Parallel evolution of auditory genes for echolocation in bats and toothed whales

PLoS Genetics

Volumn 8, Issue 6, 2012, Pages

  Shen, Yong Yi ^a   Liang, Lu ^a,b   Li, Gui Sheng ^a   Murphy, Robert W ^a,c   Zhang, Ya Ping ^a,d  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c DEPARTMENT OF NATURAL HISTORY   (Canada)

^d YUNNAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN 23; CADHERIN; MEMBRANE PROTEIN;

ARTICLE; AUDITORY CORTEX; BAT; CADHERIN 23 GENE; CONTROLLED STUDY; CONVERGENT EVOLUTION; DNA SEQUENCE; DOLPHIN; ECHOLOCATION; GENE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENETIC SCREENING; HAIR CELL; INNER EAR; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OTOFERLIN GENE; PROTOCADHERIN 15 GENE; REAL TIME POLYMERASE CHAIN REACTION; RHINOLOPHOIDEA; SEQUENCE ANALYSIS; SIGNAL DETECTION; SIGNAL TRANSDUCTION; WHALE; YANGOCHIROPTERA; ANIMAL; COCHLEAR NERVE; GENE EXPRESSION; GENETIC SELECTION; GENETICS; HEARING; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYLOGENY; PHYSIOLOGY; PSYCHOLOGICAL ASPECT;

ODONTOCETI;

ANIMALS; AUDITORY CORTEX; AUDITORY PERCEPTION; CADHERINS; CHIROPTERA; COCHLEAR NERVE; DOLPHINS; ECHOLOCATION; EVOLUTION, MOLECULAR; GENE EXPRESSION; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; SELECTION, GENETIC;

EID: 84864063616     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002788     Document Type: Article

References (65)

