Neuromodulation and differential learning across mosquito species

Abstract

Mosquitoes can change their feeding behaviours based on past experiences, such as shifting from biting animals to biting humans or avoiding defensive hosts (Wolff & Riffell 2018 J. Exp. Biol. 221 , jeb157131. ( doi:10.1242/jeb.157131 )). Dopamine is a critical neuromodulator for insects, allowing flexibility in their feeding preferences, but its role in the primary olfactory centre, the antennal lobe (AL), remains unclear (Vinauger et al. 2018 Curr. Biol. 28 , 333–344.e8. ( doi:10.1016/j.cub.2017.12.015 )). It is also unknown whether mosquitoes can learn some odours and not others, or whether different species learn the same odour cues. We assayed aversive olfactory learning in four mosquito species with different host preferences, and found that they differentially learn odours salient to their preferred host. Mosquitoes that prefer humans learned odours found in mammalian skin, but not a flower odour, and a nectar-feeding species only learned a floral odour. Comparing the brains of these four species revealed significantly different innervation patterns in the AL by dopaminergic neurons. Calcium imaging in the Aedes aegypti AL and three-dimensional image analyses of dopaminergic innervation show that glomeruli tuned to learnable odours have significantly higher dopaminergic innervation. Changes in dopamine expression in the insect AL may be an evolutionary mechanism to adapt olfactory learning circuitry without changing brain structure and confer to mosquitoes an ability to adapt to new hosts.