Comparative genomics reveals molecular features unique to the songbird lineage

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Wirthlin, Morgan ^a   Lovell, Peter V ^a   Jarvis, Erich D ^b   Mello, Claudio V ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Evolution; Novel gene family expansion; Songbird; Vocal learning; Zebra finch

Indexed keywords

RNA;

ADULT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CHROMOSOME REARRANGEMENT; COMPARATIVE GENOMICS; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ANALYSIS; GENOME; GENOMIC INSTABILITY; GENOMICS; IN SITU HYBRIDIZATION; MALE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DOMAIN; RNA SEQUENCE; SYNTENY; TAENIOPYGIA GUTTATA; TISSUE DISTRIBUTION; ANIMAL; BRAIN; COMPARATIVE STUDY; GENE EXPRESSION PROFILING; GENETICS; LEARNING; MOLECULAR GENETICS; PHYSIOLOGY; SONGBIRD; SPECIES DIFFERENCE; VOCALIZATION;

AVES; PASSERI; PASSERIFORMES; TAENIOPYGIA GUTTATA; VERTEBRATA;

ANIMALS; BRAIN; GENE EXPRESSION PROFILING; GENOMICS; LEARNING; MALE; MOLECULAR SEQUENCE ANNOTATION; SONGBIRDS; SPECIES SPECIFICITY; VOCALIZATION, ANIMAL;

EID: 84923094555     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1082     Document Type: Article

References (84)