1. Li Y, Liu Z, Shi P, Zhang J, (2010) The hearing gene Prestin unites echolocating bats and whales. Curr Biol 20: R55-R56.
2. Liu Y, Cotton JA, Shen B, Han X, Rossiter SJ, et al. (2010) Convergent sequence evolution between echolocating bats and dolphins. Curr Biol 20: R53-R54.
3. Liu Z, Li S, Wang W, Xu D, Murphy RW, et al. (2011) Parallel evolution of KCNQ4 in echolocating bats. PLoS ONE 6: e26618 doi:10.1371/journal.pone.0026618.
4. Speakman JR, (1993) The evolution of echolocation for predation. Symp zool Soc Lond 65: 39-63.
5. Arch VS, Narins PM, (2008) 'Silent' signals: selective forces acting on ultrasonic communication systems in terrestrial vertebrates. Anim Behav 76: 1423-1428.
6. Fettiplace R, (2006) Active hair bundle movements in auditory hair cells. J Physiol 576: 29-36.
7. Ashmore J, Avan P, Brownell WE, Dallos P, Dierkes K, et al. (2010) The remarkable cochlear amplifier. Hear Res 266: 1-17.
8. Zheng J, Shen W, He DZZ, Long KB, Madison LD, et al. (2000) Prestin is the motor protein of cochlear outer hair cells. Nature 405: 149-155.
9. Li G, Wang J, Rossiter SJ, Jones G, Cotton JA, et al. (2008) The hearing gene Prestin reunites echolocating bats. Proc Natl Acad Sci U S A 105: 13959-13964.
10. Liu Y, Han N, Franchini LF, Xu H, Pisciottano F, et al. (2012) The voltage-gated potassium channel subfamily KQT member 4 (KCNQ4) displays parallel evolution in echolocating bats. Mol Biol Evol 29: 1441-1450.
11. Dallos P, (2008) Cochlear amplification, outer hair cells and prestin. Curr Opin Neurobiol 18: 370-376.
12. Di Palma F, Pellegrino R, Noben-Trauth K, (2001) Genomic structure, alternative splice forms and normal and mutant alleles of cadherin 23 (Cdh23). Gene 281: 31-41.
13. Bolz H, Von Brederlow B, Ramírez A, Bryda EC, Kutsche K, et al. (2001) Mutation of CDH23, encoding a new member of the cadherin gene family, causes Usher syndrome type 1D. Nat Genet 27: 108-112.
14. Alagramam KN, Murcia CL, Kwon HY, Pawlowski KS, Wright CG, et al. (2001) The mouse Ames waltzer hearing-loss mutant is caused by mutation of Pcdh15, a novel protocadherin gene. Nat Genet 27: 99-102.
15. Ahmed ZM, Riazuddin S, Wilcox ER, (2003) The molecular genetics of Usher syndrome. Clin Genet 63: 431-444.
16. Kazmierczak P, Sakaguchi H, Tokita J, Wilson-Kubalek EM, Milligan RA, et al. (2007) Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells. Nature 449: 87-91.
17. Siemens J, Lillo C, Dumont RA, Reynolds A, Williams DS, et al. (2004) Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 428: 950-955.
18. Zak M, Pfister M, Blin N, (2011) The otoferlin interactome in neurosensory hair cells: significance for synaptic vesicle release and trans-Golgi network (Review). Int J Mol Med 28: 311-314.
19. Yasunaga S, Grati M, Cohen-Salmon M, El-Amraoui A, Mustapha M, et al. (1999) A mutation in OTOF, encoding otoferlin, a FER-1-like protein, causes DFNB9, a nonsyndromic form of deafness. Nat Genet 21: 363-369.
20. Houseman MJ, Jackson AP, Al-Gazali LI, Badin RA, Roberts E, et al. (2001) A novel mutation in a family with non-syndromic sensorineural hearing loss that disrupts the newly characterised OTOF long isoforms. J Med Genet 38: E25.
21. Varga R, Kelley PM, Keats BJ, Starr A, Leal SM, et al. (2003) Non-syndromic recessive auditory neuropathy is the result of mutations in the otoferlin (OTOF) gene. J Med Genet 40: 45-50.
22. Roux I, Safieddine S, Nouvian R, Grati M, Simmler M, et al. (2006) Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127: 277-289.
23. Schug N, Braig C, Zimmermann U, Engel J, Winter H, et al. (2006) Differential expression of otoferlin in brain, vestibular system, immature and mature cochlea of the rat. Eur J Neurosci 24: 3372-3380.
24. Fay RR, Popper AN, (2000) Evolution of hearing in vertebrates: the inner ears and processing. Hear Res 149: 1-10.
25. Seidman MD, Ahmad N, Bai U, (2002) Molecular mechanisms of age-related hearing loss. Ageing Res Rev 1: 331-343.
26. Teeling EC, Springer MS, Madsen O, Bates P, O'Brien SJ, et al. (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307: 580-584.
27. Murphy WJ, Eizirik E, O'Brien SJ, Madsen O, Scally M, et al. (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294: 2348-2351.
28. Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, et al. (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409: 614-618.
29. Adams RA, Pedersen SC, (2000) Ontogeny, Functional Ecology, and Evolution of Bats New York Cambridge University Press.
30. Perrin WF, Würsig B, Thewissen JGM, (2008) Encyclopedia of Marine Mammals San Diego, CA Academic Press.
