Comparative micromechanics of bushcricket ears with and without a specialized auditory fovea region in the crista acustica.

Jan Scherberich,Manuela Nowotny,Alexander Stoessel,Roxana Taszus

doi:10.1098/rspb.2020.0909

Abstract

In some insects and vertebrate species, the specific enlargement of sensory cell epithelium facilitates the perception of particular behaviourally relevant signals. The insect auditory fovea in the ear of the bushcricket Ancylecha fenestrata (Tettigoniidae: Phaneropterinae) is an example of such an expansion of sensory epithelium. Bushcricket ears developed in convergent evolution anatomical and functional similarities to mammal ears, such as travelling waves and auditory foveae, to process information by sound. As in vertebrate ears, sound induces a motion of this insect hearing organ (crista acustica), which can be characterized by its amplitude and phase response. However, detailed micromechanics in this bushcricket ear with an auditory fovea are yet unknown. Here, we fill this gap in knowledge for bushcricket, by analysing and comparing the ear micromechanics in Ancylecha fenestrata and a bushcricket species without auditory fovea (Mecopoda elongata, Tettigoniidae: Mecopodinae) using laser-Doppler vibrometry. We found that the increased size of the crista acustica, expanded by a foveal region in A. fenestrata, leads to higher mechanical amplitudes and longer phase delays in A. fenestrata male ears. Furthermore, area under curve analyses of the organ oscillations reveal that more sensory units are activated by the same stimuli in the males of the auditory fovea-possessing species A. fenestrata. The measured increase of phase delay in the region of the auditory fovea supports the conclusion that tilting of the transduction site is important for the effective opening of the involved transduction channels. Our detailed analysis of sound-induced micromechanics in this bushcricket ear demonstrates that an increase of sensory epithelium with foveal characteristics can enhance signal detection and may also improve the neuronal encoding.

Highlights

In acoustically communicating animals, sound production organs and sound receiving organs coevolve under the pressure of natural and sexual selection [1,2,3]
For the mechano-electrical transduction process, a pronounced phase delay that forms the travelling wave along the hearing organ is needed to open the transduction channels in the sensory cells [31]. It was unknown how an auditory fovea with suspended gradient of stiffness affects the organ mechanics and further transduction. In this comparative study, we investigated in detail the sound-induced organ deflection in bushcricket species with (A. fenestrata) and without (M. elongata) an auditory fovea
In A. fenestrata, the auditory fovea is sexspecific and most distinctly developed in male ears [19], where we found the most pronounced phase delay. This larger phase delay in the male ears was measured at the foveal region that processes the female response call frequency of about 10 kHz [16]

Summary

Introduction

Sound production organs and sound receiving organs coevolve under the pressure of natural (e.g. eavesdropping predators and parasites) and sexual selection (e.g. female choice) [1,2,3]. In the tropical Phaneropterinae species Ancylecha fenestrata, the animals show a different dominant sound frequency in male (about 30 kHz) and female (about 10 kHz) calls and sex-specific differences in the morphology and physiology of the tonotopically organized crista acustica in their sound receiving ears [16,19].

Results

Conclusion