Evolution of directional hearing in moths via conversion of bat detection devices to asymmetric pressure gradient receivers

Significance In most acoustic animals, directional hearing evolved alongside basic ear structure. Pyraloid moths differ because their ears generally function as simple bat detectors with little directional ability. Those pyraloid moths that broadcast mating calls represent a yet more special case, as these species localize sound but the ability evolved well after hearing and may be constrained by fundamental auditory features. Analyzing a species with male calling songs, we report a localization mechanism wherein the membrane structure of each ear affords sharp sensitivity to sound arriving from a distinct angle. Females can thereby track male calls but only via an indirect, curvilinear trajectory. Such inefficiency may characterize specialized perceptual traits that rely on general ones having already undergone extensive prior evolution. Small animals typically localize sound sources by means of complex internal connections and baffles that effectively increase time or intensity differences between the two ears. However, some miniature acoustic species achieve directional hearing without such devices, indicating that other mechanisms have evolved. Using 3D laser vibrometry to measure tympanum deflection, we show that female lesser waxmoths (Achroia grisella) can orient toward the 100-kHz male song, because each ear functions independently as an asymmetric pressure gradient receiver that responds sharply to high-frequency sound arriving from an azimuth angle 30° contralateral to the animal's midline. We found that females presented with a song stimulus while running on a locomotion compensation sphere follow a trajectory 20°–40° to the left or right of the stimulus heading but not directly toward it, movement consistent with the tympanum deflections and suggestive of a monaural mechanism of auditory tracking. Moreover, females losing their track typically regain it by auditory scanning—sudden, wide deviations in their heading—and females initially facing away from the stimulus quickly change their general heading toward it, orientation indicating superior ability to resolve the front–rear ambiguity in source location. X-ray computer-aided tomography (CT) scans of the moths did not reveal any internal coupling between the two ears, confirming that an acoustic insect can localize a sound source based solely on the distinct features of each ear.