Abstract
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 vector Aedes aegypti and 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 of Ae. 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.
Highlights
Pathogens and parasites have the capacity to manipulate their hosts, enhancing the cycle of disease transmission [1,2,3]
The angle between the vectors “total activity” and “infection status” was less than 90 ̊ revealing a positive correlation between the two variables (Fig 1A), and suggesting that dengue-infected females (4.5–6 dpi) move differentially compared with their non-infected counterparts
This was confirmed following a permutational MANOVA analysis, which revealed that the proportion of observed variance between infected and non-infected mosquitoes was significantly explained by infection status (R2 = 0.8, df = 1, P = 0.014)
Summary
Pathogens and parasites have the capacity to manipulate their hosts, enhancing the cycle of disease transmission [1,2,3]. Similar effects have been shown in the primary hosts, in which infection results in changes in attraction and defensive behavior, as well as in the vascular and immune systems [8,9,10,11]. Such manipulation is increasingly being described for the interaction between blood feeding insects and their vertebrate hosts. This has significant implications for the epidemiology and control of vector-borne diseases [12,13]. Recent studies indicate that pathogens and parasites may target the many conserved pathways underlying particular behavioral traits to enhance transmission [28,29,30], suggesting that the olfactory system is affected through the change in chemosensory gene expression
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