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The olfactory basis of orchid pollination by mosquitoes.

ABSTRACT: 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-diethyl-meta-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.

SUBMITTER: Lahondere C

PROVIDER: S-EPMC6955360 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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The olfactory basis of orchid pollination by mosquitoes.

Lahondère Chloé C Vinauger Clément C Okubo Ryo P RP Wolff Gabriella H GH Chan Jeremy K JK Akbari Omar S OS Riffell Jeffrey A JA

Proceedings of the National Academy of Sciences of the United States of America 20191223 1

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 ...[more]

PMID: 31871198

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Project description:The rostellum, a projecting part of the gynostemium in orchid flowers, separates the anther(s) from the stigma and thus commonly prevents auto-pollination. Nonetheless, as a modified (usually distal) portion of the median stigma lobe, the rostellum has been frequently invoked of having re-gained a stigmatic function in rare cases of orchid auto-pollination. Here it is shown that a newly discovered selfing variant of Madagascan Bulbophyllumbicoloratum has evolved a modified rostellum allowing the penetration of pollen tubes from in situ pollinia.Gynostemium micro-morphology and anatomy of selfing and outcrossing variants of B. bicoloratum was studied by using light and scanning electron microscopy and histological sections. Pollen tube growth in the selfing variant was further observed via X-ray computed microtomography (micro-CT), providing 3D reconstructions of floral tissues at a micron scale.Selfing variants possess a suberect ('displaced') rostellum rather than the conventional, erect type. Very early in anthesis, the pollinia of selfers are released from the anther and slide down onto the suberect rostellum, where pollen tube growth preferentially occurs through the non-vascularized, i.e. rear (adaxial) and (semi-) lateral parts. This penetrated tissue is comprised of a thin layer of elongate and loosely arranged cells, embedded in stigmatic exudates, as also observed in the stigmatic cavity of both selfing and outcrossing variants.Our results provide the first solid evidence of a stigmatic function for the rostellum in orchid flowers, thereby demonstrating for the first time the feasibility of the micro-CT technique for accurately visualizing pollen tube growth in flowering plants. Rostellum receptivity in B. bicoloratum probably uniquely evolved as an adaptation for reproductive assurance from an outcrossing ancestor possessing an erect (non-receptive) rostellum. These findings open up new avenues in the investigation of an organ that apparently re-gained its 'primordial function' of being penetrated by pollen tubes.

Project description:BackgroundMalaria control methods targeting indoor-biting mosquitoes have limited impact on vectors that feed and rest outdoors. Exploiting mosquito olfactory behaviour to reduce blood-feeding outdoors might be a sustainable approach to complement existing control strategies. Methodologies that can objectively quantify responses to odour under realistic field conditions and allow high-throughput screening of many compounds are required for development of effective odour-based control strategies.MethodsThe olfactory responses of laboratory-reared Anopheles gambiae in a semi-field tunnel and A. arabiensis females in an outdoor field setting to three stimuli, namely whole human odour, a synthetic blend of carboxylic acids plus carbon dioxide and CO(2) alone at four distances up to 100 metres were measured in two experiments using three-chambered taxis boxes that allow mosquito responses to natural or experimentally-introduced odour cues to be quantified.ResultsTaxis box assays could detect both activation of flight and directional mosquito movement. Significantly more (6-18%) A. arabiensis mosquitoes were attracted to natural human odour in the field up to 30 metres compared to controls, and blended synthetic human odours attracted 20% more A. gambiae in the semi-field tunnel up to 70 metres. Whereas CO(2) elicited no response in A. arabiensis in the open field, it was attractive to A. gambiae up to 50 metres (65% attraction compared to 36% in controls).ConclusionsWe have developed a simple reproducible system to allow for the comparison of compounds that are active over medium- to long-ranges in semi-field or full-field environments. Knowing the natural range of attraction of anopheline mosquitoes to potential blood sources has substantial implications for the design of malaria control strategies, and adds to the understanding of olfactory behaviour in mosquitoes. This experimental strategy could also be extended from malaria vectors to other motile arthropods of medical, veterinary and agricultural significance.

Dataset Information

The olfactory basis of orchid pollination by mosquitoes.

Publications

The olfactory basis of orchid pollination by mosquitoes.

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