Mechanoelectrical transduction of acoustic signals is the fundamental process for hearing in all ears across the animal kingdom. Here, we performed in vivo laser-vibrometric and electrophysiological measurements at the transduction site in an insect ear (Mecopoda elongata) to relate the biomechanical tonotopy along the hearing organ to the frequency tuning of the corresponding sensory cells. Our mechanical and electrophysiological map revealed a biomechanical filter process that considerably sharpens the neuronal response. We demonstrate that the channel gating, which acts on chordotonal stretch receptor neurons, is based on a mechanical directionality of the sound-induced motion. Further, anatomical studies of the transduction site support our finding of a stimulus-relevant tilt. In conclusion, we were able to show, in an insect ear, that directionality of channel gating considerably sharpens the neuronal frequency selectivity at the peripheral level and have identified a mechanism that enhances frequency discrimination in tonotopically organized ears.

Bushcrickets (katydids) rely on only 20 to 120 sensory units located in their forelegs to sense sound. Situated in tiny hearing organs less than 1 mm long (40× shorter than the human cochlea), they cover a wide frequency range from 1 kHz up to ultrasounds, in tonotopic order. The underlying mechanisms of this miniaturized frequency-place map are unknown. Sensory dendrites in the hearing organ (crista acustica [CA]) are hypothesized to stretch, thereby driving mechanostransduction and frequency tuning. However, this has not been experimentally confirmed. Using optical coherence tomography (OCT) vibrometry, we measured the relative motion of structures within and adjacent to the CA of the bushcricket Mecopoda elongata. We found different modes of nanovibration in the CA that have not been previously described. The two tympana and the adjacent septum of the foreleg that enclose the CA were recorded simultaneously, revealing an antiphasic lever motion strikingly reminiscent of vertebrate middle ears. Over the entire length of the CA, we were able to separate and compare vibrations of the top (cap cells) and base (dorsal wall) of the sensory tissue. The tuning of these two structures, only 15 to 60 μm (micrometer) apart, differed systematically in sharpness and best frequency, revealing a tuned periodic deformation of the CA. The relative motion of the two structures, a potential drive of transduction, demonstrated sharper tuning than either of them. The micromechanical complexity indicates that the bushcricket ear invokes multiple degrees of freedom to achieve frequency separation with a limited number of sensory cells.

Convergent evolution has led to surprising functional and mechanistic similarities between the vertebrate cochlea and some katydid ears [1,2]. Here we report on an 'auditory fovea' (Figure 1A) in the duetting katydid Ancylecha fenestrata (Tettigoniidae). The auditory fovea is a specialized inner-ear region with a disproportionate number of receptor cells tuned to a narrow frequency range, and has been described in the cochlea of some vertebrates, such as bats and mole rats [3,4]. In tonotopically organized ears, the location in the hearing organ of the optimal neuronal response to a tone changes gradually with the frequency of the stimulation tone. However, in the ears of A. fenestrata, the sensory cells in the auditory fovea are tuned to the dominant frequency of the female call; this area of the hearing organ is extensively expanded in males to provide an overrepresentation of this behaviorally important auditory input. Vertebrates developed an auditory fovea for improved prey or predator detection. In A. fenestrata, however, the foveal region facilitates acoustic pair finding, and the sexual dimorphism of sound-producing and hearing organs reflects the asymmetry in the mutual communication system between the sexes (Figures 1B, S1).

From mammals to insects, acoustic communication is in many species crucial for successful reproduction. In the duetting bushcricket , the mutual acoustic communication between males and females is asymmetrical. We investigated how those signalling disparities are reflected by sexual dimorphism of their ears. Both sexes have tympanic ears in their forelegs, but male ears possess a significantly longer crista acustica containing 35% more scolopidia. With more sensory cells to cover a similar hearing range, the male hearing organ shows a significantly expanded auditory fovea that is tuned to the dominant frequency of the female reply to facilitate phonotactic mate finding. This sex-specific auditory fovea is demonstrated in the mechanical and neuronal responses along the tonotopically organized crista acustica by laservibrometric and electrophysiological frequency mapping, respectively. Morphometric analysis of the crista acustica revealed an interrupted gradient in organ height solely within this auditory fovea region, whereas all other anatomical parameters decrease continuously from proximal to distal. Combining behavioural, anatomical, biomechanical and neurophysiological information, we demonstrate evidence of a pronounced auditory fovea as a sex-specific adaptation of an insect hearing organ for intraspecific acoustic communication.

A primary task of auditory systems is the localization of sound sources in space. Sound source localization in azimuth is usually based on temporal or intensity differences of sounds between the bilaterally arranged ears. In mammals, localization in elevation is possible by transfer functions at the ear, especially the pinnae. Although insects are able to locate sound sources, little attention is given to the mechanisms of acoustic orientation to elevated positions. Here we comparatively analyse the peripheral hearing thresholds of three species of bushcrickets in respect to sound source positions in space. The hearing thresholds across frequencies depend on the location of a sound source in the three-dimensional hearing space in front of the animal. Thresholds differ for different azimuthal positions and for different positions in elevation. This position-dependent frequency tuning is species specific. Largest differences in thresholds between positions are found in Ancylecha fenestrata. Correspondingly, A. fenestrata has a rather complex ear morphology including cuticular folds covering the anterior tympanal membrane. The position-dependent tuning might contribute to sound source localization in the habitats. Acoustic orientation might be a selective factor for the evolution of morphological structures at the bushcricket ear and, speculatively, even for frequency fractioning in the ear.