Hitting the right note at the right time: Circadian control of audibility in Anopheles mosquito mating swarms is mediated by flight tones.
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ABSTRACT:
SUBMITTER: Somers J
PROVIDER: S-EPMC8754303 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:An important element of mating in the malaria vector Anopheles gambiae Giles in nature is the crepuscular mating aggregation (swarm) composed almost entirely of males, where most coupling and insemination is generally believed to occur. In this study, we mathematically characterize the oscillatory movement of male An. gambiae in terms of an established individual-based mechanistic model that parameterizes the attraction of a mosquito toward the center of the swarm using the natural frequency of oscillation and the resistance to its motion, characterized by the damping ratio. Using three-dimensional trajectory data of ten wild mosquito swarms filmed in Mali, Africa, we show two new results for low and moderate wind conditions, and indicate how these results may vary in high wind. First, we show that in low and moderate wind the vertical component of the mosquito motion has a lower frequency of oscillation and higher damping ratio than horizontal motion. In high wind, the vertical and horizontal motions are similar to one another and the natural frequencies are higher than in low and moderate wind. Second, we show that the predicted average disagreement in the direction of motion of swarming mosquitoes moving randomly is greater than the average disagreement we observed between each mosquito and its three closest neighbors, with the smallest level of disagreement occurring for the nearest neighbor in seven out of 10 swarms. The alignment of the direction of motion between nearest neighbors is the highest in high wind. This result provides evidence for flight-path coordination between swarming male mosquitoes.
| S-EPMC4780853 | biostudies-literature
Project description:Mosquito flight produces a tone as a side effect of wing movement; this tone is also a communication signal that is frequency-modulated during courtship. Recordings of tones produced by tethered flying male and female Aedes aegypti were undertaken using pairs of pressure-gradient microphones above and below, ahead and behind, and to the left and right over a range of distances. Fundamental frequencies were close to those previously reported, although amplitudes were lower. The male fundamental frequency was higher than that of the female and males modulated it over a wider range. Analysis of harmonics shows that the first six partials were nearly always within 1 Hz of integer multiples of the fundamental, even when the fundamental was being modulated. Along the front-back axis, amplitude attenuated as a function of distance raised to the power 2.3. Front and back recordings were out of phase, as were above and below, while left and right were in phase. Recordings from ahead and behind showed quadratic phase coupling, while others did not. Finally, two methods are presented for separating simultaneous flight tones in a single recording and enhancing their frequency resolution. Implications for mosquito behavior are discussed.
| S-EPMC3985972 | biostudies-other
Project description:Background: Malaria mosquitoes form mating swarms around sunset, often at the same locations for months or years. Unfortunately, studies of Anopheles swarms are rare in East Africa, the last recorded field observations in Tanzania having been in 1983. Methods: Mosquito swarms were surveyed by trained volunteers between August-2016 and June-2017 in Ulanga district, Tanzania. Identified Anopheles swarms were sampled using sweep nets, and collected mosquitoes killed by refrigeration then identified by sex and taxa. Sub-samples were further identified by PCR, and spermatheca of females examined for mating status. Mosquito ages were estimated by observing female ovarian tracheoles and rotation of male genitalia. GPS locations, types of swarm markers, start/end times of swarming, heights above ground, mosquito counts/swarm, and copulation events were recorded. Results: A total of 216 Anopheles swarms were identified, characterized and mapped, from which 7,142 Anopheles gambiae s.l and 13 Anopheles funestus were sampled. The An. gambiae s.l were 99.6% males and 0.4% females, while the An. funestus were all males. Of all An. gambiae s.l analyzed by PCR, 86.7% were An. arabiensis, while 13.3% returned non-amplified DNA. Mean height (±SD) of swarms was 2.74±0.64m, and median duration was 20 (IQR; 15-25) minutes. Confirmed swarm markers included rice fields (25.5%), burned grounds (17.2%), banana trees (13%), brick piles (8.8%), garbage heaps (7.9%) and ant-hills (7.4%). Visual estimates of swarm sizes by the volunteers was strongly correlated to actual sizes by sweep nets (R=0.94; P=<0.001). All females examined were nulliparous and 95.6% [N=6787] of males had rotated genitalia, indicating sexual maturity. Conclusions: This is the first report of Anopheles swarms in Tanzania in more than three decades. The study demonstrates that the swarms can be identified and characterized by trained community-based volunteers, and highlights potential new interventions, for example targeted aerosol spraying of the swarms to improve malaria control.
