Mosquito brains encode unique features of human odour to drive host seeking.

A globally invasive form of the mosquito Aedes aegypti specializes in biting humans, making it an efficient disease vector1. Host-seeking female mosquitoes strongly prefer human odour over the odour of animals2,3, but exactly how they distinguish between the two is not known. Vertebrate odours are complex blends of volatile chemicals with many shared components4-7, making discrimination an interesting sensory coding challenge. Here we show that human and animal odours evoke activity in distinct combinations of olfactory glomeruli within the Ae. aegypti antennal lobe. One glomerulus in particular is strongly activated by human odour but responds weakly, or not at all, to animal odour. This human-sensitive glomerulus is selectively tuned to the long-chain aldehydes decanal and undecanal, which we show are consistently enriched in human odour and which probably originate from unique human skin lipids. Using synthetic blends, we further demonstrate that signalling in the human-sensitive glomerulus significantly enhances long-range host-seeking behaviour in a wind tunnel, recapitulating preference for human over animal odours. Our research suggests that animal brains may distil complex odour stimuli of innate biological relevance into simple neural codes and reveals targets for the design of next-generation mosquito-control strategies.

Exploring natural odour landscapes: A case study with implications for human-biting insects.

The natural world is full of odours-blends of volatile chemicals emitted by potential sources of food, social partners, predators, and pathogens. Animals rely heavily on these signals for survival and reproduction. Yet we remain remarkably ignorant of the composition of the chemical world. How many compounds do natural odours typically contain? How often are those compounds shared across stimuli? What are the best statistical strategies for discrimination? Answering these questions will deliver crucial insight into how brains can most efficiently encode olfactory information. Here, we undertake the first large-scale survey of vertebrate body odours, a set of stimuli relevant to blood-feeding arthropods. We quantitatively characterize the odour of 64 vertebrate species (mostly mammals), representing 29 families and 13 orders. We confirm that these stimuli are complex blends of relatively common, shared compounds and show that they are much less likely to contain unique components than are floral odours-a finding with implications for olfactory coding in blood feeders and floral visitors. We also find that vertebrate body odours carry little phylogenetic information, yet show consistency within a species. Human odour is especially unique, even compared to the odour of other great apes. Finally, we use our newfound understanding of odour-space statistics to make specific predictions about olfactory coding, which align with known features of mosquito olfactory systems. Our work provides one of the first quantitative descriptions of a natural odour space and demonstrates how understanding the statistics of sensory environments can provide novel insight into sensory coding and evolution.

Quantifying Aedes aegypti Host Odor Preference Using a Two-Port Olfactometer.

Blood-feeding mosquitoes are a leading threat to global public health-vectoring dangerous infections including Zika, dengue, and malaria. Mosquitoes identify and target hosts for blood meals by using visual, thermal, and chemical cues. Here we describe an assay for measuring odor-based host-preference behavior-that is, the preferential approach toward one host over another based on differences in the volatile compounds they emit. The assay can be adapted for use with diverse odor sources, from live animals and their breath to odor-scented sleeves with controlled amounts of CO2 Mosquitoes in this assay fly upwind to within 30 cm of the odor source and then enter a small trap. We therefore believe this assay best replicates medium- to short-range host-seeking, when females approach and are preparing to land on a host animal. We also find that relative response in a two-choice test shows less trial-to-trial variation than the absolute number of responsive mosquitoes, which appears more sensitive to exogenous factors such as rearing conditions. This assay has been used to better understand mosquito host-seeking decisions, which can provide fundamental insight into the brain and behavior as well as information useful for the design of novel vector control strategies.

An Assay for Quantifying Aedes aegypti Host Odor Preference Using a Two-Port Olfactometer.

Female mosquitoes use odor cues to locate hosts for blood meals and are often more likely to approach the odor of certain species or individuals over others. Here, we describe an assay for measuring such odor-based host preference. This assay uses a two-port olfactometer and can be adapted to study a wide variety of odor sources including live hosts, host-scented nylon sleeves or host hair samples, and single odorants or odorant blends.