Differential Gene Expression in the Heads of Behaviorally Divergent Culex pipiens Mosquitoes

SIMPLE SUMMARY: Host preference has profound impacts on the epidemiology of mosquito-borne disease transmission, yet much is still unknown about the molecular basis for these preferences. Here, we examined host preference in the West Nile virus vector, Culex pipiens. We examined human and avian landing rates for eight populations: five originating from above- and three from below-ground breeding and overwintering habitats. While above-ground populations tended to be biased toward avian landing and below-ground populations tended toward human landing, a range of behaviors was observed, consistent with other mosquito species. Patterns of differential expression and splice site variation were measured for one avian- and one human-seeking population as a first step toward identifying genes involved in regulation of blood feeding behaviors as well as differences in host preference. We conclude with a discussion of specific differentially expressed genes and their potential to influence host seeking behaviors of Cx. pipiens females. ABSTRACT: Host preferences of Cx. pipiens, a bridge vector for West Nile virus to humans, have the potential to drive pathogen transmission dynamics. Yet much remains unknown about the extent of variation in these preferences and their molecular basis. We conducted host choice assays in a laboratory setting to quantify multi-day human and avian landing rates for Cx. pipiens females. Assayed populations originated from five above-ground and three below-ground breeding and overwintering habitats. All three below-ground populations were biased toward human landings, with rates of human landing ranging from 69–85%. Of the five above-ground populations, four had avian landing rates of >80%, while one landed on the avian host only 44% of the time. Overall response rates and willingness to alternate landing on the human and avian hosts across multiple days of testing also varied by population. For one human- and one avian-preferring population, we examined patterns of differential expression and splice site variation at genes expressed in female heads. We also compared gene expression and splice site variation within human-seeking females in either gravid or host-seeking physiological states to identify genes that may regulate blood feeding behaviors. Overall, we identified genes with metabolic and regulatory function that were differentially expressed in our comparison of gravid and host-seeking females. Differentially expressed genes in our comparison of avian- and human-seeking females were enriched for those involved in sensory perception. We conclude with a discussion of specific sensory genes and their potential influence on the divergent behaviors of avian- and human-seeking Cx. pipiens.