| S-EPMC5691375 | biostudies-literature
Project description:The Anopheles gambiae species complex comprises the primary vectors of malaria in much of sub-Saharan Africa. Most of the mating in these species occurs in swarms composed almost entirely of males. Intermittent, organized patterns in such swarms have been observed, but a detailed description of male-male interactions has not previously been available. We identify frequent, time-varying interactions characterized by periods of parallel flight in data from 8 swarms of Anopheles gambiae and 3 swarms of Anopheles coluzzii filmed in 2010 and 2011 in the village of Donéguébogou, Mali. We use the cross correlation of flight direction to quantify these interactions and to induce interaction graphs, which show that males form synchronized subgroups whose size and membership change rapidly. A swarming model with damped springs between each male and the swarm centroid shows good agreement with the correlation data, provided that local interactions represented by damping of relative velocity between males are included.
| S-EPMC4161964 | biostudies-other
Project description:Anopheles gambiae sensu stricto is the major vector of malaria, a disease with devastating consequences for human health. Given the constant spread of the disease, alternative approaches to the use of insecticides are urgently needed to control vector populations. Females of this species undergo large behavioral changes after mating, which include a life-long refractoriness to further insemination and the induction of egg laying in blood-fed individuals. Genetic control strategies aimed at impacting Anopheles fertility through the release of sterile males are being advocated to reduce the size of mosquito field populations. Such strategies depend on the ability of the released sterile males to mate successfully with wild females and to switch off the female receptivity to further copulation. Here we evaluate the role of sperm in regulating female behavioral responses after mating in An. gambiae. We developed spermless males by RNAi silencing of a germ cell differentiation gene. These males mated successfully and preserved standard accessory gland functions. Females mated to spermless males exhibited normal postcopulatory responses, which included laying large numbers of eggs upon blood feeding and becoming refractory to subsequent insemination. Moreover, spermless males induced transcriptional changes in female reproductive genes comparable to those elicited by fertile males. Our data demonstrate that, in contrast to Drosophila, targeting sperm in An. gambiae preserves normal male and female reproductive behavior for the traits and time frame analyzed and validate the use of approaches based on incapacitation or elimination of sperm for genetic control of vector populations to block malaria transmission.
| S-EPMC3158155 | biostudies-literature
Project description:The mosquito Anopheles gambiae is a major African malaria vector, transmitting parasites responsible for significant mortality and disease burden. Although flight acoustics are essential to mosquito mating and present promising alternatives to insecticide-based vector control strategies, there is limited data on mosquito flight tones during swarming. Here, for the first time, we present detailed analyses of free-flying male and female An. gambiae flight tones and their harmonization (harmonic convergence) over a complete swarm sequence. Audio analysis of single-sex swarms showed synchronized elevation of male and female flight tones during swarming. Analysis of mixed-sex swarms revealed additional 50 Hz increases in male and female flight tones due to mating activity. Furthermore, harmonic differences between male and female swarm tones in mixed-sex swarms and in single-sex male swarms with artificial female swarm audio playback indicate that frequency differences of approximately 50 Hz or less at the male second and female third harmonics (M2:F3) are maintained both before and during mating interactions. This harmonization likely coordinates male scramble competition by maintaining ideal acoustic recognition within mating pairs while acoustically masking phonotactic responses of nearby swarming males to mating females. These findings advance our knowledge of mosquito swarm acoustics and provide vital information for reproductive control strategies.
| S-EPMC8677761 | biostudies-literature
Project description:The role of adipokinetic hormones (AKHs) in the regulation of carbohydrate and lipid metabolism and flight performance was evaluated for females of the African malaria mosquito, Anopheles gambiae. Injection of various dosages of synthetic Anoga-AKH-I increased carbohydrate levels in the haemolymph and reduced glycogen reserves in sugar-fed females but did not affect lipid levels. Anoga-AKH-I enhanced the flight performance of both intact and decapitated sugar-fed females, during a 4 h flight period. Anoga-AKH-II had no effect on carbohydrate or lipid levels or flight performance, thus its function remains unknown. Targeted RNA-interference lowered Anoga-AKH receptor expression in sugar-fed females, consequently injections of Anoga-AKH-I failed to mobilize glycogen reserves. Taken together, these results show that a primary role for the neurohormone, Anoga-AKH-I, is to elevate trehalose levels in the haemolymph of female mosquitoes.
