Modulation of Host Learning in Aedes aegypti Mosquitoes

• Published in: Current biology Vol. 28; no. 3; pp. 333 - 344.e8
• Main Authors: Vinauger, Clément, Lahondère, Chloé, Wolff, Gabriella H., Locke, Lauren T., Liaw, Jessica E., Parrish, Jay Z., Akbari, Omar S., Dickinson, Michael H., Riffell, Jeffrey A.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 05.02.2018
• Subjects: Aedes - physiology; Aedes aegypti; Animals; aversive conditioning; Avoidance Learning; Chickens - physiology; Conditioning, Classical; disease vector; dopamine; Dopamine - physiology; Feeding Behavior; Female; Humans; mosquito; neuromodulation; Odorants; olfactory learning; Olfactory Perception; Rats - physiology; neuromodulation; aversive conditioning; olfactory learning; disease vector; Aedes aegypti; dopamine; mosquito
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2017.12.015

How mosquitoes determine which individuals to bite has important epidemiological consequences. This choice is not random; most mosquitoes specialize in one or a few vertebrate host species, and some individuals in a host population are preferred over others. Mosquitoes will also blood feed from other hosts when their preferred is no longer abundant, but the mechanisms mediating these shifts between hosts, and preferences for certain individuals within a host species, remain unclear. Here, we show that olfactory learning may contribute to Aedes aegypti mosquito biting preferences and host shifts. Training and testing to scents of humans and other host species showed that mosquitoes can aversively learn the scent of specific humans and single odorants and learn to avoid the scent of rats (but not chickens). Using pharmacological interventions, RNAi, and CRISPR gene editing, we found that modification of the dopamine-1 receptor suppressed their learning abilities. We further show through combined electrophysiological and behavioral recordings from tethered flying mosquitoes that these odors evoke changes in both behavior and antennal lobe (AL) neuronal responses and that dopamine strongly modulates odor-evoked responses in AL neurons. Not only do these results provide direct experimental evidence that olfactory learning in mosquitoes can play an epidemiological role, but collectively, they also provide neuroanatomical and functional demonstration of the role of dopamine in mediating this learning-induced plasticity, for the first time in a disease vector insect. [Display omitted] •Aversive learning by mosquitoes suppresses responses to human hosts•Mosquitoes can learn the association between mechanical shock and certain odorants•CRISPR/Cas9 modification of the dopamine-1 receptor prevents learning•Dopamine causes heterogeneous modulation of antennal lobe neurons Mosquitoes show an ability to avoid defensive hosts, but the mechanisms mediating these shifts in host preferences are unclear. Vinauger et al. show that Aedes aegypti mosquitoes rapidly learn host odors and that learning is dependent on the dopamine-1 receptor. Understanding the mechanisms of learning may provide new tools for mosquito control.