The Genetic Basis of Host Preference and Resting Behavior in the Major African Malaria Vector, Anopheles arabiensis

Abstract

Malaria transmission is dependent on the propensity of Anopheles mosquitoes to bite humans (anthropophily) instead of other dead end hosts. Recent increases in the usage of Long Lasting Insecticide Treated Nets (LLINs) in Africa have been associated with reductions in highly anthropophilic and endophilic vectors such as Anopheles gambiae s.s., leaving species with a broader host range, such as Anopheles arabiensis, as the most prominent remaining source of transmission in many settings. An. arabiensis appears to be more of a generalist in terms of its host choice and resting behavior, which may be due to phenotypic plasticity and/or segregating allelic variation. To investigate the genetic basis of host choice and resting behavior in An. arabiensis we sequenced the genomes of 23 human-fed and 25 cattle-fed mosquitoes collected both in-doors and out-doors in the Kilombero Valley, Tanzania. We identified a total of 4,820,851 SNPs, which were used to conduct the first genome-wide estimates of “SNP heritability” for host choice and resting behavior in this species. A genetic component was detected for host choice (human vs cow fed; permuted P = 0.002), but there was no evidence of a genetic component for resting behavior (indoors versus outside; permuted P = 0.465). A principal component analysis (PCA) segregated individuals based on genomic variation into three groups which were characterized by differences at the 2Rb and/or 3Ra paracentromeric chromosome inversions. There was a non-random distribution of cattle-fed mosquitoes between the PCA clusters, suggesting that alleles linked to the 2Rb and/or 3Ra inversions may influence host choice. Using a novel inversion genotyping assay, we detected a significant enrichment of the standard arrangement (non-inverted) of 3Ra among cattle-fed mosquitoes (N = 129) versus all non-cattle-fed individuals (N = 234; χ2, p = 0.007). Thus, tracking the frequency of the 3Ra in An. arabiensis populations may be of use to infer selection on host choice behavior within these vector populations; possibly in response to vector control. Controlled host-choice assays are needed to discern whether the observed genetic component has a direct relationship with innate host preference. A better understanding of the genetic basis for host feeding behavior in An. arabiensis may also open avenues for novel vector control strategies based on driving genes for zoophily into wild mosquito populations.

Pollutants and insecticides drive local adaptation in African malaria mosquitoes

“…In addition to increased resistance, large-scale exposure of vector populations to insecticidetreated bed nets in Africa is also correlated with changes in species distribution and behavioral shifts (Bøgh et al 1998;Derua et al 2012;Moiroux et al 2012;Mwangangi et al 2013;Sokhna et al 2013). However, so far, despite ongoing efforts, there is no evidence that these changes can lead to genetic clustering or the creation of cryptic populations within species (e.g., Main et al 2016). Our data show that the genetic differentiation within the An.…”

Linked-read sequencing identifies abundant microinversions and introgression in the arboviral vector Aedes aegypti

“…Mosquitoes are often found as complexes of closely related species that are distinguished by fixed inversions but maintain some degree of gene flow [14], while structured populations at the subspecies level have also been posited based on differing inversion polymorphisms [15]. Chromosomal inversions have also been directly associated with phenotypes that are important for vector competence: thermal tolerance underlying range expansion [16][17][18], feeding behavior [19,20], oviposition site preferences [21,22], insecticide resistance [23], and immune response to parasites [24,25].…”

Recombination Suppression is Unlikely to Contribute to Speciation in SympatricHeliconiusButterflies

“…Arabidopsis thaliana [19] and maize [20]) (Table 1). Traits associated with chromosomal inversions include plumage and behavioural traits associated with alternative mating strategies in the ruff Philomachus pugnax [21,22], flowering time and morphological traits in Mimulus guttatus [23,24], colony organisation in fire ants [25], insecticide resistance, host preference and resting behaviour in Anopheles [26,27,28] and many traits in Drosophila [29]. The lack of recombination between inversion haplotypes is thought to maintain multiple co-adapted alleles in complete association, facilitating local adaptation and the maintenance of polymorphism.…”