Age-dependent regulation of host seeking in Anopheles coluzzii

Omondi, A. B.; Ghaninia, Majid; Dawit, Mengistu; Svensson, Thomas; Ignell, Rickard

doi:10.1038/s41598-019-46220-w

Cited by 51 publications

(85 citation statements)

References 49 publications

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“…aegypti, DAM2 Drosophila activity monitors, equipped with MAN2 gas distribution manifolds (TriKinetics), were used. A synthetic human odor blend, identified from the body volatiles of human volunteers [43] was used to stimulate dengue-infected and non-infected Ae. aegypti female mosquitoes.…”

Section: Odor-mediated Locomotion Behaviormentioning

confidence: 99%

Dengue infection modulates locomotion and host seeking in Aedes aegypti

Tallon

Lorenzo

Moreira³

et al. 2020

PLoS Negl Trop Dis

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Pathogens may manipulate their human and mosquito hosts to enhance disease transmission. Dengue, caused by four viral serotypes, is the fastest-growing transmissible disease globally resulting in 50-100 million infections annually. Transmission of the disease relies on the interaction between humans and the vector Aedes aegypti and is largely dependent on the odor-mediated host seeking of female mosquitoes. In this study, we use activity monitors to demonstrate that dengue virus-1 affects the locomotion and odor-mediated behavior of Ae. aegypti, reflecting the progression of infection within the mosquito. Mosquitoes 4-6 days post-infection increase locomotion, but do not alter their odor-driven host-seeking response. In contrast, females 14-16 days post-infection are less active, yet more sensitive to human odors as assessed by behavioral and electrophysiological assays. Such an increase in physiological and behavioral sensitivity is reflected by the antennal-specific increase in abundance of neural signaling transcripts in 14 days post-infection females, as determined by transcriptome analysis. This suggests that the sensitivity of the mosquito peripheral olfactory system is altered by the dengue virus by enhancing the overall neural responsiveness of the antenna, rather than the selective regulation of chemosensoryrelated genes. Our study reveals that dengue virus-1 enhances vector-related behaviors in the early stages post-infection that aid in avoiding predation and increasing spatial exploration. On the other hand, at the later stages of infection, the virus enhances the host-seeking capacity of the vector, thereby increasing the risk of virus transmission. A potential mechanism is discussed.

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Section: Odor-mediated Locomotion Behaviormentioning

confidence: 99%

Dengue infection modulates locomotion and host seeking in Aedes aegypti

Tallon

Lorenzo

Moreira³

et al. 2020

PLoS Negl Trop Dis

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“…Mosquitoes rely heavily on their sense of olfaction to integrate ecologically relevant stimuli that change over the course of their adult lifespan. When females first eclose, they are uninterested in host odor (34) and instead actively search for sugar-rich resources from plants to supplement their nutrient reserves. After a period of ~4 days post eclosion, they develop an attraction to host odors (34,35) and following a bloodmeal will experience a refractory period to host odor until after oviposition.…”

Section: Discussionmentioning

confidence: 99%

“…When females first eclose, they are uninterested in host odor (34) and instead actively search for sugar-rich resources from plants to supplement their nutrient reserves. After a period of ~4 days post eclosion, they develop an attraction to host odors (34,35) and following a bloodmeal will experience a refractory period to host odor until after oviposition. These changes in behavior have been correlated with changes in chemosensory gene transcript abundance (34,36).…”

Section: Discussionmentioning

confidence: 99%

“…After a period of ~4 days post eclosion, they develop an attraction to host odors (34,35) and following a bloodmeal will experience a refractory period to host odor until after oviposition. These changes in behavior have been correlated with changes in chemosensory gene transcript abundance (34,36). It would be interesting to determine if expression of alternative Ors in ORNs only during adulthood -when endogenous ORs are already chosen -can alter Or gene expression, or if precocious expression of Ors takes on an 'early-bird-gets-the-worm' paradigm (37).…”

Section: Discussionmentioning

confidence: 99%

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A Feedback Mechanism RegulatesOdorant ReceptorExpression in the Malaria Mosquito,Anopheles gambiae

