Dengue virus infection modifies mosquito blood-feeding behavior to increase transmission to the host

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 119; no. 3; pp. 1 - 9
• Main Authors: Xiang, Benjamin Wong Wei, Saron, Wilfried A. A., Stewart, James C., Hain, Arthur, Walvekar, Varsha, Missé, Dorothée, Thomas, Fréderic, Kini, R. Manjunatha, Roche, Benjamin, Claridge-Chang, Adam, St. John, Ashley L., Pompon, Julien
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 18.01.2022
• Series: From the Cover
• Subjects: Aedes - virology; Animal biology; Animals; Animals Behavior, Animal / physiology; Aquatic insects; Behavior; Behavior, Animal - physiology; Biological Sciences; Biting; Blood; Culicidae; Dengue - transmission; Dengue - virology; Dengue fever; Dengue Virus - physiology; Disease transmission; Ecology, environment; Epidemic models; Epidemiology; Feeding behavior; Feeding Behavior - physiology; Food and Nutrition; Host searching behavior; Host-Pathogen Interactions - physiology; Human health and pathology; Infections; Infectious diseases; Invertebrate Zoology; Life Sciences; Mathematical models; Mosquitoes; Multidisciplinary research; Multivariate Analysis; Santé publique et épidémiologie; Symbiosis; Vector-borne diseases; Viruses; epidemiology; transmission; blood-feeding behavior; dengue virus; mosquito; Dengue virus; Mosquito; Epidemiology; Blood-feeding behavior; Transmission
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.2117589119

Mosquito blood-feeding behavior is a key determinant of the epidemiology of dengue viruses (DENV), the most-prevalent mosquitoborne viruses. However, despite its importance, how DENV infection influences mosquito blood-feeding and, consequently, transmission remains unclear. Here, we developed a high-resolution, video-based assay to observe the blood-feeding behavior of Aedes aegypti mosquitoes on mice. We then applied multivariate analysis on the high-throughput, unbiased data generated from the assay to ordinate behavioral parameters into complex behaviors. We showed that DENV infection increases mosquito attraction to the host and hinders its biting efficiency, the latter resulting in the infected mosquitoes biting more to reach similar blood repletion as uninfected mosquitoes. To examine how increased biting influences DENV transmission to the host, we established an in vivo transmission model with immuno-competent mice and demonstrated that successive short probes result in multiple transmissions. Finally, to determine how DENV-induced alterations of host-seeking and biting behaviors influence dengue epidemiology, we integrated the behavioral data within a mathematical model. We calculated that the number of infected hosts per infected mosquito, as determined by the reproduction rate, tripled when mosquito behavior was influenced by DENV infection. Taken together, this multidisciplinary study details how DENV infection modulates mosquito blood-feeding behavior to increase vector capacity, proportionally aggravating DENV epidemiology. By elucidating the contribution of mosquito behavioral alterations on DENV transmission to the host, these results will inform epidemiological modeling to tailor improved interventions against dengue.