Mole-rats play evolution by ear

Abstract

Scuttling around their burrows, mole-rats can kick up a bit of a racket, calling out in the dark to their extensive family. Surprisingly, naked mole-rats and their close relatives Damaraland mole-rats have terrible hearing, especially compared with other rodents. Mole-rats have no outer ears and the vibration-sensing hair cells in their inner ear are weirdly connected to their nerves, but neither feature totally explains why they are nearly deaf. Why they evolved bad hearing is a mystery too. They might have lost hearing over time like other subterranean animals lost sight. Alternatively, poor hearing could be an advantage, dampening echoes in noisy burrows. Sonja Pyott from the University of Groningen, The Netherlands, and colleagues investigated the physiological and evolutionary causes of mole-rats’ poor hearing.First, the authors did a mole-rat hearing test to see what sounds got their inner ear – the cochlea – talking to their brain and found that naked and Damaraland mole-rat ears respond to tones between 0.5 and 4 kHz or 2 kHz, respectively, a narrower and lower range than for other rodents. Next, the authors did a full auditory system workup, seeking a physiological mechanism to explain why mole-rats are hard of hearing. As hair cells vibrate in response to incoming sounds, they make noises called otoacoustic emissions. Typically, otoacoustic emissions increase with louder noises and they track how well the cochlea amplifies sounds. Yet, unlike all mammals studied to date, mole-rat otoacoustic emissions were similar across the range of sounds tested (∼70 dB, comparable to an alarm clock), meaning their cochleas didn't make quiet sounds louder.The researchers wondered why mole-rat inner ears didn't amplify sounds, focusing on the outer hair cells that convert soundwaves into brainwaves. As mutations in the hair cell protein prestin, which helps hair cells vibrate, cause hearing loss in humans, the team hypothesized that mole-rat prestin might be dysfunctional. But, when they checked, the mole-rats didn't have any problems with their prestin; they had the right amount in the right places and none of the usual mutations previously associated with hearing loss. Moreover, when they isolated hair cells from mole-rats, the sensors sent electrical signals just as well mouse hair cells, meaning that the lack of cochlear amplification in mole-rats wasn't caused by loss or dysfunction of prestin.Undeterred, the team turned their attention to stereocilia bundles, the ‘tufts’ attached to the hair cells that sway in response to sound. Scanning electron microscopy revealed that mole-rat stereocilia are a mess, jutting out at sharp angles and even missing in some places – a situation that probably makes they them less sensitive to sounds. The disorganization seemed to be caused by several mutations in the linker proteins that connect the tips of individual stereocilia like wires, causing all of the stereocilia to sway in unison, co-ordinating their auditory signals.Confident they had identified one mechanism for poor mole-rat hearing, the team tackled the ultimate question: why? Comparing mole-rat linker proteins with those of other rodents, they found far more amino acid sequence-altering mutations than expected in the mole-rat proteins; the probability of accumulating all those mutations randomly was infinitesimal, making it unlikely they had occurred by chance. The authors concluded that several of the linker protein mutations, and the poor hearing they caused, are likely advantageous for mole-rats.As you'd expect a noisy, sociable, subterranean rodent to have excellent hearing, hard of hearing mole-rats have long been a mystery. But now part of that mystery has been resolved and a key piece of the puzzle is a few mutations in proteins that connect a small, but mighty, part of their ears.