Cochlear Cell Atlas of Two Laryngeal Echolocating Bats—New Evidence for the Adaptive Nervous Physiology in Constant Frequency Bat

Bats have evolved highly adapted auditory mechanisms associated with ecological specialisation. However, there is scattered knowledge about the neurophysiological and cellular basis underlying high-frequency hearing in echolocating bats. Herein, the total cochlear cell atlas of Rhinolophus ferrumequinum (constant frequency (CF) bat) and Myotis pilosus (frequency modulated (FM) bat) was conducted using the 10x Genomics single-nucleus RNA sequencing method. Differences in the proportion of cochlear cell types, especially for the neural cells, were detected between these two bat species. Previously, genes upregulated in the cochlea of CF compared with FM bats, were found to be mostly related to nervous activities. After mapping to the cochlear cell atlas, we found that the upregulated genes were from neural cells, lateral wall cells and neurosensory epithelium cells. A class of specific neurons and associated functions was detected in the cochlea of R. ferrumequinum, revealed by cross-species single-cell transcriptomic analyses. Furthermore, molecular evidence for the differentiation from glial cells to neuronal cells was also uncovered in the cochlea of R. ferrumequinum. Overall, this study identified specific cellular molecular properties that constitute the neuroanatomical evolutionary dynamics underlying distinct echolocating types of bats and provided new molecular evidence for high-frequency hearing of echolocating bats, promoting related studies about ecological adaptation and evolution.