Biogenic amines in malaria mosquitoes: from hearing to swarming behaviour

疟疾蚊子中的生物胺：从听觉到集群行为

• 批准号: MR/S015493/1
• 负责人: Marta Andrés Miguel
• 金额: $ 157.66万
• 依托单位: University College London
• 依托单位国家: 英国
• 项目类别: Fellowship
• 财政年份: 2019
• 资助国家: 英国
• 起止时间: 2019 至 无数据
• 项目状态: 未结题
• 来源: https://gtr.ukri.org/projects?ref=MR%2FS015493%2F1
• 关键词: Biogenic; amines; malaria; mosquitoes; hearing

Mosquitoes are more sensitive to sound than any other arthropod, by means of their fascinating tiny antennal ears, the Johnston 's organ (JO). In an organ smaller that a pin's head, male mosquitoes harbour around 15,000 auditory neurons roughly equalling the number of hair in human cochlea. Mosquitoes use their sophisticated JO's to recognize the flight tones of mating partners. Every day around sunset, male mosquitoes aggregate in areal swarms that attract females. Within swarms, male and female acoustically detect each other by their wing beats. Due to the necessity for mosquito mating, pre-mating acoustic interactions and swarming behaviour are prime targets for mosquito control tools. Despite this, the neurobiology of mosquito swarming behaviour, and the physiological mechanisms that induce it, are almost entirely unknown.We have recently shown how the mosquito JO function is modulated by an auditory efferent system. This is remarkable as auditory efferent control was believed to exist only in vertebrates. We show that the biogenic amines octopamine and serotonin are released in the mosquito JO and modulate sound-induced mechanical and electrical responses, likely contributing to JO's sophistication as sound detector. Interestingly, biogenic amines induce swarming and social behaviour in other insects. Taken together and given the intimate relationship between hearing and swarming behaviour in mosquitoes I hypothesized that they also induce mosquito aggregation in swarms and tune the mosquito auditory sensitivity to the flight tone of mating partners to maximize mating success. I argue that interfering with serotonin and octopamine signalling pathways could be a novel mosquito control target to impair hearing and swarming and consequently hinder mosquito mating. My preliminary data support this hypothesis: i) the levels of octopamine and serotonin receptors in the mosquito JO change during the time when mosquitoes are swarming, ii) the auditory sensitivity of male mosquito JO increases during swarming, and this effect is mimicked after injecting octopamine. In this project, I will use a multidisciplinary approach bridging the fields of molecular biology, physiology and behaviour to study the physiological and behavioural changes induced by octopamine and serotonin in malaria-transmitting Anopheles gambiae mosquitoes with the declared goal of devising novel vector control tools. To investigate this, I will first analyse the connection between the octopaminergic and serotonergic signalling in the mosquito JO and the circadian clock. I will study if octopamine and serotonin levels change during swarming and how these changes reflect shifts in auditory sensitivity. I will then disrupt these pathways by generating serotonin and octopamine receptor mutants and study the auditory and swarming behaviour phenotypes. Finally, I aim to translate these findings into innovative mosquito control tools by using the acquired knowledge to disrupt swarming behaviour in semi-field settings in a malaria endemic country.

蚊子比任何其他节肢动物都对声音更敏感，因为它们引人入胜的小耳朵，约翰斯顿的器官（JO）。在一个较小的销钉头的器官中，雄性蚊子藏有大约15,000个听觉神经元，大约等于人耳蜗中的头发数量。蚊子用他们精致的乔来认识交配伙伴的飞行音调。每天日落，雄性蚊子在吸引雌性的群体中聚集。在群体中，男性和女性通过翅膀的节拍互相检测。由于必须进行蚊子交配，因此预交战的声学相互作用和蜂群行为是蚊子控制工具的主要目标。尽管如此，蚊子散发行为的神经生物学以及诱导它的生理机制几乎完全未知。我们最近展示了蚊子JO功能如何通过听觉传出系统调节。这是显着的，因为据信听觉传出控制仅存在于脊椎动物中。我们表明，生物胺章鱼胺和5-羟色胺在蚊子JO中释放，并调节声音诱导的机械和电反应，可能导致Jo作为声音探测器的复杂性。有趣的是，生物胺在其他昆虫中诱导蜂群和社会行为。两者合计并考虑到蚊子中听力和蜂群行为之间的亲密关系，我假设它们还诱导了群体中的蚊子聚集，并调整了蚊子听觉敏感性对交配伙伴的飞行音调的敏感性，以最大程度地提高交配成功。我认为，干扰5-羟色胺和章鱼信号通路可能是一个新型的蚊子控制目标，以损害听力和蜂拥而至，从而阻碍蚊子交配。我的初步数据支持了这一假设：i）蚊子jo中章鱼和5-羟色胺受体的水平在蚊子蜂拥而至的时间里变化，ii）男性蚊子JO的听觉敏感性在蜂拥而至，并且在注射八达孢胺后会模仿这种作用。在这个项目中，我将使用一种跨越分子生物学，生理学和行为领域的多学科方法来研究章鱼胺和5-羟色胺在疟疾传播中引起的生理和行为变化，该疟疾是gambiae Mosquitoes，其宣告的目标是设计新型载体控制工具。为了进行调查，我将首先分析蚊子JO和昼夜节律时钟中章鱼能和5-羟色胺能信号的联系。我将研究单粒单和5-羟色胺水平在蜂群过程中是否发生变化，以及这些变化如何反映了听觉敏感性的变化。然后，我将通过产生5-羟色胺和章鱼受体突变体并研究听觉和蜂群行为表型来破坏这些途径。最后，我的目的是通过利用获得的知识破坏疟疾特有国家的半场景中的蜂群行为来将这些发现转化为创新的蚊子控制工具。

项目成果

Hitting the right note at the right time: Circadian control of audibility in Anopheles mosquito mating swarms is mediated by flight tones.

• DOI: 10.1126/sciadv.abl4844
• 发表时间: 2022-01-14
• 期刊: Science advances
• 影响因子: 13.6
• 作者: Somers J;Georgiades M;Su MP;Bagi J;Andrés M;Alampounti A;Mills G;Ntabaliba W;Moore SJ;Spaccapelo R;Albert JT
• 通讯作者: Albert JT

Acoustic Physiology in Mosquitoes

蚊子的声学生理学

• DOI: 10.1101/pdb.top107685
• 发表时间: 2023
• 期刊: Cold Spring Harbor Protocols
• 作者: Su M

A novel beta-adrenergic like octopamine receptor modulates the audition of malaria mosquitoes and serves as insecticide target

• DOI: 10.1101/2022.08.02.502538
• 发表时间: 2022-08
• 期刊: bioRxiv
• 作者: M. Georgiades;CA Alampounti;J. Somers;M. Su;D. Ellis;J. Bagi;W. Ntabaliba;S. Moore;JT Albert;M. Andrés

Hearing of malaria mosquitoes is modulated by a beta-adrenergic-like octopamine receptor which serves as insecticide target.

• DOI: 10.1038/s41467-023-40029-y
• 发表时间: 2023-07-19
• 期刊: NATURE COMMUNICATIONS
• 影响因子: 16.6
• 作者: Georgiades, Marcos;Alampounti, Alexandros;Somers, Jason;Su, Matthew P. P.;Ellis, David A.;Bagi, Judit;Terrazas-Duque, Daniela;Tytheridge, Scott;Ntabaliba, Watson;Moore, Sarah;Albert, Joerg T.;Andres, Marta
• 通讯作者: Andres, Marta