Abstract
The high vector competence of mosquitoes is intrinsically linked to their reproductive strategy because females need a vertebrate blood meal to develop large batches of eggs. However, the molecular mechanisms and pathways regulating mosquito host-seeking behaviour are largely unknown. Here, we test whether host-seeking behaviour may be linked to the female’s energy reserves, with low energy levels triggering the search for a nutrient-rich blood meal. Our results demonstrate that sugar feeding delays host-seeking behaviour in the invasive tiger mosquito Aedes albopictus, but the levels of energy reserves do not correlate with changes in host-seeking behaviour. Using tissue-specific gene expression analyses, we show for the first time, to our knowledge, that sugar feeding alone induces a transient up-regulation of several vitellogenesis-related genes in the female fat body, resembling the transcriptional response after a blood meal. Specifically, high expression levels of a vitellogenin gene (Vg-2) correlated with the lowest host-seeking activity of sugar-fed females. Knocking down the Vg-2 gene via RNA interference (RNAi) restored host-seeking behaviour in these females, firmly establishing that Vg-2 gene expression has a pivotal role in regulating host-seeking behaviour in young Ae. albopictus females. The identification of a molecular mechanism regulating host-seeking behaviour in mosquitoes could pave the way for novel vector control strategies aiming to reduce the biting activity of mosquitoes. From an evolutionary perspective, this is the first demonstration of vitellogenin genes controlling feeding-related behaviours in nonsocial insects, while vitellogenins are known to regulate caste-specific foraging and brood-care behaviours in eusocial insects. Hence, this work confirms the key role of vitellogenin in controlling feeding-related behaviours in distantly related insect orders, suggesting that this function could be more ubiquitous than previously thought.
Highlights
Mosquitoes are important vectors of many diseases around the world, transmitting numerous human pathogens that collectively cause the deaths of more than 700,000 people each year [1]
Host-seeking behaviour was significantly higher in starved mosquitoes with access to water only, compared to females provided with sucrose (Analysis of Covariance [ANCOVA], all p < 0.026 after False Discovery Rate [FDR] correction) (Fig 1B–1E)
Blood-meal–dependent vitellogenesis is best understood in the anautogenous mosquito Ae. aegypti, where vitellogenin gene expression is repressed prior to blood feeding [2]
Summary
Mosquitoes are important vectors of many diseases around the world, transmitting numerous human pathogens (e.g., the malaria parasite and arboviruses such as dengue and Zika) that collectively cause the deaths of more than 700,000 people each year [1]. Their high vector competence is intrinsically linked to their reproductive strategy because females of most mosquito species are anautogenous, i.e., relying on vertebrate blood to produce a large progeny. Multiple regulatory factors act synergistically to trigger vitellogenin protein synthesis in the fat body [3,4,5,6,7]. The distal signals initiating or suppressing the search for a blood meal have not been identified
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