The genetic basis of host preference and resting behavior in the major African malaria vector, Anopheles arabiensis

Main, B. J. et al. (2016) The genetic basis of host preference and resting behavior in the major African malaria vector, Anopheles arabiensis. PLoS Genetics, 12(9), e1006303. (doi:10.1371/journal.pgen.1006303) (PMID:27631375) (PMCID:PMC5025075)

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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. 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.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Kreppel, Dr Katharina and Ferguson, Professor Heather
Authors: Main, B. J., Lee, Y., Ferguson, H.M., Kreppel, K.S., Kihonda, A., Govella, N. J., Collier, T. J., Cornel, A.J., Eskin, E., Kang, E.Y., Nieman, C.C., Weakley, A.M., and Lanzaro, G.C.
College/School:College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
Journal Name:PLoS Genetics
Publisher:Public Library of Science
ISSN:1553-7390
ISSN (Online):1553-7404
Copyright Holders:Copyright © 2016 Main et al.
First Published:First published in PLoS Genetics 12(9): e1006303
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
511181Environmental and genetic basis of malaria transmitting behaviours in Anopheles arabiensis mosquitoesHeather FergusonNational Institute of Health (NIH-GA)1R01AI085175-01RI BIODIVERSITY ANIMAL HEALTH & COMPMED
511182Environmental and genetic basis of malaria transmitting behaviours in Anopheles arabiensis mosquitoesHeather FergusonNational Institute of Health (NIH-GA)201015556-1 UGRI BIODIVERSITY ANIMAL HEALTH & COMPMED
511183Environmental and genetic basis of malaria transmitting behaviours in Anopheles arabiensis mosquitoesHeather FergusonNational Institute of Health (NIH-GA)201015556-1 UGRI BIODIVERSITY ANIMAL HEALTH & COMPMED
511184Environmental and genetic basis of malaria transmitting behaviours in Anopheles arabiensis mosquitoesHeather FergusonNational Institute of Health (NIH-GA)201015556-1 UGRI BIODIVERSITY ANIMAL HEALTH & COMPMED
511185Environmental and genetic basis of malaria transmitting behaviours in Anopheles arabiensis mosquitoesHeather FergusonNational Institute of Health (NIH-GA)201015556-1 UGRI BIODIVERSITY ANIMAL HEALTH & COMPMED