters codes. Migration edges were coloured according to migration weight.

Fig. 4. Demographic models explored by ∂a∂i analysis to test different hypotheses for gcx1 origin.

1 gcx1-GM originated from admixture between CO and GA (‘admix_origin_no_mig’ model); 2 gcx1-GM split simultaneously from CO and GA (‘sim_split_nomig’ model), the best supported model depicted by the analysis; 3 gcx1-GM stemmed from GA (3a) or CO (3b) (‘split_nomig’ model).

Fig. 5. gcx1-GM vs Anopheles gambiae markers plot.

Rows represent individual mosquitoes (grouped by population) and columns represent SNPs (grouped by chromosome arm). Approximate chromosomal position is given below the graph. Colours represent gcx1-GM related (Purple), An. gambiae (GA; Green), gcx1-GM/GA (cyan) heterozygous genotypes; Missing genotypes in black. The column at the far right shows the individual allelic percentage (A.P.).