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High-frequency hearing is important for the survival of both echolocating bats and whales, but our understanding of its genetic basis is scattered and segmented. In this study, we combined RNA-Seq and comparative genomic analyses to obtain insights into the comprehensive gene expression profile of the cochlea and the adaptive evolution of hearing-related genes. A total of 144 genes were found to have been under positive selection in various species of echolocating bats and toothed whales, 34 of which were identified to be related to hearing behavior or auditory processes. Subsequently, multiple physiological processes associated with those genes were found to have adaptively evolved in echolocating bats and toothed whales, including cochlear bony development, antioxidant activity, ion balance, and homeostatic processes, along with signal transduction. In addition, abundant convergent/parallel genes and sites were detected between different pairs of echolocator species; however, no specific hearing-related physiological pathways were enriched by them and almost all of the convergent/parallel signals were selectively neutral, as previously reported. Notably, two adaptive parallel evolved sites in TECPR2 were shown to have been under positive selection, indicating their functional importance for the evolution of echolocation and high-frequency hearing in laryngeal echolocating bats. This study deepens our understanding of the genetic bases underlying high-frequency hearing in the cochlea of echolocating bats and toothed whales.

Evolutionary basis of high-frequency hearing in the cochleae of echolocators revealed by comparative genomics