Parallel sites implicate functional convergence of the hearing gene prestin among echolocating mammals
- PMID: 24951728
- DOI: 10.1093/molbev/msu194
Parallel sites implicate functional convergence of the hearing gene prestin among echolocating mammals
Abstract
Echolocation is a sensory system whereby certain mammals navigate and forage using sound waves, usually in environments where visibility is limited. Curiously, echolocation has evolved independently in bats and whales, which occupy entirely different environments. Based on this phenotypic convergence, recent studies identified several echolocation-related genes with parallel sites at the protein sequence level among different echolocating mammals, and among these, prestin seems the most promising. Although previous studies analyzed the evolutionary mechanism of prestin, the functional roles of the parallel sites in the evolution of mammalian echolocation are not clear. By functional assays, we show that a key parameter of prestin function, 1/α, is increased in all echolocating mammals and that the N7T parallel substitution accounted for this functional convergence. Moreover, another parameter, V1/2, was shifted toward the depolarization direction in a toothed whale, the bottlenose dolphin (Tursiops truncatus) and a constant-frequency (CF) bat, the Stoliczka's trident bat (Aselliscus stoliczkanus). The parallel site of I384T between toothed whales and CF bats was responsible for this functional convergence. Furthermore, the two parameters (1/α and V1/2) were correlated with mammalian high-frequency hearing, suggesting that the convergent changes of the prestin function in echolocating mammals may play important roles in mammalian echolocation. To our knowledge, these findings present the functional patterns of echolocation-related genes in echolocating mammals for the first time and rigorously demonstrate adaptive parallel evolution at the protein sequence level, paving the way to insights into the molecular mechanism underlying mammalian echolocation.
Keywords: NLC; bat; convergent evolution; dolphin; echolocation.
© The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Similar articles
-
The hearing gene Prestin unites echolocating bats and whales.Curr Biol. 2010 Jan 26;20(2):R55-6. doi: 10.1016/j.cub.2009.11.042. Curr Biol. 2010. PMID: 20129037
-
Parallel signatures of sequence evolution among hearing genes in echolocating mammals: an emerging model of genetic convergence.Heredity (Edinb). 2012 May;108(5):480-9. doi: 10.1038/hdy.2011.119. Epub 2011 Dec 14. Heredity (Edinb). 2012. PMID: 22167055 Free PMC article.
-
Genomic and functional evidence reveals molecular insights into the origin of echolocation in whales.Sci Adv. 2018 Oct 3;4(10):eaat8821. doi: 10.1126/sciadv.aat8821. eCollection 2018 Oct. Sci Adv. 2018. PMID: 30306134 Free PMC article.
-
Functional convergence in bat and toothed whale biosonars.Physiology (Bethesda). 2013 Sep;28(5):276-83. doi: 10.1152/physiol.00008.2013. Physiology (Bethesda). 2013. PMID: 23997187 Review.
-
A false killer whale adjusts its hearing when it echolocates.J Exp Biol. 2008 Jun;211(Pt 11):1714-8. doi: 10.1242/jeb.013862. J Exp Biol. 2008. PMID: 18490386 Review.
Cited by
-
Molecular evolution of toothed whale genes reveals adaptations to echolocating in different environments.BMC Genomics. 2024 Nov 6;25(1):1049. doi: 10.1186/s12864-024-10910-1. BMC Genomics. 2024. PMID: 39506652
-
Recent advancement of sonogenetics: A promising noninvasive cellular manipulation by ultrasound.Genes Dis. 2023 Sep 15;11(5):101112. doi: 10.1016/j.gendis.2023.101112. eCollection 2024 Sep. Genes Dis. 2023. PMID: 38947740 Free PMC article. Review.
-
WGCCRR: a web-based tool for genome-wide screening of convergent indels and substitutions of amino acids.Bioinform Adv. 2024 May 24;4(1):vbae070. doi: 10.1093/bioadv/vbae070. eCollection 2024. Bioinform Adv. 2024. PMID: 38808070 Free PMC article.
-
PolyQ length-based molecular encoding of vocalization frequency in FOXP2.iScience. 2023 Sep 27;26(10):108036. doi: 10.1016/j.isci.2023.108036. eCollection 2023 Oct 20. iScience. 2023. PMID: 37860754 Free PMC article.
-
Convergence in hearing-related genes between echolocating birds and mammals.Proc Natl Acad Sci U S A. 2023 Oct 24;120(43):e2307340120. doi: 10.1073/pnas.2307340120. Epub 2023 Oct 16. Proc Natl Acad Sci U S A. 2023. PMID: 37844245 Free PMC article.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources