Cetaceans on a molecular fast track to ultrasonic hearing

Abstract

The early radiation of cetaceans coincides with the origin of their defining ecological and sensory differences [1, 2]. Toothed whales (Odontoceti) evolved echolocation for hunting 36-34 million years ago, whereas baleen whales (Mysticeti) evolved filter feeding and do not echolocate [2]. Echolocation in toothed whales demands exceptional high-frequency hearing [3], and both echolocation and ultrasonic hearing have also evolved independently in bats [4, 5]. The motor protein Prestin that drives the electromotility of the outer hair cells (OHCs) is likely to be especially important in ultrasonic hearing, because it is the vibratory response of OHC to incoming sound waves that confers the enhanced sensitivity and selectivity of the mammalian auditory system [6, 7]. Prestin underwent adaptive change early in mammal evolution [8] and also shows sequence convergence between bats and dolphins [9, 10], as well as within bats [11]. Focusing on whales, we show for the first time that the extent of protein evolution in Prestin can be linked directly to the evolution of high-frequency hearing. Moreover, we find that independent cases of sequence convergence in mammals have involved numerous identical amino acid site replacements. Our findings shed new light on the importance of Prestin in the evolution of mammalian hearing.