The hearing gene Prestin reunites echolocating bats.
The remarkable high-frequency sensitivity and selectivity of the mammalian auditory system has been attributed to the evolution of mechanical amplification, in which sound waves are amplified by outer hair cells in the cochlea. This process is driven by the recently discovered protein prestin, encoded by the gene Prestin. Echolocating bats use ultrasound for orientation and hunting and possess the highest frequency hearing of all mammals. To test for the involvement of Prestin in the evolution of bat echolocation, we sequenced the coding region in echolocating and nonecholocating species. The resulting putative gene tree showed strong support for a monophyletic assemblage of echolocating species, conflicting with the species phylogeny in which echolocators are paraphyletic. We reject the possibilities that this conflict arises from either gene duplication and loss or relaxed selection in nonecholocating fruit bats. Instead, we hypothesize that the putative gene tree reflects convergence at stretches of functional importance. Convergence is supported by the recovery of the species tree from alignments of hydrophobic transmembrane domains, and the putative gene tree from the intra- and extracellular domains. We also found evidence that Prestin has undergone Darwinian selection associated with the evolution of specialized constant-frequency echolocation, which is characterized by sharp auditory tuning. Our study of a hearing gene in bats strongly implicates Prestin in the evolution of echolocation, and suggests independent evolution of high-frequency hearing in bats. These results highlight the potential problems of extracting phylogenetic signals from functional genes that may be prone to convergence.
Li
Gang
G
School of Life Science, East China Normal University, Shanghai 200062, China.
Wang
Jinhong
J
Rossiter
Stephen J
SJ
Jones
Gareth
G
Cotton
James A
JA
Zhang
Shuyi
S
D000818:Animals; D027321:Anion Transport Proteins / Q000235:genetics / Q000378:metabolism*; D002685:Chiroptera / Q000235:genetics* / Q000502:physiology*; D004455:Echolocation / Q000502:physiology*; D006309:Hearing / Q000235:genetics / Q000502:physiology*; D006801:Humans; D008969:Molecular Sequence Data; D010802:Phylogeny
D027321:Anion Transport Proteins
Science. 1985 Jan 11;227(4683):194-6
3966153
J Exp Biol. 1999 Dec;202(Pt 23):3359-67
10562518
Nature. 2002 Sep 19;419(6904):300-4
12239568
Bioinformatics. 1998;14(1):68-73
9520503
Biophys J. 2005 Nov;89(5):3345-52
16113116
Nucleic Acids Res. 1997 Dec 15;25(24):4876-82
9396791
Bioinformatics. 1998;14(9):819-20
9918954
Curr Biol. 1999 Jul 29-Aug 12;9(15):R572-4
10469559
Proc Biol Sci. 2003 Nov 7;270(1530):2293-9
14613617
Science. 2005 Jan 28;307(5709):580-4
15681385
J Comp Neurol. 1992 Apr 22;318(4):367-79
1578008
Trends Ecol Evol. 2006 Mar;21(3):149-56
16701491
Nature. 1997 Sep 4;389(6646):63-6
9288966
Sci China C Life Sci. 2007 Aug;50(4):492-6
17653670
Nature. 1991 Mar 14;350(6314):155-7
2005965
Nature. 2005 Feb 24;433(7028):880-3
15696193
J Comp Physiol A. 1994 Oct;175(4):449-55
7965917
Proc Natl Acad Sci U S A. 2001 May 22;98(11):6241-6
11353869
J Acoust Soc Am. 2004 May;115(5 Pt 1):2178-84
15139629
J Physiol. 2004 Nov 1;560(Pt 3):821-30
15319415
Mol Biol Evol. 2006 Feb;23(2):254-67
16221896
Nature. 2000 Jan 13;403(6766):188-92
10646602
Hum Mol Genet. 2003 May 15;12(10):1155-62
12719379
Mol Biol Evol. 2007 Aug;24(8):1586-91
17483113
Brief Bioinform. 2004 Jun;5(2):150-63
15260895
Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1431-6
11805285
Nat Rev Mol Cell Biol. 2002 Feb;3(2):104-11
11836512
Neurosci Lett. 2006 Sep 1;404(3):270-5
16839688
Syst Biol. 2002 Jun;51(3):492-508
12079646
J Biol Chem. 2006 Aug 11;281(32):22964-73
16754669
Mol Biol Evol. 2005 Sep;22(9):1869-86
15930153
Mol Biol Evol. 2004 Feb;21(2):397-403
14660685
J Cell Sci. 2005 Jul 1;118(Pt 13):2987-96
15976456
J Comp Neurol. 1992 Apr 22;318(4):380-91
1578009
J Neurosci. 2000 Dec 15;20(24):RC116
11125015
Philos Trans R Soc Lond B Biol Sci. 1998 Apr 29;353(1368):607-17
9602535
Brain Res Mol Brain Res. 2004 Jul 5;126(1):30-7
15207913
Appl Bioinformatics. 2002;1(3):159-61
15130843
BMC Med Genet. 2005 Aug 08;6:30
16086836
Nature. 2000 May 11;405(6783):149-55
10821263
Mol Biol Evol. 1998 May;15(5):568-73
9580986
Curr Opin Neurobiol. 2003 Aug;13(4):459-68
12965294
Mol Phylogenet Evol. 2006 Dec;41(3):622-35
16854604
Mol Biol Evol. 2005 Dec;22(12):2472-9
16107592
Curr Opin Neurobiol. 2007 Aug;17(4):498-503
17707636
J Physiol. 1987 Jul;388:323-47
3656195
Science. 2001 Dec 14;294(5550):2348-51
11743200
Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4420-5
10200277
PLoS One. 2007 Sep 19;2(9):e900
17878935
J Neurosci. 1989 Aug;9(8):2954-62
2769373
Genome Res. 2005 Jul;15(7):978-86
15965030
J Neurosci. 2006 Mar 8;26(10):2757-66
16525055
Hear Res. 2000 Nov;149(1-2):1-10
11033242