By beating their wings faster around sunset, male Anopheles mosquitoes sensitize their auditory system to female flight tones.
Background Insecticide-treated net (ITN) durability, measured through physical integrity and bioefficacy, must be accurately assessed in order to plan the timely replacement of worn out nets and guide procurement of longer-lasting, cost-effective nets. World Health Organization (WHO) guidance advises that new intervention class ITNs be assessed 3 years after distribution, in experimental huts. In order to obtain information on whole-net efficacy cost-effectively and with adequate replication, a new bioassay, the Ifakara Ambient Chamber Test (I-ACT), a semi-field whole net assay baited with human host, was compared to established WHO durability testing methods. Methods Two experiments were conducted using pyrethroid-susceptible female adult Anopheles gambiae sensu stricto comparing bioefficacy of Olyset ® , PermaNet ® 2.0 and NetProtect ® evaluated by I-ACT and WHO cone and tunnel tests. In total, 432 nets (144/brand) were evaluated using I-ACT and cone test. Olyset ® nets (132/144) that did not meet the WHO cone test threshold criteria (≥ 80% mortality or ≥ 95% knockdown) were evaluated using tunnel tests with threshold criteria of ≥ 80% mortality or ≥ 90% feeding inhibition for WHO tunnel and I-ACT. Pass rate of nets tested by WHO combined standard WHO bioassays (cone/tunnel tests) was compared to pass in I-ACT only by net brand and time after distribution. Results Overall, more nets passed WHO threshold criteria when tested with I-ACT than with standard WHO bioassays 92% vs 69%, (OR: 4.1, 95% CI 3.5–4.7, p < 0.0001). The proportion of Olyset ® nets that passed differed if WHO 2005 or WHO 2013 LN testing guidelines were followed: 77% vs 71%, respectively. Based on I-ACT results, PermaNet ® 2.0 and NetProtect ® demonstrated superior mortality and non-inferior feeding inhibition to Olyset ® over 3 years of field use in Tanzania. Conclusion Ifakara Ambient Chamber Test may have use for durability studies and non-inferiority testing of new ITN products. It measures composite bioefficacy and physical integrity with both mortality and feeding inhibition endpoints, using fewer mosquitoes than standard WHO bioassays (cone and tunnel tests). The I-ACT is a high-throughput assay to evaluate ITN products that work through either contact toxicity or feeding inhibition. I-ACT allows mosquitoes to interact with a host sleeping underneath a net as encountered in the field, without risk to human participants. Electronic supplementary material The online version of this article (10.1186/s12936-019-2741-y) contains supplementary material, which is available to authorized users.
Hearing is an essential sense in the life cycle of malaria mosquitoes. Within large swarms formed transiently at dusk, mosquitoes acoustically recognize their mating partners by their wingbeats. Indeed, malaria mosquitoes only respond to the flight tones of mating partners during swarm time. This phenomenon implies a sophisticated context- and time-dependent modulation of mosquito audition, the mechanisms of which are still largely unknown. Using transcriptomics, we identify a complex network of candidate neuromodulators regulating mosquito hearing. Among them, octopamine stands out as regulator of the auditory performance during swarm time. To explore octopamine roles in mosquito hearing, we carried out an in-depth analysis of octopamine-mediated effects on auditory function. We found that octopamine affects the properties of the mosquito ear on multiple levels: it modulates the tuning and stiffness of the flagellar sound receiver and it controls the erection of antennal fibrillae in males. We found that two different receptors are driving octopamine auditory roles, including a novel beta octopamine receptor. We also demonstrate that the octopaminergic auditory control system can be targeted by insecticides. Our findings identify octopamine signalling as a key component of hearing and mating partner detection in malaria mosquitoes, and as a potential novel target for mosquito control.
Mating swarms of malaria mosquitoes form every day at sunset throughout the tropical world, they typically last less than 30 minutes. Activity patterns must thus be highly synchronized between the sexes. Moreover, males must be able to identify the few sporadically entering females by detecting the females’ faint flight tones. We here show that the Anopheles circadian clock ensures a tight synchrony of male and female activity and –importantly – also retunes the males’ acoustic detection system: by lifting their own flight tones at dusk, males actively enhance the audibility of females. The reported phenomenon of ‘harmonic convergence’ is a random by-product of the mosquitoes’ flight tone variance. Intriguingly, flight tones of individual mosquitoes occupy narrow –partly non-overlapping-frequency ranges, suggesting that the audibility of individual females varies across males.One Sentence SummaryMale mosquitoes sharpen their hearing at sunset.
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