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

Abstract

Recent findings of sequence convergence in the Prestin gene among some bats and cetaceans suggest that parallel adaptations for high-frequency hearing have taken place during the evolution of echolocation. To determine if this gene is an exception, or instead similar processes have occurred in other hearing genes, we have examined Tmc1 and Pjvk, both of which are associated with non-syndromic hearing loss in mammals. These genes were amplified and sequenced from a number of mammalian species, including echolocating and non-echolocating bats and whales, and were analysed together with published sequences. Sections of both genes showed phylogenetic signals that conflicted with accepted species relationships, with coding regions uniting laryngeal echolocating bats in a monophyletic clade. Bayesian estimates of posterior probabilities of convergent and divergent substitutions provided more direct evidence of sequence convergence between the two groups of laryngeal echolocating bats as well as between echolocating bats and dolphins. We found strong evidence of positive selection acting on some echolocating bat species and echolocating cetaceans, contrasting with purifying selection on non-echolocating bats. Signatures of sequence convergence and molecular adaptation in two additional hearing genes suggest that the acquisition of high-frequency hearing has involved multiple loci.

Hearing echoes

“…At the gene Prestin, where this phenomenon of extreme parallel evolution was originally reported, even echolocating whales join the gaggle before the fruit bats get a look in (Figure 1, middle panel). The two additional genes, described by Davies et al (2012), recapitulate the results at Prestin: the pattern is more widespread (two additional genes and more species) but less sharp (fewer recurring mutations, less discrepancy between the gene and the species tree, Figure 1, right panel). Davies et al (2012) raise an interesting question: how often do we hear evolutionary echoes like this?…”

“…The two additional genes, described by Davies et al (2012), recapitulate the results at Prestin: the pattern is more widespread (two additional genes and more species) but less sharp (fewer recurring mutations, less discrepancy between the gene and the species tree, Figure 1, right panel). Davies et al (2012) raise an interesting question: how often do we hear evolutionary echoes like this? Indeed, the picture may be emerging that convergent phenotypes may often correspond to parallel mechanisms down to the finest molecular level, as unlikely as that proposition may appear at first glance.…”

“…Natural examples, like those detected by Davies et al (2012), have also started to accumulate, showing that parallelism is not just a laboratory curiosity. Parallel mutations in multiple species at the same genes conferring insecticide resistance are not only common but have also arisen rapidly (ffrench-Constant et al, 2004).…”

“…A readjustment may well be in order, thanks to recent studies by Li et al (2010) and Davies et al (2012) in this current issue. In contrast to traditional views that convergent evolution reflects only functional but not mechanistic convergence in achieving analogous adaptations, molecular evolutionary biologists use the term 'parallel evolution' to convey the mechanistic parallelism between independent cases.…”

“…What's more, this phenomenon does not occur just once, but was found in as many as four (perhaps more?) genes implicated in haircell formation, the same cells that are missing among whom hearing is high-frequency-challenged (Li et al, 2010;Liu et al, 2011;Davies et al, 2012).…”