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"Ignell, Rickard"
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Modulation of odour-guided behaviour in mosquitoes
2021
Mosquitoes are emerging as model systems with which to study innate behaviours through neuroethology and functional genomics. Decades of work on these disease vectors have provided a solid behavioural framework describing the distinct repertoire of predominantly odour-mediated behaviours of female mosquitoes, and their dependence on life stage (intrinsic factors) and environmental cues (extrinsic factors). The purpose of this review is to provide an overview of how intrinsic factors, including adult maturation, age, nutritional status, and infection, affect the attraction to plants and feeding on plant fluids, host seeking, blood feeding, supplemental feeding behaviours, pre-oviposition behaviour, and oviposition in female mosquitoes. With the technological advancements in the recent two decades, we have gained a better understanding of which volatile organic compounds are used by mosquitoes to recognise and discriminate among various fitness-enhancing resources, and characterised their neural and molecular correlates. In this review, we present the state of the art of the peripheral olfactory system as described by the neural physiology, functional genomics, and genetics underlying the demonstrated changes in the behavioural repertoire in female mosquitoes. The review is meant as a summary introduction to the current conceptual thinking in the field.
Journal Article
Effect of extended egg quiescence and elevation in carbon dioxide on life history traits of Aedes aegypti
by
Nalikkaramal, Sukritha
,
Hill, Sharon Rose
,
Ignell, Rickard
in
631/158/2165
,
631/158/856
,
Aedes - drug effects
2025
Elevation in carbon dioxide is a global threat, driving anthropogenic climate change. How disease-vectoring mosquitoes respond to these changes is currently largely unknown. The dengue vector,
Aedes aegypti,
has adapted to urban environments, which are more affected by climatic changes, especially CO
2
.
Aedes aegypti
lay eggs around ephemeral water bodies that are prone to desiccation, with the pharate larvae possessing the ability to resist the desiccation, during which the permeability across the chorion is compromised. The study investigates the combined effects of elevated atmospheric CO
2
and extended egg quiescence duration on life-history traits of immature and adult stages, including development rate, survival and size. Furthermore, we analysed the metabolic reserves of newly emerged females and whether mosquitoes display compensatory feeding in response to restricted reserves. Extended egg quiescence duration, combined with elevated CO
2
level, differentially affected developmental duration and larval survival, with carry-over effects on adult metabolic reserves, size and survival. The interaction of elevated CO
2
conditions and egg quiescence period differentially impact life-history traits of
Ae. aegypti
. The findings of this study provide evidential support for assertion that changing climatic conditions significantly impact survival and population dynamics, as well as feeding propensity, which directly affect the vectorial capacity of
Ae. aegypti
.
Journal Article
Cattle-Derived Unsaturated Aldehydes Repel Biting Midges and Mosquitoes
2022
Host-derived repellents offer a novel way to reduce disease vector–host interactions, particularly for vectors and nuisance pests where commercial repellents are not available, e.g., Culicoides biting midges. By revising the criteria previously used to identify bioactive volatile organic compounds for Culicoides nubeculosus, we identify (E)-2-hexenal, (E)-2-heptenal, (E)-2-octenal, and (E)-2-nonenal to be differentially present in the headspace odour of cattle hair and to elicit antennal responses in this research model species. A blend of these unsaturated aldehydes elicited an aversive response in C. nubeculosus, as well as a repellent response in three disease vector mosquito species, Aedes aegypti, Culex quinquefasciatus and Anopheles coluzzii, a response that was stronger than that to the commercially available repellents tested (DEET, IR3535, PMD, icaridin, and d-allethrin). Culicoides nubeculosus was behaviourally indifferent to these commercially available repellents tested, except d-allethrin to which it was attracted. The identification of a host-derived repellent odour blend, which reduces the interaction between biting midges extends the array of tools to be used in integrated vector management of these and other disease vectors.
Journal Article
Regulation of the antennal transcriptome of the dengue vector, Aedes aegypti, during the first gonotrophic cycle
by
Hill, Sharon Rose
,
Taparia, Tanvi
,
Ignell, Rickard
in
Aedes - genetics
,
Aedes aegypti
,
Animal Genetics and Genomics
2021
Background
In the light of dengue being the fastest growing transmissible disease, there is a dire need to identify the mechanisms regulating the behaviour of the main vector
Aedes aegypti
. Disease transmission requires the female mosquito to acquire the pathogen from a blood meal during one gonotrophic cycle, and to pass it on in the next, and the capacity of the vector to maintain the disease relies on a sustained mosquito population.
Results
Using a comprehensive transcriptomic approach, we provide insight into the regulation of the odour-mediated host- and oviposition-seeking behaviours throughout the first gonotrophic cycle. We provide clear evidence that the age and state of the female affects antennal transcription differentially. Notably, the temporal- and state-dependent patterns of differential transcript abundance of chemosensory and neuromodulatory genes extends across families, and appears to be linked to concerted differential modulation by subsets of transcription factors.
