Olfaction, experience and neural mechanisms underlying mosquito host preference

Wolff, Gabriella H.; Riffell, Jeffrey A.

doi:10.1242/jeb.157131

Cited by 66 publications

(68 citation statements)

References 145 publications

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“…There are over 3500 species of mosquitoes that exhibit remarkable diversity in feeding preferences, from flowers to humans and other mammals, and even frogs or birds 1,2 . Despite their often specific preferences for blood-hosts, mosquitoes exhibit a high degree of behavioral flexibility 3 . One mechanism for this flexibility is their capacity to learn and modify feeding preferences.…”

Section: Introductionmentioning

confidence: 99%

Neuromodulation and Differential Learning Across Mosquito Species

Wolff

Lahondère

Vinauger

et al. 2019

Preprint

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Mosquitoes can learn to change their host-feeding behaviors, such as shifting activity times to avoid bednets or switching from biting animals to biting humans, leading to the transfer of zoonotic diseases. Dopamine is critical for insect learning, but its role in the antennal lobe remains unclear, and it is unknown whether different mosquito species learn the same odor cues. We assayed aversive olfactory learning and dopaminergic brain innervation in four mosquito species with different host preferences and report here that they differentially learn odors salient to their preferred host and innervation patterns vary across species. Using genetically-encoded GCaMP6s Aedes aegypti, we mapped odor-evoked antennal lobe activity and report that glomeruli tuned to “learnable” odors have significantly higher dopaminergic innervation. Changes in dopamine expression in the antennal lobes of diverse invertebrate species may be an evolutionary mechanism to adapt olfactory learning circuitry without changing brain structure and for mosquitoes an ability to adapt to other hosts when their preferred are no longer present.

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Section: Introductionmentioning

confidence: 99%

Neuromodulation and Differential Learning Across Mosquito Species

Wolff

Lahondère

Vinauger

et al. 2019

Preprint

Self Cite

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“…This behavior is often underappreciated when compared with blood-feeding because it is during the latter that transmission of pathogens can occur. A few mosquito genera feed solely from plant sources [3], while in hematophagous (see Glossary) species, females consume sugar sources as well as blood. If deprived of sugar, males typically die within 4 days of eclosion [4].…”

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Not Just from Blood: Mosquito Nutrient Acquisition from Nectar Sources

Barredo

DeGennaro

2020

Trends in Parasitology

117

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Anthropophilic female mosquitoes are well known for their strong attraction to human hosts, but plant nectar is a common energy source in their diets. When sugar sources are scarce, female mosquitoes of some species can compensate by taking larger and more frequent blood meals. Male mosquitoes are exclusively dependent on plant nectar or alternative sugar sources. Plant preference is likely driven by an innate attraction that may be enhanced by experience, as mosquitoes learn to recognize available sugar rewards. Nectar-seeking involves the integration of at least three sensory systems: olfaction, vision and taste. The prevention of vector-borne illnesses, the determination of the mosquitoes' ecological role, and the design of efficient sugar-baited traps will all benefit from understanding the molecular basis of nectar-seeking. Plant Nectar Is a Common Nutrition Source across Mosquito SpeciesNectar-feeding constitutes an important source of nutrition for adult mosquitoes of both sexes, particularly males, which feed exclusively from plant nectar and require frequent sugar intake for survival [1,2]. This behavior is often underappreciated when compared with blood-feeding because it is during the latter that transmission of pathogens can occur. A few mosquito genera feed solely from plant sources [3], while in hematophagous (see Glossary) species, females consume sugar sources as well as blood. If deprived of sugar, males typically die within 4 days of eclosion [4]. Moreover, lacking the energy reserves needed for flying and copulation that come from a sugar meal, males are unlikely to achieve reproductive success [1]. Although females are less susceptible to rapid mortality caused by sugar deprivation, their survival rate and fecundity can be compromised by reduced energy reserves [1,4]. The sensory cues that enable nectar-feeding include odors [1,2], tastants [5], and visual stimuli [6,7], but the molecular mechanisms of how these cues are perceived, as well as their relative contribution to the detection of a nectar source, are poorly understood (Figure 1). This review highlights the role of sugar feeding in the life cycle of mosquitoes, the plant sources they prefer, the volatiles that attract them, and the contribution of vision, olfaction, and gustation to this behavior.

