Convergent sequence evolution between echolocating bats and dolphins

Abstract

Cases of convergent evolution - where different lineages have evolved similar traits independently - are common and have proven central to our understanding of selection. Yet convincing examples of adaptive convergence at the sequence level are exceptionally rare [1]. The motor protein Prestin is expressed in mammalian outer hair cells (OHCs) and is thought to confer high frequency sensitivity and selectivity in the mammalian auditory system [2]. We previously reported that the Prestin gene has undergone sequence convergence among unrelated lineages of echolocating bat [3]. Here we report that this gene has also undergone convergent amino acid substitutions in echolocating dolphins, which group with echolocating bats in a phylogenetic tree of Prestin. Furthermore, we find evidence that these changes were driven by natural selection.

Parallel signatures of sequence evolution among hearing genes in echolocating mammals: an emerging model of genetic convergence

“…Examination of the relative site-wise support for the convergent topology (data not shown), as well as the Lento plots, indicated that most support for the 'convergent topologies' was concentrated within exonic regions, whereas phylogenetic signal for the true species relationships was more obvious in intronic sections. Together with other very recent research (Li et al, 2008;Rokas and Carroll, 2008;Castoe et al, 2009;Li et al, 2010;Liu et al, 2010a), the data suggest that sequence convergence might be much more common than previously thought.…”

“…Prestin encodes a motor protein of the outer hair cell and is thought to drive the cochlear amplifier that gives mammalian hearing its characteristically high sensitivity and selectivity (Zheng et al, 2000). Phylogenies based on Prestin lead to erroneous groupings of unrelated echolocating bats (Li et al, 2008) and also horseshoe bats and echolocating cetaceans (Li et al, 2010;Liu et al, 2010a b). These results as well as observed associations between numbers of replacements and auditory sensitivity (Liu et al, 2010b;Rossiter et al, 2011) all suggest a strong link between Prestin and high-frequency hearing.…”

“…The 'hearing gene' Prestin was recently shown to have undergone unprecedented levels of sequence convergence between lineages of echolocating mammals (Li et al, 2008(Li et al, , 2010Liu et al, 2010a). Prestin encodes a motor protein of the outer hair cell and is thought to drive the cochlear amplifier that gives mammalian hearing its characteristically high sensitivity and selectivity (Zheng et al, 2000).…”

Evolutionary Paths to Mammalian Cochleae

“…Remarkably, highly evolved and specialized prestins that are found in modern ultrasound-echolocation species such as bats and toothed whales show many of the same sequence changes over evolutionary time, but evolved independently and during different geological time periods (Li et al 2010;Liu et al 2010). The evolution of acetylcholine receptor systems that control the outer hair-cell efferent feedback correlates with the evolution of prestins in therians (Elgoyhen and Franchini 2011) and suggests a parallel evolution of control systems, on the one hand, and a motor system, on the other hand, in the mammalian inner ear.…”

What is comparable in comparative cognition?

“…On occasion, these are clearly identifiable as instances of convergence when abilities have emerged in highly distinct lineages, such as echolocation in bats and dolphins [20,21] or flexible tool use in primates and corvids [22]. Yet, distinguishing homology from convergence is sometimes difficult without knowledge of the underlying mechanisms.…”