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 mosquitoesemit 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.Platanthera | mosquitoes | Aedes aegypti | olfaction | nectar M osquitoes are important vectors of disease, such as dengue, malaria, or Zika, and are considered one of the deadliest animal on earth (1); for this reason, research has largely focused on mosquito-host interactions, and in particular, the mosquito's sensory responses to those hosts (2-5). Nectar feeding is one such aspect of mosquito sensory biology that has received comparatively less attention, despite being an excellent system in which to probe the neural bases of behavior (6). For instance, nectar and sugar feeding is critically important for both male and female mosquitoes, serving to increase their lifespan, survival rate, and reproduction, and for males, it is required for survival (6, 7).Mosquitoes are attracted to, and feed on, a variety of plant nectar sources, including those from flowers (8)(9)(10)(11)(12). Although most examples of mosquito-plant interactions have shown that mosquitoes contribute little in reproductive services to the plant (13), there are examples of mosquitoes being potential pollinators (9, 10, 14-17). However, few studies have identified the floral cues that serve to attract and mediate these decisions by the mosquitoes and how these behaviors influence pollination.The association between the Platanthera obtusata orchid and Aedes mosquitoes is one of the few examples that shows mosquitoes as effective pollinators (14-17) and thus provides investigators a unique opportunity to identify the sensory mechanisms th...

Not Just from Blood: Mosquito Nutrient Acquisition from Nectar Sources

“…plants they visit, they are the primary pollinator of the orchid Platanthera obtusata, and scents from this plant elicit strong olfactory and behavioral responses in Aedes species and An. stephensi [99].…”

Controlling mosquitoes with semiochemicals: a review

“…gambiae (s.s.) had a preference for specific plants (namely Mangifera indica, Delonix regia, Thevetia neriifolia, Senna didymobotrya, Senna siamea, Cassia sieberiana and Parthenium hysterophorus) [100,101]. Lahondère et al [102] demonstrated how orchid odours mediate mutualistic relationships between Ae. aegypti and the orchid Platanthera obtusata.…”

“…However, the level of these two attractants influence the attractiveness of the orchid to the mosquito. Higher levels of nonanal are released by the orchid species visited by the mosquito, whereas higher levels of lilac aldehyde were released by an orchid not visited by mosquitoes [102]. The identification of the semiochemicals responsible for the behavioural response (i.e.…”

Anthrax toxin component, Protective Antigen, protects insects from bacterial infections

“…While our study may help understand the mechanism through which insects tolerate anthrax, resulting in their greater opportunity to transmit the anthrax-causing bacteria, it further suggests that PA 20 could be used beneficially in agriculture. Since fruit flies and mosquitoes are known to act as plant pollinators [ 71 , 72 ], PA 20 should be further evaluated for its ability to reduce the sensitivity of pollinating insects to bacterial pathogens, such as Serratia and Bacillus species [ 73 – 75 ].…”