Sex Recognition through Midflight Mating Duets in Culex Mosquitoes Is Mediated by Acoustic Distortion

Abstract

Sexual recognition through wing-beat frequency matching was first demonstrated in Toxorhynchites brevipalpis, where wing-beat frequencies of males and females are similar. Here we show frequency matching in Culex quinquefasciatus, where the wing-beat frequencies of males and females differ considerably. The wing-beat frequencies converge not on the fundamental but on the nearest shared harmonic (usually female's third and male's second). Frequencies in this range are, however, too high to elicit phasic sensory-neural responses from the Johnston's organ (JO) or to drive the mosquito's motor neurons. Potential cues for frequency matching are difference tones produced by nonlinear mixing of male and female flight tones in the vibrations of the mosquito's antennae. Receptor potentials and neural-motor activity were recorded in response to difference tones produced when a mosquito was stimulated simultaneously by two tones at frequencies outside the phasic response range of the JO but within range of the antennal vibrations. We demonstrate sexual recognition through matching of flight-tone harmonics in Culex mosquitoes and suggest that difference tones are used as an error signal for frequency matching beyond the frequency range of the JO's sensory-neural range. This is the first report of acoustic distortion being exploited as a sensory cue, rather than existing as an epiphenomenon.

Efficient Encoding of Vocalizations in the Auditory Midbrain

“…The distortion product with the highest intensity generated through this mechanism ( f 2 Ϫ f 1 ) falls within the FRA of this neuron, perhaps causing its response. Neural sensitivity to cochlear distortion products has been documented previously throughout the auditory system (Goldstein and Kiang, 1968;McAlpine, 2004;Abel and Kössl, 2009;Portfors et al, 2009) and has been proposed as a mechanism for providing sensory cues in communication Warren et al, 2009). …”

Comparative Aspects of Hearing in Vertebrates and Insects with Antennal Ears

“…Rather than giving a comprehensive view on acoustic communication in mosquitoes, and on the role of the transducer machinery therein, we would like to concentrate on one particular example that showcases how the very periphery of hearing may preprocess and analyse sound. For three species it has been reported that the wingbeat-matching behavior results in a convergence of higher harmonics rather than of the fundamental frequencies [41,43,47]. In all three cases a match appears to be achieved around the second harmonic of the male wingbeat (M2) and the third harmonic of the female wingbeat (F3; Figure 1D).…”

“…Males detect, locate and chase females by detecting, locating and chasing a female flight tone [40]. Both sexes, in turn, have been reported to respond to each other's wingbeat frequencies by modulating their own [41][42][43], an acoustic behavior thought to mediate male-female interactions within larger mating swarms. Just as in Drosophila, mosquito antennae have been reported to be active, nonlinear oscillators of exquisite nanometer-range sensitivity [23,[44][45][46], with the source of the observed activity and nonlinearity likely (A) When stimulated by pure tones at its best frequency, the wild-type Drosophila antennal receiver displays a compressive nonlinearity, which produces relatively larger displacements for smaller stimuli (particle velocities), depicted by the green curve.…”

“…Intriguingly, the solution to this sensitivity dilemma that the sensory periphery faces has been suggested to come from the sensory periphery itself [43,48]. It is a key feature of active hearing organs that the nonlinearities of the system together with an inherent reciprocity of force transmission must lead to the generation of distortion products [5].…”

“…In all three cases a match appears to be achieved around the second harmonic of the male wingbeat (M2) and the third harmonic of the female wingbeat (F3; Figure 1D). For a 'prototypical' mosquito species with a male wingbeat of $600 Hz and a female wingbeat of $400 Hz, this would result in a convergence at a frequency of $1,200 Hz, which is commonly assumed to be considerably above the range of antennal mechanical sensitivity and thus above the mosquito hearing range.Intriguingly, the solution to this sensitivity dilemma that the sensory periphery faces has been suggested to come from the sensory periphery itself [43,48]. It is a key feature of active hearing organs that the nonlinearities of the system together with an inherent reciprocity of force transmission must lead to the generation of distortion products [5].…”