Conclusions
By identifying these regulatory pathways, we provide a substrate for future studies targeting subsets of genes across disparate families involved in generating key vector behaviours, with the goal to develop novel vector control tools.
Journal Article
Putative Chemosensory Receptors of the Codling Moth, Cydia pomonella, Identified by Antennal Transcriptome Analysis
by
Trona, Federica
,
Montagné, Nicolas
,
Bengtsson, Jonas M.
in
Adults
,
Agricultural and Veterinary Sciences
,
Agriculture, Forestry and Fisheries
2012
The codling moth, Cydia pomonella, is an important fruit pest worldwide. As nocturnal animals, adults depend to a large extent on olfactory cues for detection of food and mates, and, for females, oviposition sites. In insects, odor detection is mediated by odorant receptors (ORs) and ionotropic receptors (IRs), which ensure the specificity of the olfactory sensory neuron responses. In this study, our aim was to identify chemosensory receptors in the codling moth as a means to uncover new targets for behavioral interference. Using next-generation sequencing techniques, we identified a total of 43 candidate ORs, one gustatory receptor and 15 IRs in the antennal transcriptome. Through Blast and sequence similarity analyses we annotated the insect obligatory co-receptor ORco, five genes clustering in a conserved clade containing sex pheromone receptors, one homolog of the Bombyx mori female-enriched receptor BmorOR30 (but no homologs of the other B. mori female-enriched receptors) and one gene clustering in the sugar receptor family. Among the candidate IRs, we identified homologs of the two highly conserved co-receptors IR8a and IR25a, and one homolog of an IR involved in phenylethyl amine detection in Drosophila. Our results open for functional characterization of the chemosensory receptors of C. pomonella, with potential for new or refined applications of semiochemicals for control of this pest insect.
Journal Article
Impact of elevated CO2 level and egg quiescence duration on gene expression in the peripheral olfactory system of Aedes aegypti
by
Nalikkaramal, Sukritha
,
Hill, Sharon Rose
,
Ignell, Rickard
in
631/158/2165
,
631/158/2452
,
631/158/856
2025
Elevation in CO
2
can significantly impact the biology of various organisms, affecting life-history traits of both aquatic and terrestrial forms, including disease-vectoring mosquitoes. For mosquitoes, this effect is accentuated by egg quiescence duration, resulting in a change in foraging of adult females. Female mosquitoes rely on their olfactory system for locating resources, such as nectar and blood. This study employs a transcriptomic approach to investigate how a projected elevation in CO
2
level, under a worst-case scenario, interacts with extended egg quiescence duration to modulate the molecular machinery of the peripheral olfactory system, the antennae and maxillary palps, of the yellow fever mosquito,
Aedes aegypti
. The transcriptome analysis demonstrates significant changes in the abundance of genes related to metabolism, xenobiotics degradation and chemosensory function, with the most pronounced effects observed in the CO
2
sensing tissue, the maxillary palp. The study provides novel insights into how anthropogenic climate change can modulate the olfactory sensory system of disease vectors, which may have cascading effects on resource-seeking behaviour.
Journal Article
Evolution of mosquito preference for humans linked to an odorant receptor
2014
Female mosquitoes are major vectors of human disease and the most dangerous are those that preferentially bite humans. A ‘domestic’ form of the mosquito
Aedes aegypti
has evolved to specialize in biting humans and is the main worldwide vector of dengue, yellow fever, and chikungunya viruses. The domestic form coexists with an ancestral, ‘forest’ form that prefers to bite non-human animals and is found along the coast of Kenya. We collected the two forms, established laboratory colonies, and document striking divergence in preference for human versus non-human animal odour. We further show that the evolution of preference for human odour in domestic mosquitoes is tightly linked to increases in the expression and ligand-sensitivity of the odorant receptor
AaegOr4
, which we found recognizes a compound present at high levels in human odour. Our results provide a rare example of a gene contributing to behavioural evolution and provide insight into how disease-vectoring mosquitoes came to specialize on humans.
The mosquito
Aedes aegypti
includes two subspecies, one of which shows a preference for biting humans, whereas the other prefers to bite non-human animals; genetic analysis reveals that changes in the mosquito odorant receptor Or4 contribute to the behavioural difference—in human-preferring mosquitoes, Or4 is more highly expressed and more sensitive to sulcatone, a compound present at high levels in human odour.
How mosquitoes got a taste for human blood
A 'domestic' form of the mosquito
Aedes aegypti
, which is the major worldwide vector of dengue, yellow fever and chikungya viruses, has evolved from an ancestral 'forest' form. The former preferentially bites humans, the latter avoids them. Leslie Vosshall and colleagues collected the two forms where they coexist in coastal Kenya, and document striking divergence in preference for human versus animal odour. The human-preferring mosquito carries a version of the olfactory receptor
Or4
that is more highly expressed, with greater ligand sensitivity and that makes the mosquito more sensitive to sulcatone, a compound found at high concentration in human odour. This finding provides a rare example of a gene linked to the evolution of behaviour in natural populations.
