Molecular convergence and transgenic evidence suggest a single origin of laryngeal echolocation in bats

The evolutionary tuning of hearing

“…Signatures of positive selection have been identified in the coding region of α-tectorin in mammals [61] and mole rats [62], and β-tectorin in the star-nosed mole [58]. Convergent evolution in echolocating mammals has been described for otoancorin, a protein involved in the attachment of the tectorial membrane to the spiral limbus (Table 2) [51,63]. This identifies proteins involved in mechanical resonance as potential drivers of evolutionary change in mammalian hearing.…”

“…Moreover, positive selection in inner-ear-expressed genes has also been reported within mammalian branches [38][39][40][41][42][43][44]. In addition, instances of parallel and/or convergent evolution between echolocating bats and whales have been identified in hearing-related genes [38,40,[45][46][47][48][49][50][51], potentially reflecting distinct environmental demands. Thus, the coding sequences of inner ear genes can be proposed as hotspots for evolutionary innovation in mammals.…”

“…These include proteins localised at ankle links and stereocilia rootlets, along the stereocilia shaft, at the stereocilia tips and on the tip links (Figure 2). Additionally, convergent evolution has been reported for stereocilia proteins in echolocating mammals, leading to the hypothesis that these were likely driven by selection for the detection of high frequency sounds [38,40,[49][50][51]. It was initially thought that the subterranean lifestyle of mole rats, which shifted their auditory environment to lower frequency sounds (125 Hz to 8 kHz in naked mole rats) had led to relaxed evolutionary pressure on hair bundle proteins that had been fine-tuned to higher frequencies [44].…”

“…Three adaptive events have been proposed for early mammalian evolution in this context: gain of nonlinear capacitance and electromotility in stem mammals; improvement in electromotility in therians; and further enhancements related to prestin loss of solute transport in placental mammals [98]. The voltage dependence of prestin was further refined in echolocating mammals, seemingly driven by convergent amino acid changes and in relation to high frequency hearing [46,51,99].…”

“…Additionally, Slc12a2, which encodes the Na + /K + transporter NKCC1 involved in K + secretion to the endolymph [26] and in K + reuptake by supporting cells in chickens [27], has been under positive selection in naked mole rats [62]. Finally, Gjb2 and Gjb6, the genes coding for connexin 26 and connexin 30 that participate in K + recirculation [83], have been described under convergent evolution in echolocating mammals [50,51]. Overall, these lines of evidence identify a high endolymphatic potential and K + recirculation as crucial factors in the refinement of amniote hearing, with changes in both coding sequences and gene expression patterns potentially contributing to the extension of the hearing range in mammals.…”