A tympanal insect ear exploits a critical oscillator for active amplification and tuning

A 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.