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Male swarming aggregation pheromones increase female attraction and mating success among multiple African malaria vector mosquito species
Stockholm University, Faculty of Science, Department of Zoology. Nature Research Centre, Lithuania.
Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
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Number of Authors: 122020 (English)In: Nature Ecology & Evolution, E-ISSN 2397-334X, Vol. 4, p. 1395-1401Article in journal (Refereed) Published
Abstract [en]

Accumulating behavioural data indicate that aggregation pheromones may mediate the formation and maintenance of mosquito swarms. However, chemical cues possibly luring mosquitoes to swarms have not been adequately investigated, and the likely molecular incitants of these complex reproductive behaviours remain unknown. Here we show that males of the important malaria vector species Anopheles arabiensis and An. gambiae produce and release aggregation pheromones that attract individuals to the swarm and enhance mating success. We found that males of both species released significantly higher amounts of 3-hydroxy-2-butanone (acetoin), 6-methyl-5-hepten-2-one (sulcatone), octanal, nonanal and decanal during swarming in the laboratory. Feeding males with stable-isotope-labelled glucose revealed that the males produced these five compounds. A blend composed of synthetic analogues to these swarming odours proved highly attractive to virgin males and females of both species under laboratory conditions and substantially increased mating in five African malaria vectors (An. gambiae, An. coluzzii, An. arabiensis, An. merus and An. funestus) in semi-field experiments. Our results not only narrow a conspicuous gap in understanding a vital aspect of the chemical ecology of male mosquitoes but also demonstrate fundamental roles of rhythmic and metabolic genes in the physiology and behavioural regulation of these vectors. These identified aggregation pheromones have great potential for exploitation against these highly dangerous insects. Manipulating such pheromones could increase the efficacy of malaria-vector control programmes.

Place, publisher, year, edition, pages
2020. Vol. 4, p. 1395-1401
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:su:diva-185421DOI: 10.1038/s41559-020-1264-9ISI: 000555399800004PubMedID: 32747772OAI: oai:DiVA.org:su-185421DiVA, id: diva2:1475957
Available from: 2020-10-13 Created: 2020-10-13 Last updated: 2023-01-13Bibliographically approved
In thesis
1. Decoding the language of transmission among vector-pathogen-host
Open this publication in new window or tab >>Decoding the language of transmission among vector-pathogen-host
2023 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Vector-borne diseases account for over 17 percent of all infectious diseases and lead to more than 700,000 mortalities annually. Importantly, there is a complex interaction between infectious organisms and their host. Vectors spread pathogens, which have a significant negative health effect on humans and animals and therefore detrimental economic and environmental impacts. Only 2% of the more than 3,600 mosquito species are blood feeders, primarily; the Anopheles, Culex, and Aedes which spread the Malaria parasite, Zika, Chikungunya, West Nile, and Dengue viruses. Therefore, understanding the complex chemical signaling and the molecular mechanisms that mediate pathogen and vector interaction, and allow the pathogen to survive and spread, are the subjects of this thesis.

In project I, we determined the production and release of Anopheles male aggregation Volatile Organic Compounds (VOCs) that initiate swarming, and enhance mating success. In addition, we compared the RNA-sequencing libraries of swarming to flag for chemosensory and circadian genes. The goal was to identify the molecular mechanisms of swarming and metabolite roles in mating success.

In project II, we evaluated the phagostimulant effects of (E)-4-Hydroxy-3-methyl-but-2-enyl pyrophosphate (HMBPP) on an artificial feeding system for some important vectors (Anopheles coluzzii, An. arabiensis, An. gambiae s.s., Culex pipiens/Culex torrentium, and Aedes aegypti). We showed that our toxic plant-based solution can kill the five lethal vectors.

In project III, we studied the alteration of An. gambiae behavior by the Plasmodium falciparum at infected (oocyst-carrying, 7 days post-infection) and infective (sporozoite-carrying, 14 days post-infection) stages. To discover whether antennal chemosensory genes expression changes at different stages of infection, we performed RNA-seq and examined the candidate olfactory genes’ abundance to provide a possible molecular mechanism for manipulating the parasite-carrying mosquitoes' behavior.

Finally, in project IV, we presented the results of RNA-seq analysis that revealed the network connection between developmental genes and the physiological plasticity in male mosquitoes of An. funestus. We identified the transcripts that associated with the male An. funestus sexual maturation and mating success.

In summary, this thesis focuses on understanding how vector-pathogen interaction manipulates the vector’s transcriptome, physiology, and behavior to enhance transmission success and thereby identify novel targets for vector-borne disease control. 

 

Place, publisher, year, edition, pages
Stockholm: Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, 2023. p. 44
Keywords
Vector-borne disease, Malaria, Anopheles, Plasmodium falciparum, Zika, Aedes, Vector control strategy
National Category
Health Sciences Veterinary Science Behavioral Sciences Biology Biochemistry Molecular Biology
Research subject
Molecular Bioscience
Identifiers
urn:nbn:se:su:diva-213656 (URN)978-91-8014-162-8 (ISBN)978-91-8014-163-5 (ISBN)
Public defence
2023-02-27, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
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Available from: 2023-02-02 Created: 2023-01-13 Last updated: 2025-02-20Bibliographically approved

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Mozūraitis, RaimondasHajkazemian, MelikaSzymczak, JoannaSekar, VaishnoviBiryukova, InnaKoekemoer, Lizette L.Emami, S. Noushin

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Mozūraitis, RaimondasHajkazemian, MelikaSzymczak, JoannaSekar, VaishnoviBiryukova, InnaKoekemoer, Lizette L.Emami, S. Noushin
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Department of ZoologyDepartment of Molecular Biosciences, The Wenner-Gren InstituteScience for Life Laboratory (SciLifeLab)
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