Precopulatory acoustic interactions of the New World malaria vector Anopheles albimanus (Diptera: Culicidae)

Abstract

Background Anopheles albimanus is a malaria vector in Central America, northern South America and the Caribbean. Although a public health threat, An. albimanus precopulatory mating behaviors are unknown. Acoustics play important roles in mosquito communication, where flight tones allow males to detect and attract potential mates. The importance of sound in precopulatory interactions has been demonstrated in Toxorhynchites brevipalpis , Aedes aegypti , Culex quinquefasciatus and Anopheles gambiae ; convergence in a shared harmonic of the wing beat frequency (WBF) during courtship is thought to increase the chance of copulation. To our knowledge, An. albimanus precopulatory acoustic behaviors have not been described to date. Here, we characterized An. albimanus (i) male and female flight tones; (ii) male–female precopulatory acoustic interactions under tethered and free flight conditions; and (iii) male-male acoustic interactions during free flight. Results We found significant increases in the WBFs of both sexes in free flight compared to when tethered. We observed harmonic convergence between 79% of tethered couples. In free flight, we identified a female-specific behavior that predicts mate rejection during male mating attempts: females increase their WBFs significantly faster during mate rejection compared to a successful copulation. This behavior consistently occurred during mate rejection regardless of prior mating attempts (from the same or differing male). During group flight, males of An. albimanus displayed two distinct flying behaviors: random flight and a swarm-like, patterned flight, each associated with distinct acoustic characteristics. In the transition from random to patterned flight, males converged their WBFs and significantly decreased flight area, male-male proximity and the periodicity of their trajectories. Conclusions We show that tethering of An. albimanus results in major acoustic differences compared to free flight. We identify a female-specific behavior that predicts mate rejection during male mating attempts in this species and show that male groups in free flight display distinct flying patterns with unique audio and visual characteristics. This study shows that An. albimanus display acoustic features identified in other mosquito species, further suggesting that acoustic interactions provide worthwhile targets for mosquito intervention strategies. Our results provide compelling evidence for swarming in this species and suggests that acoustic signaling is important for this behavior. Electronic supplementary material The online version of this article (10.1186/s13071-019-3648-8) contains supplementary ma...

Mosquito sound communication: are male swarms loud enough to attract females?

“…found frequency-matching occurred more consistently within pairs of the same molecular form than in hetero-specific pairs [4]. However, in a separate study, a type of acoustic interaction associated with mating (rapid wingbeat frequency modulations) was elicited by males when they were close to a female [6,8,9], but rapid-frequency modulations in males of both An coluzzii and An. gambiae s.s. were similar when exposed to pure tones mimicking the female's fundamental wingbeat frequency [44].…”

“…It is known that male mosquitoes are attracted to a source of female flight tones, either the sound of a live female or a speaker emitting female flight tones. Males and females are both tuned to the 'difference-tone' between their respective wingbeat frequencies, which provides a relatively robust means of locating each other in mating swarms [1][2][3][4]6,8,9,[23][24][25]. This observation raises the hypothesis that females may be attracted to the sound of male swarms, and if so, might they hear larger swarms from a long distance (> 1m)?…”

“…The hearing organs of males and females are tuned to 'difference tones' derived from the combined wingbeat frequencies of both sexes, discernible indirectly by convergence patterns in the wingbeat harmonics of male and uninseminated female mosq,uitoes. This acoustic behaviour has been documented in four species of medical importance (Anopheles gambiae s.l., Anopheles albimanus, Aedes aegypti and Culex quinquefasciatus), plus Toxorhynchites brevipalpis and Culex pipiens [1][2][3][4][5][6][7][8][9][10] as well as in other flies [11].…”

“…In principle, the significant change in her wingbeat frequency increases the strength of the input to the nervous system, thereby increasing her ability to hear and locate the male [3,11]. A change in flight speed which indicates a change in flight trajectory (uninseminated females are observed to fly toward male swarms [9,24,45], but we don't know whether it is due to the swarm sound). Finally, the measured results were extrapolated to estimate how far away a female mosquito can hear a swarm of a given number of males.…”

Assessing the acoustic behaviour ofAnopheles gambiaes.l.dsxFmutants: Implications for Vector Control

“…The relationship between wing beat frequency (= flight tone) and wing length is far more contentious however, with conflicting reports on potential correlations (see e.g. [26,27]). We measured wing lengths for each group and found significant differences between the sexes (Two-way ANOVA; p<0.001; Figure 1c).…”