A role for acoustic distortion in novel rapid frequency modulation behaviour in free-flying male mosquitoes

Abstract

We describe a new stereotypical acoustic behaviour by male mosquitoes in response to the fundamental frequency of female flight tones during mating sequences. This male-specific free-flight behaviour consists of phonotactic flight beginning with a steep increase in wing-beat frequency (WBF) followed by rapid frequency modulation (RFM) of WBF in the lead up to copula formation. Male RFM behaviour involves remarkably fast changes in WBF and can be elicited without acoustic feedback or physical presence of the female. RFM features are highly consistent, even in response to artificial tones that do not carry the multi-harmonic components of natural female flight tones. Comparison between audiograms of the robust RFM behaviour and the electrical responses of the auditory Johnston's organ (JO) reveals that the male JO is tuned not to the female WBF per se but, remarkably, to the difference between the male and female WBFs. This difference is generated in the JO responses as a result of intermodulation distortion products (DPs) caused by non-linear interaction between male-female flight tones in the vibrations of the antenna. We propose that male mosquitoes rely on their own flight tones in making use of DPs to acoustically detect, locate and orientate towards flying females. We argue that the previously documented flight-tone harmonic convergence of flying male and female mosquitoes could be a consequence of WBF adjustments so that DPs generated through flight-tone interaction fall within the optimal frequency ranges for JO detection.

Masking of an auditory behaviour reveals how male mosquitoes use distortion to detect females

“…More recently it has been used to study the sensory and neural mechanisms of acoustic (RFM) - [9,10] and of the electrical responses of the auditory Johnston's organ (JO) [9, 11-transduced into electrical signals by several thousand mechanosensory scolopidia, which 51 compose the JO housed in the pedicel at the base of each of the antennae [17]. The mechanics 52 of the antenna are nonlinear; it behaves as a rod that becomes stiffer with increasing 53 displacement [11].…”

“…When the antenna is vibrated by two tones, it generates a strong distortion 54 product (vibration) at a frequency that is the arithmetic difference of these two tones, 55 including those that mimic the wing beat frequency (WBF) of male and female mosquitoes 56 [11][12][13]. Largely because of this nonlinearity, the male JO is tuned overall to detect the 57 difference in frequency between the male's own WBF and that of the female [9,[11][12][13][14]. The 58 bandwidths of the sensory receptors of the JO set upper frequency limits on the phasic 59 electrical responses that can be recorded from the JO [9,[11][12][13][14][15][16].…”

“…Male and female WBFs are 60 above the frequency bandwidth of the JO. It is therefore hypothesized that male mosquitoes 61 must fly to detect and locate females through listening to difference tones [9,[11][12][13][14]. 62 It has long been established that male mosquitoes are attracted by female flight-tones 63 [18][19][20][21][22][23][24][25].…”

“…Male mosquitoes are also attracted to artificial sound sources emitting pure tones that 67 simulate the flight-tones of a conspecific female mosquito [9,10,[22][23][24][25]. Recently, we 68 reported that free-flying male mosquitoes in two different taxonomic sub-families, C. behaviour is defined by its spectrographic characteristics and by the flight path of the flying 72 male; it consists of a steep increase in the male's WBF concomitant with fast phonotactic performed only when the male mosquito has detected, located and reached (within ~5 cm) the 76 sound source and represents an acoustic measure of a mating attempt by the male [9,10].…”

“…All 121 tone presentations lasted for 10 s and the interval between presentations was ~5 s. Three 122 different probe tone frequencies were used, all within the stimulus range for eliciting an RFM 123 response in males [9]: 340 Hz, which is within the 10 dB bandwidth of the JO; 400 Hz,…”