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Research article - Peer-reviewed, 2020

Dengue infection modulates locomotion and host seeking in Aedes aegypti

Tallon, Anais K.; Lorenzo, Marcelo G.; Moreira, Luciano A.; Martinez Villegas, Luis E.; Hill, Sharon Rose; Ignell, Rickard

Abstract

Author summary The mosquitoAedes aegyptiis a major urban vector for human pathogens, including dengue, the most rapidly-spreading infectious disease globally. We show that one of the four strains of the dengue virus differentially, and inversely, affects the locomotion and odour-mediated behaviour of femaleAedes aegypti. During the early stages after infection, female mosquitoes show an increased locomotion activity suggesting that the virus likely promotes mosquito dispersion and increases its spatial exploration. In contrast, in the later infective stages, dengue infection modulates the mosquito's host-seeking capacity, by enhancing the physiological and behavioural sensitivity to human odors, thus increasing the risk of virus transmission. At this stage of infection, neural signalling gene expression is enhanced, providing a mechanism for the increased sensitivity to human odor, while genes involved in chemosensation and neuromodulation are likely playing a secondary role. A better understanding of alterations of mosquito host-seeking behavior upon pathogen infection will contribute to the development of novel control strategies against vector borne diseases.Pathogens may manipulate their human and mosquito hosts to enhance disease transmission. Dengue, caused by four viral serotypes, is the fastest-growing transmissible disease globally resulting in 50-100 million infections annually. Transmission of the disease relies on the interaction between humans and the vectorAedes aegyptiand is largely dependent on the odor-mediated host seeking of female mosquitoes. In this study, we use activity monitors to demonstrate that dengue virus-1 affects the locomotion and odor-mediated behavior ofAe.aegypti, reflecting the progression of infection within the mosquito. Mosquitoes 4-6 days post-infection increase locomotion, but do not alter their odor-driven host-seeking response. In contrast, females 14-16 days post-infection are less active, yet more sensitive to human odors as assessed by behavioral and electrophysiological assays. Such an increase in physiological and behavioral sensitivity is reflected by the antennal-specific increase in abundance of neural signaling transcripts in 14 days post-infection females, as determined by transcriptome analysis. This suggests that the sensitivity of the mosquito peripheral olfactory system is altered by the dengue virus by enhancing the overall neural responsiveness of the antenna, rather than the selective regulation of chemosensory-related genes. Our study reveals that dengue virus-1 enhances vector-related behaviors in the early stages post-infection that aid in avoiding predation and increasing spatial exploration. On the other hand, at the later stages of infection, the virus enhances the host-seeking capacity of the vector, thereby increasing the risk of virus transmission. A potential mechanism is discussed.

Published in

PLoS Neglected Tropical Diseases
2020, volume: 14, number: 9, article number: e0008531
Publisher: PUBLIC LIBRARY SCIENCE

Authors' information

Tallon, Anaïs
Swedish University of Agricultural Sciences, Department of Plant Protection Biology
Lorenzo, Marcelo G.
Fundacao Oswaldo Cruz
Moreira, Luciano A.
Fundacao Oswaldo Cruz
Martinez Villegas, Luis E.
Fundacao Oswaldo Cruz
Swedish University of Agricultural Sciences, Department of Plant Protection Biology
Swedish University of Agricultural Sciences, Department of Plant Protection Biology

UKÄ Subject classification

Microbiology in the medical area

Publication Identifiers

DOI: https://doi.org/10.1371/journal.pntd.0008531

URI (permanent link to this page)

https://res.slu.se/id/publ/108158