1. Monroe BL, Sibley CG: A World Checklist of Birds. New Haven: Yale University Press; 1993.
2. Lasiewski RC, Dawson WR: A re-examination of the relation between standard metabolic rate and body weight in birds. Condor 1967, 69:13-23. 10.2307/1366368.
3. Smith JA: Chapter 31 - Passeriformes (Songbirds, Perching Birds). In Fowler's Zoo and Wild Animal Medicine, Volume 8. Edited by: Fowler ME, Miller RE. St. Louis: W.B. Saunders; 2015:236-246.
4. Marler P, Tamura M: Culturally transmitted patterns of vocal behavior in sparrows. Science 1964, 146:1483-1486. 10.1126/science.146.3650.1483.
5. Nottebohm F: The origins of vocal learning. Am Nat 1972, 106:116-140. 10.1086/282756.
6. Jarvis ED: Learned birdsong and the neurobiology of human language. Ann N Y Acad Sci 2004, 1016:749-777. 10.1196/annals.1298.038.
7. Doupe AJ, Kuhl PK: Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci 1999, 22:567-631. 10.1146/annurev.neuro.22.1.567.
8. Knörnschild M, Nagy M, Metz M, Mayer F, von Helversen O: Complex vocal imitation during ontogeny in a bat. Biol Lett 2010, 6:156-159. 10.1098/rsbl.2009.0685.
9. Boughman JW: Vocal learning by greater spear-nosed bats. Proc R Soc Lond [Biol] 1998, 265:227-233. 10.1098/rspb.1998.0286.
10. Janik VM, Slater PJB: Vocal learning in mammals. Adv Stud Behav 1997, 26:59-100.
11. Lilly JC: Vocal mimicry in Tursiops: ability to match numbers and durations of human vocal bursts. Science 1965, 147:300-301. 10.1126/science.147.3655.300.
12. Poole JH, Tyack PL, Stoeger-Horwath AS, Watwood S: Animal behaviour: elephants are capable of vocal learning. Nature 2005, 434:455-456. 10.1038/434455a.
13. Sanvito S, Galimberti F, Miller EH: Observational evidences of vocal learning in southern elephant seals: a longitudinal study. Ethology 2007, 113:137-146. 10.1111/j.1439-0310.2006.01306.x.
14. Reichmuth C, Casey C: Vocal learning in seals, sea lions, and walruses. Curr Opin Neurobiol 2014, 28:66-71.
15. Baptista LF, Schuchmann K-L: Song learning in the Anna hummingbird ( Calypte anna ). Ethology 1990, 84:15-26.
16. Nottebohm F, Paton JA, Kelley DB: Connections of vocal control nuclei in the canary telencephalon. J Comp Neurol 1982, 207:344-357. 10.1002/cne.902070406.
17. Bottjer SW, Halsema KA, Brown SA, Miesner EA: Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. J Comp Neurol 1989, 279:312-326. 10.1002/cne.902790211.
18. Paton J, Manogue K, Nottebohm F: Bilateral organization of the vocal control pathway in the budgerigar, Melopsittacus undulatus. J Neurosci 1981, 1:1279-1288.
19. Gahr M: Neural song control system of hummingbirds: comparison to swifts, vocal learning (Songbirds) and nonlearning (Suboscines) passerines, and vocal learning (Budgerigars) and nonlearning (Dove, owl, gull, quail, chicken) nonpasserines. J Comp Neurol 2000, 426:182-196. 10.1002/1096-9861(20001016)426:2<182::AID-CNE2>3.0.CO;2-M.
20. Durand SE, Heaton JT, Amateau SK, Brauth SE: Vocal control pathways through the anterior forebrain of a parrot ( Melopsittacus undulatus ). J Comp Neurol 1997, 377:179-206. 10.1002/(SICI)1096-9861(19970113)377:2<179::AID-CNE3>3.0.CO;2-0.
21. Jarvis ED, Ribeiro S, da Silva ML, Ventura D, Vielliard J, Mello CV: Behaviourally driven gene expression reveals song nuclei in hummingbird brain. Nature 2000, 406:628-632. 10.1038/35020570.
22. Brauth SE, Heaton JT, Durand SE, Liang W, Hall WS: Functional anatomy of forebrain auditory pathways in the budgerigar (Melopsittacus undulatus). Brain Behav Evol 1994, 44:210-233. 10.1159/000113578.
23. Vates GE, Broome BM, Mello CV, Nottebohm F: Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches ( Taenopygia guttata ). J Comp Neurol 1996, 366:613-642. 10.1002/(SICI)1096-9861(19960318)366:4<613::AID-CNE5>3.0.CO;2-7.
24. Jarvis ED, Mello CV: Molecular mapping of brain areas involved in parrot vocal communication. J Comp Neurol 2000, 419:1-31. 10.1002/(SICI)1096-9861(20000327)419:1<1::AID-CNE1>3.0.CO;2-M.
25. Brenowitz EA, Margoliash D, Nordeen KW: An introduction to birdsong and the avian song system. J Neurobiol 1997, 33:495-500. 10.1002/(SICI)1097-4695(19971105)33:5<495::AID-NEU1>3.0.CO;2-#.
26. Zeigler HP, Marler P: Neuroscience of Birdsong. Cambridge: Cambridge University Press; 2008.
27. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, Kunstner A, Searle S, White S, Vilella AJ, Fairley S, Heger A, Kong L, Ponting CP, Jarvis ED, Mello CV, Minx P, Lovell P, Velho TAF, Ferris M, Balakrishnan CN, Sinha S, Blatti C, London SE, Li Y, Lin Y-C, George J, Sweedler J, Southey B, Gunaratne P, Watson M, et al.: The genome of a songbird. Nature 2010, 464:757-762. 10.1038/nature08819.
28. Lespinet O, Wolf YI, Koonin EV, Aravind L: The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 2002, 12:1048-1059. 10.1101/gr.174302.
29. Dennis Megan Y, Nuttle X, Sudmant Peter H, Antonacci F, Graves Tina A, Nefedov M, Rosenfeld Jill A, Sajjadian S, Malig M, Kotkiewicz H, Curry Cynthia J, Shafer S, Shaffer Lisa G, de Jong Pieter J, Wilson Richard K, Eichler Evan E: Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell 2012, 149:912-922. 10.1016/j.cell.2012.03.033.
30. Hillier LW, Miller W, Ewan B, Warren W, Hardison RC, Ponting CP, Bork P, Burt DW, Groenen MAM, Delany ME, Dodgson JB, Chinwalla AT, Cliften PF, Clifton SW, Delehaunty KD, Fronick C, Fulton RS, Graves TA, Kremitzki C, Layman D, Magrini V, McPherson JD, Miner TL, Minx P, Nash WE, Nelson MNNJO, Oddy LG, Pohl CS, Randall-Maher J, Smith SM, et al.: Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 2004, 432:695-716. 10.1038/nature03154.
31. Kong L, Lovell PV, Heger A, Mello CV, Ponting CP: Accelerated evolution of PAK3- and PIM1-like kinase gene families in the zebra finch, Taeniopygia guttata. Mol Biol Evol 2010, 27:1923-1934. 10.1093/molbev/msq080.
32. Lomsadze A, Burns PD, Borodovsky M: Integration of mapped RNA-Seq reads into automatic training of eukaryotic gene finding algorithm. Nucleic Acids Res 2014, 42:e119. 10.1093/nar/gku557.
33. Lovell PV, Carleton JB, Mello CV: Genomics analysis of potassium channel genes in songbirds reveals molecular specializations of brain circuits for the maintenance and production of learned vocalizations. BMC Genomics 2013, 14:470. 10.1186/1471-2164-14-470.
34. Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, Ho SYW, Faircloth BC, Nabholz B, Howard JT, Suh A, Weber CC, Fonseca RR, Li J, Zhang F, Li H, Zhou L, Narula N, Liu L, Ganapathy G, Boussau B, Bayzid MS, Zavidovych V, Subramanian S, Gabaldón T, Capella-Gutiérrez S, Huerta-Cepas J, Rekepalli B, Munch K, Schierup M, et al.: Whole-genome analyses resolve the early branches in the tree of life of modern birds. Science 2014, 346:1320-1331. 10.1126/science.1253451.
35. Zhang G, Li C, Li Q, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW, Ödeen A, Cui J, Zhou Q, Xu L, Pan H, Wang Z, Jin L, Zhang P, Hu H, Yang W, Hu J, Xiao J, Yang Z, Liu Y, Xie Q, Yu H, Lian J, Wen P, Zhang F, Li H, et al.: Comparative genomics reveals insights into avian genome evolution and adaptation. Science 2014, 346:1311-1320. 10.1126/science.1251385.
36. Völker M, Backström N, Skinner BM, Langley EJ, Bunzey SK, Ellegren H, Griffin DK: Copy number variation, chromosome rearrangement, and their association with recombination during avian evolution. Genome Res 2010, 20:503-511. 10.1101/gr.103663.109.
37. Peterson M, Whittaker D, Ambreth S, Sureshchandra S, Buechlein A, Podicheti R, Choi J-H, Lai Z, Mockatis K, Colbourne J, Tang H, Ketterson E: De novo transcriptome sequencing in a songbird, the dark-eyed junco (Junco hyemalis): genomic tools for an ecological model system. BMC Genomics 2012, 13:305. 10.1186/1471-2164-13-305.
38. Bottjer S, Miesner E, Arnold A: Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 1984, 224:901-903. 10.1126/science.6719123.
39. Brainard MS, Doupe AJ: Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 2000, 404:762-766. 10.1038/35008083.
40. Bottjer SW, Brady JD, Cribbs B: Connections of a motor cortical region in zebra finches: Relation to pathways for vocal learning. J Comp Neurol 2000, 420:244-260. 10.1002/(SICI)1096-9861(20000501)420:2<244::AID-CNE7>3.0.CO;2-M.
41. Jarvis ED, Yu J, Rivas MV, Horita H, Feenders G, Whitney O, Jarvis SC, Jarvis ER, Kubikova L, Puck AEP, Siang-Bakshi C, Martin S, McElroy M, Hara E, Howard J, Pfenning A, Mouritsen H, Chen C-C, Wada K: Global view of the functional molecular organization of the avian cerebrum: Mirror images and functional columns. J Comp Neurol 2013, 521:3614-3665. 10.1002/cne.23404.
42. Chen C-C, Winkler CM, Pfenning AR, Jarvis ED: Molecular profiling of the developing avian telencephalon: Regional timing and brain subdivision continuities. J Comp Neurol 2013, 521:3666-3701. 10.1002/cne.23406.
