Olfactory learning and chemical ecology of olfaction in disease vector mosquitoes: a life history perspective

Lutz, Eleanor K.; Lahondère, Chloé; Vinauger, Clément; Riffell, Jeffrey A.

doi:10.1016/j.cois.2017.03.002

Cited by 45 publications

(53 citation statements)

References 95 publications

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“…Despite being repulsive during baseline conditions, skatole at 100 μg/l could be attractive for gravid Aedes aegypti females if previously reared in water containing this chemical. These results verified that early experience of mosquitoes at aquatic stage could have an impact in the adult mosquito life 7,43 . As previously reported 15,16 for Anopheles malaria vectors, the dissociation between oviposition site, which is often scarce, and remote food source implies needs for long or mid-range orientation and would necessitate “some form of learnt behaviour” 15 .…”

Section: Discussionsupporting

confidence: 78%

Dengue virus infection changesAedes aegyptioviposition olfactory preferences

Gaburro

Paradkar

Klein

et al. 2018

Preprint

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14Aedes aegypti mosquitoes, main vectors for numerous flaviviruses, have olfactory 15 preferences and are capable of olfactory learning especially when seeking their required 16 environmental conditions to lay their eggs. In this study, we showed that semiochemical 17 conditions during Aedes aegypti larval rearing affected future female choice for oviposition: 18 water-reared mosquitoes preferred to lay eggs in water or p-cresol containers, while skatole 19 reared mosquitoes preferred skatole sites. Using two independent behavioural assays, we 20 showed that this skatole preference was lost in mosquitoes infected with dengue virus. Viral 21 RNA was extracted from infected female mosquito heads, and an increase of virus load was 22 detected from 3 to 10 days post infection, indicating replication in the insect head and 23 possibly in the central nervous system. Expression of selected genes, potentially implied in 24 olfactory learning processes, were also altered during dengue infection. Based on these 25 results, we hypothesise that dengue virus infection alters gene expression in the mosquito's 26 head and is associated with a loss of olfactory preferences, possibly modifying oviposition 27 site choice of female mosquitoes.It is important for insects to identify and localize sites for food resources, mating and egg 30 laying to successfully survive and reproduce. It is generally known that insects, including 31 mosquitoes, are capable of information retention, acquired either during larval development, 32 hatching or foraging, and that new information could influence their behaviour 1 . In this 33 study, we define the term of "olfactory learning" as change of olfactory preferences induced 34 by exposure to odour. 35In insect vectors, such as mosquitoes, learning from its own experience could influence the 36 vector behaviour, such as the potential preferences in vector-host interactions 2,3 , which can 37 be of great interest to epidemiologists. Mosquitoes are also capable of associative learning, 38 which is the process of learning the association between two stimuli 4 , in the context of 39 feeding 5 , or responding to odour cues 6-10 . Also, learning in mosquito vectors could 40 significantly influence virus transmission through host contact and survival rate 9 . In nature, 41 environments are constantly subjected to changes, especially chemical cues involved in 42 potential food or oviposition site 11 . In order to respond to such rapid change and improve its 43 searching efficiency, a vector needs to adapt by learning to respond to odour cues 6 . The 44 mosquito experience to olfactory cues from larval, pupal or early adult vector environment 45 could influence its behaviour. 46After a blood meal from a host, female mosquitoes look for suitable oviposition sites to 47 guarantee success of the offspring 12 . Among different factors, chemical cues play a key role 48 in determining location for mosquito to lay its eggs 13,14 . The chemical signature of an ideal 49 oviposition site is not certai...

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Section: Discussionsupporting

confidence: 78%

Dengue virus infection changesAedes aegyptioviposition olfactory preferences

Gaburro

Paradkar

Klein

et al. 2018

Preprint

View full text Add to dashboard Cite

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“…To detect and locate suitable hosts, mosquitoes rely on multiple sensory cues, including olfactory, visual, and thermosensory information [1][2][3][4][5] while flying through a dynamic environment [6]. Whereas responses to olfactory (for review [7][8][9]) and, to a lesser extent, thermal stimuli [10,11] have been well studied, comparatively less is known about how visual cues evoke behavioural responses in mosquitoes (but see [12,13]) and how olfaction and vision are integrated. A recent study showed that CO2 detection activates a strong attraction to visual features that is critical for mediating interaction with close-range cues like heat and other host volatiles [3].…”

