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Fat body–specific vitellogenin expression regulates host-seeking behaviour in the mosquito Aedes albopictus

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...

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Autores principales: Dittmer, Jessica, Alafndi, Ayad, Gabrieli, Paolo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6508604/
https://www.ncbi.nlm.nih.gov/pubmed/31071075
http://dx.doi.org/10.1371/journal.pbio.3000238
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author Dittmer, Jessica
Alafndi, Ayad
Gabrieli, Paolo
author_facet Dittmer, Jessica
Alafndi, Ayad
Gabrieli, Paolo
author_sort Dittmer, Jessica
collection PubMed
description 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.
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spelling pubmed-65086042019-05-23 Fat body–specific vitellogenin expression regulates host-seeking behaviour in the mosquito Aedes albopictus Dittmer, Jessica Alafndi, Ayad Gabrieli, Paolo PLoS Biol Research Article 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. Public Library of Science 2019-05-09 /pmc/articles/PMC6508604/ /pubmed/31071075 http://dx.doi.org/10.1371/journal.pbio.3000238 Text en © 2019 Dittmer et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Dittmer, Jessica
Alafndi, Ayad
Gabrieli, Paolo
Fat body–specific vitellogenin expression regulates host-seeking behaviour in the mosquito Aedes albopictus
title Fat body–specific vitellogenin expression regulates host-seeking behaviour in the mosquito Aedes albopictus
title_full Fat body–specific vitellogenin expression regulates host-seeking behaviour in the mosquito Aedes albopictus
title_fullStr Fat body–specific vitellogenin expression regulates host-seeking behaviour in the mosquito Aedes albopictus
title_full_unstemmed Fat body–specific vitellogenin expression regulates host-seeking behaviour in the mosquito Aedes albopictus
title_short Fat body–specific vitellogenin expression regulates host-seeking behaviour in the mosquito Aedes albopictus
title_sort fat body–specific vitellogenin expression regulates host-seeking behaviour in the mosquito aedes albopictus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6508604/
https://www.ncbi.nlm.nih.gov/pubmed/31071075
http://dx.doi.org/10.1371/journal.pbio.3000238
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