| S-EPMC2267862 | biostudies-literature
Project description:BackgroundAnopheles gambiae continues to be widespread and an important malaria vector species complex in Uganda. New approaches to malaria vector control are being explored including population suppression through swarm reductions and genetic modification involving gene drives. Designing and evaluating these new interventions require good understanding of the biology of the target vectors. Anopheles mosquito swarms have historically been hard to locate in Uganda and therefore have remained poorly characterized. In this study we sought to identify and characterize An. gambiae s.l mosquito swarms in three study sites of high An. gambiae s.l prevalence within Central Uganda.MethodsNine sampling visits were made to three villages over a 2-year period. Sampling targeted both wet and dry seasons and was done for 2 days per village during each trip, using sweep nets. All swarm data were analysed using the JMP 14 software (SAS Institute, Inc., Cary, NC, USA), parametrically or non-parametrically as appropriate.ResultsMost of the An. gambiae s.s. swarms sampled during this study were single-species swarms. However, some mixed An. gambiae s.s. and Culex spp. mosquito swarms were also observed. Swarms were larger in the wet season than in the dry season. Mean swarm height ranged from 2.16 m to 3.13 m off the ground and only varied between villages but not by season. Anopheles gambiae mosquitoes were present in all three villages, preferred to swarm over bare ground markers, and could be effectively sampled by field samplers.ConclusionsThis study demonstrated that An. gambiae s.l swarms could be effectively located and sampled in South Central Uganda and provided in-depth descriptions of hitherto poorly understood aspects of An. gambiae local swarm characteristics. Swarms were found close to inhabited households and were greater in size and number during the rainy season. Anopheles gambiae s.s swarms were significantly associated with bare ground markers and were sometimes at heights over 4 m above the ground, showing a necessity to develop tools suitable for swarm sampling at these heights. While mixed species swarms have been reported before elsewhere, this is the first documented instance of mixed genus swarms found in Uganda and should be studied further as it could have implications for swarm sampling explorations where multiple species of mosquitoes exist.
| S-EPMC10956327 | biostudies-literature
Project description:Many arboviral proteins are phosphorylated in infected mammalian cells, but it is unknown if the same phosphorylation events occur when insects are similarly infected. One of the mammalian kinases responsible for phosphorylation, protein kinase G (PKG), has been implicated in the behavior of multiple nonvector insects, but is unstudied in mosquitoes. PKG from Aedes aegypti was cloned, and phosphorylation of specific viral sites was monitored by mass spectrometry from biochemical and cell culture experiments. PKG from Aedes mosquitoes is able to phosphorylate dengue nonstructural protein 5 (NS5) at specific sites in cell culture and cell-free systems and autophosphorylates its own regulatory domain in a cell-free system. Injecting Aedes aegypti and Anopheles gambiae mosquitoes with a pharmacological PKG activator resulted in increased Aedes wing activity during periods of their natural diurnal/crepuscular activity and increased Anopheles nocturnal locomotor/flight activity. Thus, perturbation of the PKG signaling pathway in mosquitoes alters flight behavior. The demonstrated effect of PKG alterations is consistent with a viral PKG substrate triggering increased PKG activity. This increased PKG activity could be the mechanism by which dengue virus increases flight behavior and possibly facilitates transmission. Whether or not PKG is part of the mechanism by which dengue increases flight behavior, this report is the first to show PKG can modulate behavior in hematophagous disease vectors.
| S-EPMC3741427 | biostudies-literature
Project description:Malaria control programs are being jeopardized by the spread of insecticide resistance in mosquito vector populations. It has been estimated that the spread of resistance could lead to an additional 120000 deaths per year, and interfere with the prospects for sustained control or the feasibility of achieving malaria elimination. Another complication for the development of resistance management strategies is that, in addition to insecticide resistance, mosquito behavior evolves in a manner that diminishes the impact of LLINs and IRS. Mosquitoes may circumvent LLIN and IRS control through preferential feeding and resting outside human houses and/or being active earlier in the evening before people go to sleep. Recent developments in our understanding of mosquito swarming suggest that new tools targeting mosquito swarms can be designed to cut down the high reproductive rate of malaria vectors. Targeting swarms of major malaria vectors may provide an effective control method to counteract behavioral resistance developed by mosquitoes. Here, we evaluated the impact of systematic spraying of swarms of Anopheles gambiae s.l. using a mixed carbamate and pyrethroid aerosol. The impact of this intervention on vector density, female insemination rates and the age structure of males was measured. We showed that the resulting mass killing of swarming males and some mate-seeking females resulted in a dramatic 80% decrease in population size compared to a control population. A significant decrease in female insemination rate and a significant shift in the age structure of the male population towards younger males incapable of mating were observed. This paradigm-shift study therefore demonstrates that targeting primarily males rather than females, can have a drastic impact on mosquito population.
| S-EPMC5344402 | biostudies-literature