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对声音都更敏感，这得益于它们迷人的微小触角耳朵，即约翰斯顿器官（JO）。在一个比针头还小的器官中，雄性蚊子拥有大约 15,000 个听觉神经元，大约相当于人类耳蜗中毛发的数量。蚊子利用其复杂的 JO 来识别交配伙伴的飞行音。每天日落时分，雄性蚊子都会聚集成群，吸引雌性蚊子。在蜂群中，雄性和雌性通过翅膀的拍打声来相互探测。由于蚊子交配的必要性，交配前的声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，蚊子成群行为的神经生物学以及诱发这种行为的生理机制几乎完全未知。我们最近展示了蚊子 JO 功能是如何通过听觉传出系统调节的。这是值得注意的，因为听觉传出控制被认为只存在于脊椎动物中。我们表明，生物胺章鱼胺和血清素在蚊子 JO 中释放，并调节声音引起的机械和电响应，这可能有助于 JO 作为声音探测器的复杂性。有趣的是，生物胺会诱导其他昆虫的集群和社会行为。综合考虑，考虑到蚊子的听觉和成群行为之间的密切关系，我假设它们还会诱导蚊子聚集成群，并根据交配伙伴的飞行音调调整蚊子的听觉敏感度，以最大限度地提高交配成功率。我认为，干扰血清素和章鱼胺信号通路可能是一种新的蚊子控制目标，可以损害听力和蜂群，从而阻碍蚊子交配。我的初步数据支持这一假设：i）蚊子 JO 中的章鱼胺和血清素受体水平在蚊子成群时发生变化，ii）雄性蚊子 JO 的听觉敏感性在成群过程中增加，注射章鱼胺后​​模拟了这种效果。在这个项目中，我将采用跨学科的方法，连接分子生物学、生理学和行为学领域，研究章鱼胺和血清素在传播疟疾的冈比亚按蚊中引起的生理和行为变化，其目标是设计新型病媒控制工具。为了研究这一点，我将首先分析蚊子 JO 中的章鱼胺能和血清素能信号与生物钟之间的联系。我将研究章鱼胺和血清素水平在蜂群过程中是否发生变化，以及这些变化如何反映听觉敏感性的变化。然后，我将通过生成血清素和章鱼胺受体突变体来破坏这些途径，并研究听觉和蜂群行为表型。最后，我的目标是将这些发现转化为创新的蚊子控制工具，利用所获得的知识来扰乱疟疾流行国家半野外环境中的蜂群行为。

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

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

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