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“…Malaria-transmitting mosquitoes are often described as primary or secondary vectors with this categorisation informed, in part, by their level of anthropophagy as indicated by their HBI. Owing to the influences of different environmental settings, however, studies reporting HBI for the same vector species demonstrate considerable variability 21,[23][24][25] . We recently showed that the HBI of Anopheles coluzzii varied significantly over an extraordinarily small spatial scale, thus demonstrating how localised host biting behaviour can be 26 .…”

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Evidence of extrinsic factors dominating intrinsic blood host preferences of major African malaria vectors

Orsborne

Mohammed

Jeffries

et al. 2020

Sci Rep

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one of the key determinants of a haematophagous vector's capacity to transmit pathogens is its selection of which host to secure a blood meal from. This choice is influenced by both intrinsic (genetic) and extrinsic (environmental) factors, but little is known of their relative contributions. Blood fed Anopheles mosquitoes were collected from a malaria endemic village in Ghana. collections were conducted across a range of different host availabilities and from both indoor and outdoor locations. these environmental factors were shown to impact dramatically the host choice of caught malaria vectors: mosquitoes caught indoors were ten-fold more likely to have sourced their blood meal from humans; and a halving in odds of being human-fed was found for mosquitoes caught only 25 m from the centre of the village. For the first time, we demonstrate that anthropophagy was better explained by extrinsic factors (namely, local host availability and indoor/outdoor trapping location) than intrinsic factors (namely, the (sibling) species of the mosquito caught) (respective Akaike information criterion estimates: 243.0 versus 359.8). Instead of characterizing biting behaviour on a taxonomic level, we illustrate the importance of assessing local entomology. Accounting for this behavioural plasticity is important, both in terms of measuring effectiveness of control programmes and in informing optimal disease control strategies.Mosquitoes are responsible for the transmission of multiple human pathogens with malaria the most prominent of the resulting diseases. Malaria is transmitted by the bite of several Anopheles mosquito species when infected with Plasmodium parasites. As the successful transmission of the parasite requires two successful bites (one for the mosquito to become infected and one for the parasite to be transmitted to the human host), the mosquito's choice of which host species to bite has an exaggerated, non-linear impact on malaria transmission intensity 1 . The way in which host availability impacts the choice of host is largely unknown despite the dramatic impact it has on transmission and control of vector-borne diseases of diverse aetiology 2 . Similarly little is known of the short-and long-term impacts of different control methods on host choice.The introduction of indoor residual spraying and insecticidal nets has resulted in a change in the biting behaviour of major malaria vectors with many mosquito species seeking a higher proportion of blood meals outdoors 3-6 and/or from non-human hosts 7-10 . Coupled with increasing rates of insecticide resistance 11 , these behavioural changes indicate potential inadequacies of current leading vector-control tools to target outdoor biting and, correspondingly, sustained residual malaria transmission [12][13][14][15][16][17][18][19] . Therefore, understanding this behaviour is becoming increasingly important when implementing vector control strategies.In the field, which host is ultimately bitten is a complex balance between intrinsic (genetic) and extrinsic (environme...

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Olfaction, experience and neural mechanisms underlying mosquito host preference

Cited by 66 publications

References 145 publications

Neuromodulation and Differential Learning Across Mosquito Species

Neuromodulation and Differential Learning Across Mosquito Species

Not Just from Blood: Mosquito Nutrient Acquisition from Nectar Sources

Evidence of extrinsic factors dominating intrinsic blood host preferences of major African malaria vectors

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