Harmonic convergence coordinates swarm mating by enhancing mate detection in the malaria mosquito Anopheles gambiae

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.

Flight-tone mediated circadian control of audibility in mating swarms of Anopheles mosquitoes

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.

Synchronized swarming: Harmonic convergence and acoustic mating dynamics in the malaria mosquito Anopheles gambiae

The mosquito Anopheles gambiae is a major African malaria vector, transmitting parasites responsible for significant mortality and disease burden. Malaria declines have stagnated recently due to widespread insecticide resistance among vector populations. Flight acoustics are essential to mosquito mating biology and represent promising alternative targets for mosquito control. However, mosquito swarm acoustics data are limited. 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 elevated male or female flight tone frequencies and amplitudes during swarming flight with gradual declines to pre-swarm levels over an approximately 35-min period. Analysis of mixed-sex swarms revealed additional increases in flight tone frequencies and amplitudes due to mating activity. Data from mixed-sex swarms suggest harmonic convergence during swarming enhances the efficiency of female detection by synchronizing male and female baseline swarm tones. Further, data from experiments using female swarm tone playbacks to males indicate that harmonic convergence during mating interactions coordinates male scramble competition by acoustically masking mating couple flight tones. These findings advance our knowledge of mosquito swarm acoustics, providing vital information for reproductive control strategies.

Sexual selection theory meets disease vector control: Testing harmonic convergence as a “good genes” signal in Aedes aegypti mosquitoes

Background The mosquito Aedes aegypti is a medically important, globally distributed vector of the viruses that cause dengue, yellow fever, chikungunya, and Zika. Although reproduction and mate choice are key components of vector population dynamics and control, our understanding of the mechanisms of sexual selection in mosquitoes remains poor. In “good genes” models of sexual selection, females use male cues as an indicator of both mate and offspring genetic quality. Recent studies in Ae. aegypti provide evidence that male wingbeats may signal aspects of offspring quality and performance during mate selection in a process known as harmonic convergence. However, the extent to which harmonic convergence may signal overall inherent quality of mates and their offspring remains unknown. Methodology/Principal findings To examine this, we measured the relationship between acoustic signaling and a broad panel of parent and offspring fitness traits in two generations of field-derived Ae. aegypti originating from dengue-endemic field sites in Thailand. Our data show that in this population of mosquitoes, harmonic convergence does not signal male fertility, female fecundity, or male flight performance traits, which despite displaying robust variability in both parents and their offspring were only weakly heritable. Conclusions/Significance Together, our findings suggest that vector reproductive control programs should treat harmonic convergence as an indicator of some, but not all aspects of inherent quality, and that sexual selection likely affects Ae. aegypti in a trait-, population-, and environment-dependent manner.

Sex, age, and parental harmonic convergence behavior affect the immune performance of Aedes aegypti offspring

Harmonic convergence is a potential cue, female mosquitoes use to choose male mates. However, very little is known about the benefits this choice confers to offspring performance. Using Aedes aegypti (an important vector of human disease), we investigated whether offspring of converging parental pairs showed differences in immune competence compared to offspring derived from non-converging parental pairs. Here we show that harmonic convergence, along with several other interacting factors (sex, age, reproductive, and physiological status), significantly shaped offspring immune responses (melanization and response to a bacterial challenge). Harmonic convergence had a stronger effect on the immune response of male offspring than on female offspring. Further, female offspring from converging parental pairs disseminated dengue virus more quickly than offspring derived from non-converging parental pairs. Our results provide insight into a wide range of selective pressures shaping mosquito immune function and could have important implications for disease transmission and control.

Sexual selection theory meets disease vector control: Testing harmonic convergence as a “good genes” signal in Aedes aegypti mosquitoes

The mosquito Aedes aegypti is a medically important, globally distributed vector of the viruses that cause dengue, yellow fever, chikungunya, and Zika. Although reproduction and mate choice are key components of vector population dynamics and control, our understanding of the mechanisms of sexual selection in mosquitoes remains poor. In “good genes” models of sexual selection, females use male cues as an indicator of both mate and offspring inherent genetic quality. Recent studies in Ae. aegypti provide evidence that male wingbeat acoustics signal aspects of offspring quality and performance during mate selection in a process known as harmonic convergence. However, the extent to which harmonic convergence may signal overall inherent quality of mates and their offspring remains unknown. To examine this, we measured the potential acoustic signaling and heritability of a broad panel of parent and offspring fitness traits in two generations of field-derived Ae. aegypti originating from dengue endemic field sites in Thailand. Our data show that in this population of mosquitoes, harmonic convergence does not signal male fertility, female fecundity, and male flight performance traits, which despite displaying robust variability in both parents and their offspring were only weakly heritable. Together with previous work, our findings suggest that vector reproductive control programs should treat harmonic convergence as an indicator of some, but not all aspects of inherent quality, and that multiple forms of sexual selection are likely at play in Ae. aegypti in a trait, population, and environment dependent manner.

Competing Cultures: A New Age in Chaco Canyon

Chaco Culture National Historical Park was founded to protect and preserve the archaeological remains of a complex pre-Hispanic American Southwestern society. The 1987 celebration of the Harmonic Convergence in Chaco Canyon forced the park to re-examine its museum collection policies. A new cultural use of the park arose with modern “offerings” left in archaeological sites by non-Native visitors. At the same time, Native American descendant communities were finding their political voices and making themselves heard by federal land managers. Managing the physical manifestations of competing cultural uses has evolved over time at Chaco, in response to descendant communities, “New Age” practitioners, and researchers.

Sex, Age, and Parental Harmonic Convergence Behavior Affect the Immune Performance of Aedes aegypti Offspring

Aedes aegypti is an important vector of several pathogenic arboviruses including dengue, chikungunya and Zika. Innovative approaches to control Aedes populations, involving synthetic transgenic modifications as well as Wolbachia bacteria, appear promising. For the various techniques requiring offspring inheritance of a trait, released males must successfully compete for mating partners against wildtype males. However, very little is known about mechanisms of mate selection in mosquitoes in general and in particular about potential correlations between mating success and offspring immune performance.Harmonic convergence signals have been proposed as a cue for females to predict male quality. We investigated whether offspring of converging parental pairs showed differences in immune competence compared to offspring derived from non-converging parental pairs using three different types of immune assays. We found that offspring immune responses (melanization response and response to a bacterial challenge) differed between offspring from converging and non-converging parents. However, immune responses were shaped by several interacting factors such as sex, age, reproductive status, and parental mating behavior. Parental mating behavior had a stronger effect on the immune response of male offspring than on female offspring. Further, a population of female offspring derived from converging parental pairs reached their peak dengue virus dissemination rate earlier compared to a population of offspring derived from non-converging parental pairs. Our results provide insight into a wide range of selective pressures shaping mosquito immune function. Evolutionary trade-offs between naturally and sexually selected traits can have important implications for disease transmission and control and should be considered in the development of reproductive control strategies.