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

Somers, Jason; Georgiades, Marcos; Su, Matthew P.; Bagi, Judit; Andrés, Marta; Alampounti, Alexandros; Mills, Gordon; Ntabaliba, Watson; Moore, Sarah; Spaccapelo, Roberta; Albert, Joerg T.

doi:10.1126/sciadv.abl4844

Cited by 39 publications

(53 citation statements)

References 41 publications

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“…For instance, species that are thought to use resonant effects are observed to undergo additional notable, but seemingly random, wingbeat frequency variation-for instance, variation of up to 15% in fruit flies [14]. A range of these species are also observed to alter wingbeat frequency in a controlled manner: in honeybees, fruit flies and hawkmoths, as a mechanism of aerodynamic force control [9,[15][16][17], and in mosquitos, for acoustic courtship interactions [18,19]. More complex relationships are also observed: both positive and negative [20,21] correlations between wingbeat frequency and ambient temperature in species of bee and fly, with population-averaged frequency alterations of up to 30% [21].…”

Section: Introductionmentioning

confidence: 99%

“…The operation of sets of pleurosternal and tergopleural muscles has been proposed as a mechanism for time-varying control of the thoracic resonant frequency [9,[22][23][24][25][26], potentially allowing wingbeat frequencies to vary while maintaining a state of continued resonance. Alternatively, behaviour involving intentional frequency control has been motivated in terms of the trade-off between deviating from resonance and achieving other goals: for instance, performing a manoeuvre [9], or engaging in courtship [18]. One of the impediments to understanding these effects, and candidate explanations, is the lack of any clear information on what resonance actually represents in an insect indirect flight motor-and what costs, exactly, would be associated with deviating from resonance.…”

Section: Introductionmentioning

confidence: 99%

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Distinct forms of resonant optimality within insect indirect flight motors

Pons

Beatus

2022

J. R. Soc. Interface.

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Insect flight motors are extraordinary natural structures that operate efficiently at high frequencies. Structural resonance is thought to play a role in ensuring efficient motor operation, but the details of this role are elusive. While the efficiency benefits associated with resonance may be significant, a range of counterintuitive behaviours are observed. In particular, the relationship between insect wingbeat frequencies and thoracic natural frequencies is uncertain, with insects showing wingbeat frequency modulation over both short and long time scales. Here, we offer new explanations for this modulation. We show how, in linear and nonlinear models of an indirect flight motor, resonance is not a unitary state at a single frequency, but a complex cluster of distinct and mutually exclusive states, each representing a different form of resonant optimality. Additionally, by characterizing the relationship between resonance and the state of negative work absorption within the motor, we demonstrate how near-perfect resonant energetic optimality can be maintained over significant wingbeat frequency ranges. Our analysis leads to a new conceptual model of flight motor operation: one in which insects are not energetically restricted to a precise wingbeat frequency, but instead are robust to changes in thoracic and environmental properties—an illustration of the extraordinary robustness of these natural motors.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Distinct forms of resonant optimality within insect indirect flight motors

Pons

Beatus

2022

J. R. Soc. Interface.

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“…Male Ae. aegypti require a highly sensitive, complex hearing organ to overcome the significant acoustic challenges they face in identifying the small number of females in a male-dominated environment ( Somers et al, 2022 ). The mosquito ear is comprised of two parts—a hairy flagellum which acts as a sound sail, and a Johnston’s organ (JO), the site of auditory mechanotransduction equivalent to a mammalian cochlear ( Boo and Richards, 1975b ).…”

Section: Introductionmentioning

confidence: 99%

Serotonin modulation in the male Aedes aegypti ear influences hearing

Loh

Lee

et al. 2022

Front. Physiol.

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Male Aedes aegypti (Ae. aegypti) mosquitoes rely on hearing to identify conspecific females for mating, with the male attraction to the sound of flying females (“phonotaxis”) an important behavior in the initial courtship stage. Hearing thus represents a promising target for novel methods of mosquito control, and hearing behaviors (such as male phonotaxis) can be targeted via the use of sound traps. These traps unfortunately have proven to be relatively ineffective during field deployment. Shifting the target from hearing behavior to hearing function could therefore offer a novel method of interfering with Ae. aegypti mating. Numerous neurotransmitters, including serotonin (5-hydroxytryptamine, or 5-HT) and octopamine, are expressed in the male ear, with modulation of the latter proven to influence the mechanical responses of the ear to sound. The effect of serotonin modulation however remains underexplored despite its significant role in determining many key behaviors and biological processes of animals. Here we investigated the influence of serotonin on the Ae. aegypti hearing function and behaviors. Using immunohistochemistry, we found significant expression of serotonin in the male and female Ae. aegypti ears. In the male ear, presynaptic sites identified via antibody labelling showed only partial overlap with serotonin. Next, we used RT-qPCR to identify and quantify the expression levels of three different serotonin receptor families (5-HT1, 5-HT2, and 5-HT7) in the mosquito heads and ears. Although all receptors were identified in the ears of both sexes, those from the 5-HT7 family were significantly more expressed in the ears relative to the heads. We then thoracically injected serotonin-related compounds into the mosquitoes and found a significant, reversible effect of serotonin exposure on the male ear mechanical tuning frequency. Finally, oral administration of a serotonin-synthesis inhibitor altered male phonotaxis. The mosquito serotonergic system and its receptors thus represent interesting targets for novel methods of mosquito, and thus disease, control.

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“…It is also hypothesized that SSOs of the male flagellum act as amplifiers of the female wingbeats to increase the power of the DPs generated (7), and as such, facilitate the detection of the female. Moreover, recent research shows that males increase their wingbeat frequencies at swarm time thereby enhancing the audibility of females (57). Our data show that the SSO frequency increases at swarm time ZT12 and that octopamine exposure also causes a shift of the SSO frequency to higher frequencies (Fig.…”

Section: Discussionmentioning

confidence: 99%

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

Georgiades

Alampounti

Somers

et al. 2022

Preprint

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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.

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

Abstract: By beating their wings faster around sunset, male Anopheles mosquitoes sensitize their auditory system to female flight tones.

Cited by 39 publications

References 41 publications

Distinct forms of resonant optimality within insect indirect flight motors

Distinct forms of resonant optimality within insect indirect flight motors

Serotonin modulation in the male Aedes aegypti ear influences hearing

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

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