Ochwedo Kevin O, Wang Xiaodi, Céspedes Nora, Bentil Ronald E, Wild Ryan, Hernandez Emily, Hernandez Amy, Kaylor Hannah L, Debebe Yared, Datta Jyotishka, Robert Michael A, Riffell Jeffrey A, Lewis Edwin E, Luckhart Shirley
Department of Entomology, Plant Pathology, and Nematology, University of Idaho, Moscow, Idaho, United States of America.
Department of Biology, University of Washington, Seattle, Washington, United States of America.
PLoS Pathog. 2025 Apr 28;21(4):e1013139. doi: 10.1371/journal.ppat.1013139. eCollection 2025 Apr.
Disrupting behaviors linked to movement of primary mosquito vectors, such as diel locomotor activity and visual sensitivity, is a novel and plausible malaria control intervention. Diel locomotor activity is an output of arthropod circadian activity and is influenced by factors such as light, temperature, and infection status. The biogenic amines histamine and serotonin (5-HT) are ingested with blood and differ between healthy hosts and those with severe malaria. They regulate malaria parasite infection in Anopheles stephensi, but the degree to which aging, temperature, and infection interact with ingested biogenic amines to influence mosquito behavior was unknown prior to these studies. We provisioned A. stephensi with histamine and 5-HT at healthy- and malaria-associated levels to examine diel locomotor activity of uninfected A. stephensi across lifespan, at temperatures that A. stephensi could encounter within its range, and on Plasmodium yoelii-infected mosquitoes during sporogony. We further evaluated treatment effects on retinal sensitivity of uninfected mosquitoes during light and dark periods typically associated with low and high activity for this crepuscular species. Treatment with malaria-associated levels of histamine and 5-HT significantly increased the locomotor activity of A. stephensi across lifespan and enhanced retinal sensitivity to a broad spectrum of wavelengths at the onset of light. This treatment in combination with higher temperatures also increased activity levels and broadened the peak hours of activity of A. stephensi. Notably, these effects were infection dependent. Together, our data suggest that histaminergic and serotonergic signaling within the gut-brain axis of A. stephensi could be targeted to alter mosquito activity and visual sensitivity as the basis for novel transmission-blocking strategies for malaria control.
破坏与主要蚊虫媒介活动相关的行为,如昼夜运动活动和视觉敏感性,是一种新颖且可行的疟疾控制干预措施。昼夜运动活动是节肢动物昼夜节律活动的一种表现,受光照、温度和感染状态等因素影响。生物胺组胺和血清素(5-羟色胺)会随血液摄入,在健康宿主和患有严重疟疾的宿主之间存在差异。它们调节斯氏按蚊体内的疟原虫感染,但在这些研究之前,衰老、温度和感染与摄入的生物胺相互作用影响蚊子行为的程度尚不清楚。我们为斯氏按蚊提供了处于健康和疟疾相关水平的组胺和5-羟色胺,以研究未感染的斯氏按蚊在其整个生命周期内、在其所能遇到的温度范围内以及在约氏疟原虫感染的蚊子处于孢子生殖期时的昼夜运动活动。我们还评估了这些处理对未感染蚊子视网膜敏感性的影响,这些蚊子处于该晨昏性物种通常与低活动和高活动相关的明期和暗期。用疟疾相关水平的组胺和5-羟色胺进行处理显著增加了斯氏按蚊在整个生命周期内的运动活动,并在光照开始时增强了其对广谱波长的视网膜敏感性。这种处理与较高温度相结合还增加了斯氏按蚊的活动水平,并拓宽了其活动高峰期。值得注意的是,这些影响依赖于感染。总之,我们的数据表明,斯氏按蚊肠脑轴内的组胺能和血清素能信号传导可作为靶点,以改变蚊子的活动和视觉敏感性,作为疟疾控制新的传播阻断策略的基础。