31. Ahmed ZM, Goodyear R, Riazuddin S, Lagziel A, Legan PK, et al. (2006) The tip-link antigen, a protein associated with the transduction complex of sensory hair cells, is protocadherin-15. J Neurosci 26: 7022-7034.
32. Di Palma F, Holme RH, Bryda EC, Belyantseva IA, Pellegrino R, et al. (2001) Mutations in Cdh23, encoding a new type of cadherin, cause stereocilia disorganization in waltzer, the mouse model for Usher syndrome type 1D. Nat Genet 27: 103-107.
33. Zakon HH, (2002) Convergent evolution on the molecular level. Brain Behav Evol 59: 250-261.
34. Castoe TA, de Koning AP, Kim HM, Gu W, Noonan BP, et al. (2009) Evidence for an ancient adaptive episode of convergent molecular evolution. Proc Natl Acad Sci U S A 106: 8986-8991.
35. Zhang J, (2006) Parallel adaptive origins of digestive RNases in Asian and African leaf monkeys. Nat Genet 38: 819-823.
36. Yokoyama S, Radlwimmer FB, (1998) The 'five-sites' rule and the evolution of red and green color vision in mammals. Mol Biol Evol 15: 560-567.
37. Dallos P, Wu X, Cheatham MA, Gao J, Zheng J, et al. (2008) Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. Neuron 58: 333-339.
38. Mellado Lagarde MM, Drexl M, Lukashkina VA, Lukashkin AN, Russell IJ, (2008) Outer hair cell somatic, not hair bundle, motility is the basis of the cochlear amplifier. Nat Neurosci 11: 746-748.
39. Kennedy HJ, Crawford AC, Fettiplace R, (2005) Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature 433: 880-883.
40. Chan DK, Hudspeth AJ, (2005) Ca2+ current-driven nonlinear amplification by the mammalian cochlea in vitro. Nat Neurosci 8: 149-155.
41. Rauschecker JP, Shannon RV, (2002) Sending sound to the brain. Science 295: 1025-1029.
42. Liberman MC, Gao J, He DZ, Wu X, Jia S, et al. (2002) Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419: 300-304.
43. Albert JT, Winter H, Schaechinger TJ, Weber T, Wang X, et al. (2007) Voltage-sensitive Prestin orthologue expressed in zebrafish hair cells. J Physiol 580: 451-461.
44. Cheatham MA, Huynh KH, Gao J, Zuo J, Dallos P, (2004) Cochlear function in Prestin knockout mice. J Physiol 560: 821-830.
45. Assad JA, Corey DP, (1992) An active motor model for adaptation by vertebrate hair cells. J Neurosci 12: 3291-3309.
46. Howard J, Hudspeth AJ, (1988) Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell. Neuron 1: 189-199.
47. Sotomayor M, Weihofen WA, Gaudet R, Corey DP, (2010) Structural determinants of cadherin-23 function in hearing and deafness. Neuron 66: 85-100.
48. Zheng QY, Yan D, Ouyang XM, Du LL, Yu H, et al. (2005) Digenic inheritance of deafness caused by mutations in genes encoding cadherin 23 and protocadherin 15 in mice and humans. Hum Mol Genet 14: 103-111.
49. Perrin WF, Würsig B, Thewissen JGM, (2008) Encyclopedia of Marine Mammals San Diego, CA Academic Press pp. 1126-1127.
50. Shanahan CM, Cary NR, Metcalfe JC, Weissberg PL, (1994) High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J Clin Invest 93: 2393-2402.
51. Uguccioni M, Mackay CR, Ochensberger B, Loetscher P, Rhis S, et al. (1997) High expression of the chemokine receptor CCR3 in human blood basophils. Role in activation by eotaxin, MCP-4, and other chemokines. J Clin Invest 100: 1137-1143.
52. Chermak GD, Musiek FE, (1997) Central Auditory Processing Disorders: New Perspectives San Diego Singular Publishing Group Press.
53. Sambrook J, Russell DW, (2001) Molecular Cloning: A Laboratory Manual New York Cold Spring Harbor Laboratory Press.
54. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
55. Posada D, (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
56. Posada D, (2009) Selection of models of DNA evolution with jModelTest. Methods Mol Biol 537: 93-112.
57. Darriba D, Taboada GL, Doallo R, Posada D, (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27: 1164-1165.
58. Swofford DL, (2003) PAUP*: phylogenetic analysis using parsimony (* and other methods). Version 4.0 Sunderland, Massachusetts Sinauer Associates.
59. Huelsenbeck JP, Ronquist F, (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
60. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
61. Li WH, Wu CI, Luo CC, (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2: 150-174.
62. Zhang J, Nei M, (1997) Accuracies of ancestral amino acid sequences inferred by the parsimony, likelihood, and distance methods. J Mol Evol 44: S139-146.
63. Zhang J, Kumar S, (1997) Detection of convergent and parallel evolution at the amino acid sequence level. Mol Biol Evol 14: 527-536.
64. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
65. Talairach J, Tournoux P, (1988) Co-Planar Stereotaxic Atlas of the Human Brain New York Thieme Press.