A Tympanal Insect Ear Exploits a Critical Oscillator for Active Amplification and Tuning

Abstract

SummaryA dominant theme of acoustic communication is the partitioning of acoustic space into exclusive, species-specific niches to enable efficient information transfer. In insects, acoustic niche partitioning is achieved through auditory frequency filtering, brought about by the mechanical properties of their ears [1]. The tuning of the antennal ears of mosquitoes [2] and flies [3], however, arises from active amplification, a process similar to that at work in the mammalian cochlea [4]. Yet, the presence of active amplification in the other type of insect ears—tympanal ears—has remained uncertain [5]. Here we demonstrate the presence of active amplification and adaptive tuning in the tympanal ear of a phylogenetically basal insect, a tree cricket. We also show that the tree cricket exploits critical oscillator-like mechanics, enabling high auditory sensitivity and tuning to conspecific songs. These findings imply that sophisticated auditory mechanisms may have appeared even earlier in the evolution of hearing and acoustic communication than currently appreciated. Our findings also raise the possibility that frequency discrimination and directional hearing in tympanal systems may rely on physiological nonlinearities, in addition to mechanical properties, effectively lifting some of the physical constraints placed on insects by their small size [6] and prompting an extensive reexamination of invertebrate audition.

Active auditory mechanics in female black-horned tree crickets (Oecanthus nigricornis)

“…This peak may be due to incomplete anaesthesia of the animals or perhaps some other non-specific effect of the anaesthetic. As has been reported previously in O. henryi (Mhatre and Robert 2013), a smaller animal than O. nigricornis, full anaesthesia takes at least 30 minutes of CO2 exposure. This is a long time, but may not be sufficient to completely switch off the active mechanics in all of the O. nigricornis measured here.…”

“…We expect the best frequency of the female ear to fall within the range of male calls and also anticipate finding active auditory mechanics similar to those found in the Indian O. henryi (Mhatre and Robert 2013). We also examine the presence of SOs in the absence of acoustic stimuli and the physiological vulnerability of the auditory mechanics in both CO2 anaesthetised animals and post mortem.…”

“…These characteristics are also seen in the Indian tree cricket O. henryi (Mhatre and Robert 2013) suggesting that these characteristics of active amplification may be widespread in auditory systems in the genus Oecanthus, and it remains to be seen whether other Gryllids show similar nonlinear and potentially active auditory dynamics.…”

“…In vertebrates too, hair cells are motile and actively produce auditory nonlinearities (Manley et al 2008). As the auditory scolopidia in Oecanthus lie near the position of maximal displacement on the membrane (Mhatre and Robert 2013), and as other active auditory systems employ motile mechanosensory cells that generate nonlinearities (Göpfert and Robert 2007), it is highly probable that mechanosensory cells are responsible for the motion generation in the tree cricket anterior TM.…”

“…To achieve this many animals have evolved a nonlinear auditory response, whereby the receiver shows increased sensitivity to quiet sounds and sensory cells selectively and actively tune into frequencies of interest. Auditory nonlinearities are known across all vertebrate groups (Manley 2000;Manley et al 2008) and in insects have been found in mosquitoes (Göpfert and Robert 2001), Drosophila (Göpfert and Robert 2003) and the tree cricket, O. henryi (Mhatre and Robert 2013). The female O. henryi auditory system becomes selectively tuned into male call frequencies at low amplitudes, but at high stimulus amplitudes this tuning is lost.…”