Section: Resultsmentioning

confidence: 99%

Visual-olfactory integration in the human disease vector mosquito,Aedes aegypti

Vinauger

Breugel

Locke

et al. 2019

Preprint

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Mosquitoes rely on the integration of multiple sensory cues, including olfactory, visual, and thermal stimuli, to detect, identify and locate their hosts [1][2][3][4]. Although we increasingly know more about the role of chemosensory behaviours in mediating mosquito-host interactions [1], the role of visual cues remains comparatively less studied [3], and how the combination of olfactory and visual information is integrated in the mosquito brain remains unknown. In the present study, we used a tethered-flight LED arena, which allowed for quantitative control over the stimuli, to show that CO2 exposure affects target-tracking responses, but not responses to large-field visual stimuli. In addition, we show that CO2 modulates behavioural responses to visual objects in a time-dependent manner. To gain insight into the neural basis of this olfactory and visual coupling, we conducted two-photon microscopy experiments in a new GCaMP6s-expressing mosquito line. Imaging revealed that the majority of ROIs in the lobula region of the optic lobe exhibited strong responses to small-field stimuli, but showed little response to a large-field stimulus. Approximately 20% of the neurons we imaged were modulated when an attractive odour preceded the visual stimulus; these same neurons also elicited a small response when the odour was presented alone. By contrast, imaging in the antennal lobe revealed no modulation when visual stimuli were presented before or after the olfactory stimulus. Together, our results are the first to reveal the dynamics of olfactory modulation in visually evoked behaviours of mosquitoes, and suggest that coupling between these sensory systems is asymmetrical and timedependent.3 Results and DiscussionTo detect and locate suitable hosts, mosquitoes rely on multiple sensory cues, including olfactory, visual, and thermosensory information [1][2][3][4][5] while flying through a dynamic environment [6]. Whereas responses to olfactory (for review [7][8][9]) and, to a lesser extent, thermal stimuli [10,11] have been well studied, comparatively less is known about how visual cues evoke behavioural responses in mosquitoes (but see [12,13]) and how olfaction and vision are integrated. A recent study showed that CO2 detection activates a strong attraction to visual features that is critical for mediating interaction with close-range cues like heat and other host volatiles [3]. However, because this study relied on free-flight assays, it was difficult to control the sensory experience of the mosquitoes, which is a function of both their trajectories through space and the spatiotemporal distribution of the stimuli within the wind tunnel. In other animals, ranging from bees to humans, prior exposure to a visual stimulus can modify olfactory responses [14][15][16], and vice versa [17]. It thus remains an open question how the temporal order and interval between detection of olfactory and visual stimuli influences mosquito behaviour and processing in the brain.In contrast to free-flight assays, tethered flight experiments ...

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Section: Main Text Introductionmentioning

confidence: 99%

“…Food scarcity is an important ecological constraint on mosquito larvae [26] , but little is known about the chemosensory mechanism of foraging in larval mosquitoes. Given the relative simplicity of the larval nervous system, understanding chemosensory signal transduction, coding, and behavior in larvae could lead to novel control interventions and enable a more holistic understanding of mosquito behavior in areas such as food seeking and chemotaxis [17,24] .Notwithstanding, as of recently, we have lacked effective genetic tools to study mosquito larval sensory systems as they process environmental information. Current tools used in mosquitos to monitor neural activity include extracellular recording from sensilla and antennal lobe cells [27] , as well as using synthetic calcium-sensitive dyes (e.g., FURA-2) in vivo or in heterologous systems [28,29] .…”

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confidence: 99%

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Live calcium imaging ofAedes aegyptineuronal tissues reveals differential importance of chemosensory systems for life-history-specific foraging strategies

Bui

Shyong²,

Lutz

et al. 2018

Preprint

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Aedes aegypti have a wide variety of sensory pathways that have supported success as a species as well as a highly competent vector of numerous debilitating infectious pathogens. Investigations into mosquito sensory systems and their effects on behavior are valuable resources for the advancement of mosquito control strategies. Numerous studies have elucidated key 1 . CC-BY-ND 4.0 International license It is made available under a (which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/345389 doi: bioRxiv preprint first posted online Jun. 12, 2018; aspects of mosquito sensory systems, however there remains critical gaps within the field. In particular, compared to that of the adult form, there has been a lack of studies directed towards the immature life stages. Additionally, although numerous studies have pinpointed specific sensory receptors as well as relevant response behaviors, there has been a lack of studies able to monitor both concurrently. To begin filling aforementioned gaps, here we engineered Ae. aegypti to ubiquitously express a genetically encoded calcium indicator, GCaMP6s. Using this strain, combined with advanced confocal microscopy, we were able to simultaneously measure live stimulus-evoked calcium responses in both neuronal and muscle cells with a wide spatial range and resolution. Moreover, by coupling in vivo calcium imaging with behavioral assays we were able to gain functional insights into how stimulus-evoked neural and muscle activities are represented, modulated, and transformed in mosquito larvae enabling us to elucidate mosquito sensorimotor properties important for life-history-specific foraging strategies. Significance StatementUnderstanding mosquito sensory systems and resulting behavior has been a major factor in the advancement of mosquito control innovations. Aedes aegypti larvae offer an effective life stage for further elucidating information on mosquito sensory systems. Due to their relatively simplified nervous system, mosquito larvae are ideal for studying neural signal transduction, coding, and behavior. Moreover, a better understanding of the larval sensory system may enable the development of novel control methodologies able to target mosquitoes before they reach a vector-competent stage. Here we engineer Ae. aegypti to ubiquitously express a genetically encoded calcium indicator, GCaMP6s and use this tool to observe links between sensorimotor responses and behavior by exploiting live calcium imaging as well as live tracking based behavioral assays. Main Text IntroductionThe yellow fever mosquito, Aedes aegypti , is a global vector of numerous debilitating arboviruses including Chikungunya, Dengue, Yellow Fever, and Zika [1] . Due to its ability to transmit copious pathogens, adaptability to diverse climates, flexibility in oviposition sites, and desiccation-tolerant eggs, Ae. aegypti are significant worldwide epidemiological...

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Olfactory learning and chemical ecology of olfaction in disease vector mosquitoes: a life history perspective

Cited by 45 publications

References 95 publications

Dengue virus infection changesAedes aegyptioviposition olfactory preferences

Dengue virus infection changesAedes aegyptioviposition olfactory preferences

Visual-olfactory integration in the human disease vector mosquito,Aedes aegypti

Live calcium imaging ofAedes aegyptineuronal tissues reveals differential importance of chemosensory systems for life-history-specific foraging strategies

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