43. Simpson H, Vicario D: Brain pathways for learned and unlearned vocalizations differ in zebra finches. J Neurosci 1990, 10:1541-1556.
44. Dutar P, Vu HM, Perkel DJ: Multiple cell types distinguished by physiological, pharmacological, and anatomic properties in nucleus HVc of the adult zebra finch. J Neurophysiol 1998, 80:1828-1838.
45. Spiro JE, Dalva MB, Mooney R: Long-range inhibition within the zebra finch song nucleus RA can coordinate the firing of multiple projection neurons. J Neurophysiol 1999, 81:3007-3020.
46. Hubbard T, Barker D, Birney E, Cameron G, Chen Y, Clark L, Cox T, Cuff J, Curwen V, Down T, Durbin R, Eyras E, Gilbert J, Hammond M, Huminiecki L, Kasprzyk A, Lehvaslaiho H, Lijnzaad P, Melsopp C, Mongin E, Pettett R, Pocock M, Potter S, Rust A, Schmidt E, Searle S, Slater G, Smith J, Spooner W, Stabenau A, et al.: The Ensembl genome database project. Nucleic Acids Res 2002, 30:38-41. 10.1093/nar/30.1.38.
47. Curwen V, Eyras E, Andrews TD, Clarke L, Mongin E, Searle SMJ, Clamp M: The Ensembl automatic gene annotation system. Genome Res 2004, 14:942-950. 10.1101/gr.1858004.
48. Lynch M, Conery JS: The evolutionary fate and consequences of duplicate genes. Science 2000, 290:1151-1155. 10.1126/science.290.5494.1151.
49. Lynch M: Gene duplication and evolution. Science 2002, 297:945-947. 10.1126/science.1075472.
50. Skinner BM, Griffin DK: Intrachromosomal rearrangements in avian genome evolution: evidence for regions prone to breakpoints. Heredity 2012, 108:37-41. 10.1038/hdy.2011.99.
51. Lupski JR, Stankiewicz P: Genomic disorders: molecular mechanisms for rearrangements and conveyed phenotypes. PLoS Genet 2005, 1:e49. 10.1371/journal.pgen.0010049.
52. Itoh Y, Arnold A: Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosome Res 2005, 13:47-56. 10.1007/s10577-005-6602-x.
53. Yuri T, Kimball RT, Braun EL, Braun MJ: Duplication of accelerated evolution and growth hormone gene in passerine birds. Mol Biol Evol 2008, 25:352-361. 10.1093/molbev/msm260.
54. Han K, Lee J, Meyer TJ, Remedios P, Goodwin L, Batzer MA: L1 recombination-associated deletions generate human genomic variation. Proc Natl Acad Sci 2008, 105:19366-19371. 10.1073/pnas.0807866105.
55. Stankiewicz P, Lupski JR: Genome architecture, rearrangements and genomic disorders. Trends Genet 2002, 18:74-82. 10.1016/S0168-9525(02)02592-1.
56. Xing J, Wang H, Belancio VP, Cordaux R, Deininger PL, Batzer MA: Emergence of primate genes by retrotransposon-mediated sequence transduction. Proc Natl Acad Sci 2006, 103:17608-17613. 10.1073/pnas.0603224103.
57. Li X, Wang X-J, Tannenhauser J, Podell S, Mukherjee P, Hertel M, Biane J, Masuda S, Nottebohm F, Gaasterland T: Genomic resources for songbird research and their use in characterizing gene expression during brain development. Proc Natl Acad Sci 2007, 104:6834-6839. 10.1073/pnas.0701619104.
58. Lovell PV, Clayton DF, Replogle KL, Mello CV: Birdsong "Transcriptomics": neurochemical specializations of the oscine song system. PLoS One 2008, 3:e3440. 10.1371/journal.pone.0003440.
59. Pfenning AR, Hara E, Whitney O, Rivas MV, Wang R, Roulhac PL, Howard JT, Wirthlin M, Lovell PV, Ganapathy G, Mouncastle J, Moseley MA, Thompson JW, Soderblom EJ, Iriki A, Kato M, Gilbert MTP, Zhang G, Bakken T, Bongaarts A, Bernard A, Lein E, Mello CV, Hartemink AJ, Jarvis ED: Convergent transcriptional specializations in the brains of humans and song learning birds. Science 2014, 346:1333.
60. Thuresson B, Westman JS, Olsson ML: Identification of a novel A4GALT exon reveals the genetic basis of the P1/P2 histo-blood groups. Blood 2011, 117:678-687. 10.1182/blood-2010-08-301333.
61. Szwergold BS: Fructosamine-6-phosphates are deglycated by phosphorylation to fructosamine-3,6-bisphosphates catalyzed by fructosamine-3-kinase (FN3K) and/or fructosamine-3-kinase-related-protein (FN3KRP). Med Hypotheses 2007, 68:37-45. 10.1016/j.mehy.2006.06.030.
62. Zhang Z, Futamura M, Vikis HG, Wang M, Li J, Wang Y, Guan K-L, You M: Positional cloning of the major quantitative trait locus underlying lung tumor susceptibility in mice. Proc Natl Acad Sci 2003, 100:12642-12647. 10.1073/pnas.2133947100.
63. Goldman SA, Nottebohm F: Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci 1983, 80:2390-2394. 10.1073/pnas.80.8.2390.
