Abstract
For echolocating bats, hearing is essential for survival. Specializations for detecting and processing high frequency sounds are apparent throughout their auditory systems. Recent studies on echolocating mammals have reported evidence of parallel evolution in some hearing-related genes in which distantly related groups of echolocating animals (bats and toothed whales), cluster together in gene trees due to apparent amino acid convergence. However, molecular adaptations can occur not only in coding sequences, but also in the regulation of gene expression. The aim of this study was to examine the expression of hearing-related genes in the inner ear of developing big brown bats, Eptesicus fuscus, during the period in which echolocation vocalizations increase dramatically in frequency. We found that seven genes were significantly upregulated in juveniles relative to adults, and that the expression of four genes through development correlated with estimated age. Compared to available data for mice, it appears that expression of some hearing genes is extended in juvenile bats. These results are consistent with a prolonged growth period required to develop larger cochlea relative to body size, a later maturation of high frequency hearing, and a greater dependence on high frequency hearing in echolocating bats.
Highlights
Echolocating bats have among the highest frequency hearing in the animal kingdom [1]
Expression was higher in adults for six genes—bone morphogenic protein 7 (Bmp7), carcinoembryonic antigen-related cell adhesion molecule 16 (Ceacam16), collagen type XI alpha 2 chain (Col11A2), POU class 4 transcription factor 3 (Pou4f3), transmembrane channel-like 2 (Tmc2), and USH1 protein network component harmonin (Ush1C), and higher in juveniles for the remaining two genes—gap junction protein beta 2 (Gjb2) and POU class 3 transcription factor 4 (Pou3f4)
Linear fits of adjusted fold change to estimated age revealed that juvenile age over a two-week period predicted expression for four genes: POU class 3 transcription factor 4 (Pou3f4), transmembrane channel-like 1 (Tmc1), and gap junction protein beta 2 (Gjb2) and 6 (Gjb6; Table 3; Fig 2)
Summary
Echolocating bats have among the highest frequency hearing in the animal kingdom [1]. While high frequency hearing confers a survival benefit to many animals, it is essential for the survival of bats, because they rely on echolocation to avoid obstacles, obtain food, and find roosts and conspecifics. High frequencies allow bats to control the directionality of calls [2], [3], determine distance to targets [4], reject non-target echo clutter [5], and resolve fine spatial details such as shape, size, and texture [6,7,8]. The need for echolocation throughout life suggests that the ability to hear high frequencies without severe age-related deterioration may have been under positive selection in echolocating bats.
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