Journal Article
Sex and age modulate antennal chemosensory-related genes linked to the onset of host seeking in the yellow-fever mosquito, Aedes aegypti
2019
The mosquito
Aedes aegypti
is the primary vector for the fastest growing infectious disease in the world, dengue fever. Disease transmission heavily relies on the ability of female mosquitoes to locate their human hosts. Additionally, males may be found in close proximity to humans, where they can find mates. Host seeking behaviour of both sexes is dependent on adult sexual maturation. Identifying the molecular basis for the onset of host seeking may help to determine targets for future vector control. In this study, we investigate modulation of the host seeking behaviour and the transcript abundance of the main chemoreceptor families between sexes and across ages in newly-emerged mosquitoes. Attraction to human odour was assessed using a Y-tube olfactometer, demonstrating that both males and females display age-dependent regulation of host seeking. The largest increase in transcript abundance was identified for select chemosensory genes in the antennae of young adult
Ae
.
aegypti
mosquitoes and reflects the increase in attraction to human odour observed between 1 and 3 day(s) post-emergence in both males and females. Future functional characterisation of the identified differentially abundant genes may provide targets for the development of novel control strategies against vector borne diseases.
Journal Article
Blood meal induced regulation of the chemosensory gene repertoire in the southern house mosquito
by
Hill, Sharon Rose
,
Taparia, Tanvi
,
Ignell, Rickard
in
Agricultural and Veterinary Sciences
,
Agricultural Biotechnology
,
Animal Feed
2017
Background
The southern house mosquito,
Culex quinquefasciatus
, is one of the most prevalent vectors of lymphatic filariasis and flavivirus-induced encephalitis. Its vectorial capacity is directly affected by its reproductive feeding behaviors, such as host seeking, blood feeding, resting, and egg laying. In mosquitoes, these gonotrophic behaviors are odor-mediated and regulated following blood feeding. Immediately after a blood meal, female mosquitoes show reduced olfactory responsiveness and flight activity, as they enter a resting state. Insights into antennal chemosensory gene regulation at this time period can provide a foundation to identify targets involved in the state switch between host seeking and resting.
Results
This study used quantitative gene expression analyses to explore blood meal induced regulation of chemosensory gene families in the antennae of 6 days post-emergence
C. quinquefasciatus
females. Improved annotations for multiple chemosensory gene families, and a quantitative differential gene expression analysis between host seeking and 24 h post- blood fed females of the same age, allowed for the detection of transcripts that potentially play a role in the switch from host seeking to resting, in
C. quinquefasciatus
. The expression profiles of chemosensory genes varied significantly between the two treatments.
Conclusions
Annotations for chemosensory gene repertoires in
C. quinquefasciatus
have been manually curated and corrected for 3’ exon choice and transcript length, through sequence and transcriptome analyses. The gene expression analyses identified various molecular components of the peripheral olfactory system in
C. quinquefasciatus
, including odorant receptors, ionotropic receptors, odorant binding proteins and chemosensory proteins, that are regulated in response to blood feeding, and could be critical for the behavioral switch from host seeking to resting. Functional characterization of these proteins in the future can identify targets essential for the females’ gonotrophic behaviors, and can be used to design novel vector control strategies.
Journal Article
Ionotropic Chemosensory Receptors Mediate the Taste and Smell of Polyamines
by
Üçpunar, Habibe K.
,
Gompel, Nicolas
,
Quillery, Elsa
in
Aedes - physiology
,
Aging
,
Animal Feed
2016
The ability to find and consume nutrient-rich diets for successful reproduction and survival is fundamental to animal life. Among the nutrients important for all animals are polyamines, a class of pungent smelling compounds required in numerous cellular and organismic processes. Polyamine deficiency or excess has detrimental effects on health, cognitive function, reproduction, and lifespan. Here, we show that a diet high in polyamine is beneficial and increases reproductive success of flies, and we unravel the sensory mechanisms that attract Drosophila to polyamine-rich food and egg-laying substrates. Using a combination of behavioral genetics and in vivo calcium imaging, we demonstrate that Drosophila uses multisensory detection to find and evaluate polyamines present in overripe and fermenting fruit, their favored feeding and egg-laying substrate. In the olfactory system, two coexpressed ionotropic receptors (IRs), IR76b and IR41a, mediate the long-range attraction to the odor. In the gustatory system, multimodal taste sensation by IR76b receptor and GR66a bitter receptor neurons is used to evaluate quality and valence of the polyamine providing a mechanism for the fly's high attraction to polyamine-rich and sweet decaying fruit. Given their universal and highly conserved biological roles, we propose that the ability to evaluate food for polyamine content may impact health and reproductive success also of other animals including humans.
Journal Article