64. Alvarez-Buylla A, Nottebohm F: Migration of young neurons in adult avian brain. Nature 1988, 335:353-354. 10.1038/335353a0.
65. Zhang Z, Theler D, Kaminska KH, Hiller M, de la Grange P, Pudimat R, Rafalska I, Heinrich B, Bujnicki JM, Allain FH-T, Stamm S: The YTH domain is a novel RNA binding domain. J Biol Chem 2010, 285:14701-14710. 10.1074/jbc.M110.104711.
66. Morohashi K, Sahara H, Watashi K, Iwabata K, Sunoki T, Kuramochi K, Takakusagi K, Miyashita H, Sato N, Tanabe A, Shimotohno K, Kobayashi S, Sakaguchi K, Sugawara F: Cyclosporin A associated helicase-like protein facilitates the association of hepatitis C virus RNA polymerase with its cellular cyclophilin B. PLoS One 2011, 6:e18285. 10.1371/journal.pone.0018285.
67. Walbott H, Mouffok S, Capeyrou R, Lebaron S, Humbert O, van Tilbeurgh H, Henry Y, Leulliot N: Prp43p contains a processive helicase structural architecture with a specific regulatory domain. EMBO J 2010, 29:2194-2204. 10.1038/emboj.2010.102.
68. Knowles DG, McLysaght A: Recent de novo origin of human protein-coding genes. Genome Res 2009, 19:1752-1759. 10.1101/gr.095026.109.
69. Drickamer K: C-type lectin-like domains. Curr Opin Struct Biol 1999, 9:585-590. 10.1016/S0959-440X(99)00009-3.
70. Cambi A, Figdor CG: Dual function of C-type lectin-like receptors in the immune system. Curr Opin Cell Biol 2003, 15:539-546. 10.1016/j.ceb.2003.08.004.
71. Jessell TM: Adhesion molecules and the hierarchy of neural development. Neuron 1988, 1:3-13. 10.1016/0896-6273(88)90204-8.
72. Suh A, Paus M, Kiefmann M, Churakov G, Franke FA, Brosius J, Kriegs JO, Schmitz J: Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds. Nat Commun 2011, 2:443.
73. Striedter GF: The vocal control pathways in budgerigars differ from those in songbirds. J Comp Neurol 1994, 343:35-56. 10.1002/cne.903430104.
74. Kent WJ: BLAT-The BLAST-Like alignment tool. Genome Res 2002, 12:656-664. 10.1101/gr.229202. Article published online before March 2002.
75. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D: The human genome browser at UCSC. Genome Res 2002, 12:996-1006. 10.1101/gr.229102. Article published online before print in May 2002.
76. Ganapathy G, Howard J, Ward J, Li J, Li B, Li Y, Xiong Y, Zhang Y, Zhou S, Schwartz D, Schatz M, Aboukhalil R, Fedrigo O, Bukovnik L, Wang T, Wray G, Rasolonjatovo I, Winer R, Knight J, Koren S, Warren W, Zhang G, Phillippy A, Jarvis E: High-coverage sequencing and annotated assemblies of the budgerigar genome. GigaScience 2014, 3:11. 10.1186/2047-217X-3-11.
77. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP: Integrative genomics viewer. Nat Biotech 2011, 29:24-26. 10.1038/nbt.1754.
78. Kinsella RJ, Kähäri A, Haider S, Zamora J, Proctor G, Spudich G, Almeida-King J, Staines D, Derwent P, Kerhornou A, Kersey P, Flicek P: Ensembl BioMarts: a hub for data retrieval across taxonomic space. Database: the journal of biological databases and curation 2011, 2011:bar030.
79. Donthu R, Lewin H, Larkin D: SyntenyTracker: a tool for defining homologous synteny blocks using radiation hybrid maps and whole-genome sequence. BMC Res Notes 2009, 2:148. 10.1186/1756-0500-2-148.
80. Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong S-Y, Lopez R, Hunter S: InterProScan 5: genome-scale protein function classification. Bioinformatics 2014, 30:1236-1240. 10.1093/bioinformatics/btu031.
81. Replogle K, Arnold A, Ball G, Band M, Bensch S, Brenowitz E, Dong S, Drnevich J, Ferris M, George J, Gong G, Hasselquist D, Hernandez A, Kim R, Lewin H, Liu L, Lovell P, Mello C, Naurin S, Rodriguez-Zas S, Thimmapuram J, Wade J, Clayton D: The Songbird Neurogenomics (SoNG) Initiative: community-based tools and strategies for study of brain gene function and evolution. BMC Genomics 2008, 9:131. 10.1186/1471-2164-9-131.
82. Wada K, Howard JT, McConnell P, Whitney O, Lints T, Rivas MV, Horita H, Patterson MA, White SA, Scharff C, Haesler S, Zhao S, Sakaguchi H, Hagiwara M, Shiraki T, Hirozane-Kishikawa T, Skene P, Hayashizaki Y, Carninci P, Jarvis ED: A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc Natl Acad Sci 2006, 103:15212-15217. 10.1073/pnas.0607098103.
83. Mello CV, Vicario DS, Clayton DF: Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci U S A 1992, 89:6818-6822. 10.1073/pnas.89.15.6818.
84. Jarvis ED, Nottebohm F: Motor-driven gene expression. Proc Natl Acad Sci U S A 1997, 94:4097-4102. 10.1073/pnas.94.8.4097.