The olfactory basis of orchid pollination by mosquitoes

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 117; no. 1; pp. 708 - 716
• Main Authors: Lahondère, Chloé, Vinauger, Clément, Okubo, Ryo P., Wolff, Gabriella H., Chan, Jeremy K., Akbari, Omar S., Riffell, Jeffrey A.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 07.01.2020
• Series: PNAS Plus
• Subjects: Aedes - physiology; Aedes aegypti; Aldehydes; Animals; Antennal lobe; Appetitive Behavior - drug effects; Appetitive Behavior - physiology; Arthropod Antennae - cytology; Arthropod Antennae - physiology; Attraction; Biological Sciences; Brain - physiology; Calcium; Calcium imaging; Carbohydrates; Culicidae; DEET; DEET - pharmacology; Ecological effects; Female; Glomerulus; Host searching behavior; Information processing; Insect Repellents - pharmacology; Male; Mosquito Vectors - drug effects; Mosquito Vectors - physiology; Mosquitoes; Mutualism; Nectar; Neuroimaging; Nonanal; Odorants; Olfactory glomeruli; Olfactory Perception - drug effects; Olfactory Perception - physiology; Olfactory Receptor Neurons - physiology; Orchidaceae - physiology; Plant reproduction; Platanthera obtusata; PNAS Plus; Pollination; Pollination - drug effects; Pollination - physiology; Pollinators; Repellents; Scents; Vectors; mosquitoes; olfaction; Aedes aegypti; Platanthera; nectar
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1910589117

Mosquitoes are important vectors of disease and require sources of carbohydrates for reproduction and survival. Unlike host-related behaviors of mosquitoes, comparatively less is understood about the mechanisms involved in nectar-feeding decisions, or how this sensory information is processed in the mosquito brain. Here we show that Aedes spp. mosquitoes, including Aedes aegypti, are effective pollinators of the Platanthera obtusata orchid, and demonstrate this mutualism is mediated by the orchid’s scent and the balance of excitation and inhibition in the mosquito’s antennal lobe (AL). The P. obtusata orchid emits an attractive, nonanal-rich scent, whereas related Platanthera species—not visited by mosquitoes—emit scents dominated by lilac aldehyde. Calcium imaging experiments in the mosquito AL revealed that nonanal and lilac aldehyde each respectively activate the LC2 and AM2 glomerulus, and remarkably, the AM2 glomerulus is also sensitive to N,N-diethylmeta-toluamide (DEET), a mosquito repellent. Lateral inhibition between these 2 glomeruli reflects the level of attraction to the orchid scents. Whereas the enriched nonanal scent of P. obtusata activates the LC2 and suppresses AM2, the high level of lilac aldehyde in the other orchid scents inverts this pattern of glomerular activity, and behavioral attraction is lost. These results demonstrate the ecological importance of mosquitoes beyond operating as disease vectors and open the door toward understanding the neural basis of mosquito nectar-seeking behaviors.