Maguire

Afify

Goff

et al. 2020

Preprint

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Mosquitoes locate and approach humans (‘host-seek’) when specific Olfactory Neurons (ORNs) in the olfactory periphery activate a specific combination of glomeruli in the mosquito Antennal Lobe (AL). We hypothesize that dysregulating proper glomerular activation in the presence of human odor will prevent host-seeking behavior. In experiments aimed at ectopically activating most ORNs in the presence of human odor, we made a surprising finding: ectopic expression of an AgOr (AgOr2) in Anopheles gambiae ORNs dampens the activity of the expressing neuron. This contrasts studies in Drosophila melanogaster, the typical insect model of olfaction, in which ectopic expression of non-native ORs in ORNs confers ectopic neuronal responses without interfering with native olfactory physiology. To gain insight into this dysfunction in mosquitoes, RNA-seq analyses were performed comparing wild-type antennae to those ectopically expressing AgOr2 in ORNs. Remarkably, almost all Or transcripts were significantly downregulated (except for AgOr2), and additional experiments suggest that it is AgOR2 protein rather than mRNA that mediates this downregulation. Our study shows that ORNs of Anopheles mosquitoes (in contrast to Drosophila) employ a currently unexplored regulatory mechanism of OR expression, which may be adaptable as a vector-control strategy.SIGNIFICANCE STATEMENTStudies in Drosophila melanogaster suggest that insect Olfactory Receptor Neurons (ORNs) do not contain mechanisms by which Odorant Receptors (ORs) regulate OR expression. This has proved useful in studies where ectopic expression of an OR in Drosophila ORNs confers responses to the odorants that activate the newly expressed OR. In experiments in Anopheles gambiae mosquitoes, we found that ectopic expression of an OR in most Anopheles ORNs dampened the activity of the expressing neurons. RNA-seq analyses demonstrated that ectopic OR expression in Anopheles ORNs leads to downregulation of endogenous Or transcripts. Additional experiments suggest that this downregulation required ectopic expression of a functional OR protein. These findings reveal that Anopheles mosquitoes, in contrast to Drosophila, contain a feedback mechanism to regulate OR expression. Mosquito ORNs might employ regulatory mechanisms of OR expression previously thought to occur only in non-insect olfactory systems.

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“…Besides feeding on plant resources, mosquitoes use vertebrate blood as a nutritional resource for reproduction (Briegel 1990 ; Omondi et al 2019 ). Most medically important species have been identified to express strong and inherent host selection behavior.…”

Section: Insect Vectors Of Diseasesmentioning

confidence: 99%

Insect chemical ecology: chemically mediated interactions and novel applications in agriculture

Mbaluto

Ayelo

Duffy

et al. 2020

Arthropod-Plant Interactions

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Insect chemical ecology (ICE) evolved as a discipline concerned with plant–insect interactions, and also with a strong focus on intraspecific pheromone-mediated communication. Progress in this field has rendered a more complete picture of how insects exploit chemical information in their surroundings in order to survive and navigate their world successfully. Simultaneously, this progress has prompted new research questions about the evolution of insect chemosensation and related ecological adaptations, molecular mechanisms that mediate commonly observed behaviors, and the consequences of chemically mediated interactions in different ecosystems. Themed meetings, workshops, and summer schools are ideal platforms for discussing scientific advancements as well as identifying gaps and challenges within the discipline. From the 11th to the 22nd of June 2018, the 11th annual PhD course in ICE was held at the Swedish University of Agricultural Sciences (SLU) Alnarp, Sweden. The course was made up of 35 student participants from 22 nationalities (Fig. 1a) as well as 32 lecturers. Lectures and laboratory demonstrations were supported by literature seminars, and four broad research areas were covered: (1) multitrophic interactions and plant defenses, (2) chemical communication focusing on odor sensing, processing, and behavior, (3) disease vectors, and (4) applied aspects of basic ICE research in agriculture. This particular article contains a summary and brief synthesis of these main emergent themes and discussions from the ICE 2018 course. In addition, we also provide suggestions on teaching the next generation of ICE scientists, especially during unprecedented global situations.

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Age-dependent regulation of host seeking in Anopheles coluzzii

Cited by 51 publications

References 49 publications

Dengue infection modulates locomotion and host seeking in Aedes aegypti

Dengue infection modulates locomotion and host seeking in Aedes aegypti

A Feedback Mechanism RegulatesOdorant ReceptorExpression in the Malaria Mosquito,Anopheles gambiae

Insect chemical ecology: chemically mediated interactions and novel applications in agriculture

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