Lung mediated auditory contrast enhancement improves the Signal-to-noise ratio for communication in frogs

Abstract

Environmental noise is a major source of selection on animal sensory and communication systems. The acoustic signals of other animals represent particularly potent sources of noise for chorusing insects, frogs, and birds, which contend with a multi-species analog of the human "cocktail party problem" (i.e., our difficulty following speech in crowds). However, current knowledge of the diverse adaptations that function to solve noise problems in nonhuman animals remains limited. Here, we show that a lung-to-ear sound transmission pathway in frogs serves a heretofore unknown noise-control function in vertebrate hearing and sound communication. Inflated lungs improve the signal-to-noise ratio for communication by enhancing the spectral contrast in received vocalizations in ways analogous to signal processing algorithms used in hearing aids and cochlear implants. Laser vibrometry revealed that the resonance of inflated lungs selectively reduces the tympanum's sensitivity to frequencies between the two spectral peaks present in conspecific mating calls. Social network analysis of continent-scale citizen science data on frog calling behavior revealed that the calls of other frog species in multi-species choruses can be a prominent source of environmental noise attenuated by the lungs. Physiological modeling of peripheral frequency tuning indicated that inflated lungs could reduce both auditory masking and suppression of neural responses to mating calls by environmental noise. Together, these data suggest an ancient adaptation for detecting sound via the lungs has been evolutionarily co-opted to create auditory contrast enhancement that contributes to solving a multi-species cocktail party problem.