The genome of a songbird

Wesley C. Warren; David F. Clayton; Hans Ellegren; Arthur P. Arnold; Ladeana W. Hillier; Axel Künstner; Steve Searle; Simon White; Albert J. Vilella; Susan Fairley; Andreas Heger; Lesheng Kong; Chris P. Ponting; Erich D. Jarvis; Claudio V. Mello; Pat Minx; Peter Lovell; Tarciso A.F. Velho; Margaret Ferris; Christopher N. Balakrishnan; Saurabh Sinha; Charles Blatti; Sarah E. London; Yun Li; Ya Chi Lin; Julia George; Jonathan Sweedler; Bruce Southey; Preethi Gunaratne; Michael Watson; Kiwoong Nam; Niclas Backström; Linnea Smeds; Benoit Nabholz; Yuichiro Itoh; Osceola Whitney; Andreas R. Pfenning; Jason Howard; Martin Völker; Bejamin M. Skinner; Darren K. Griffin; Liang Ye; William M. McLaren; Paul Flicek; Victor Quesada; Gloria Velasco; Carlos Lopez-Otin; Xose S. Puente; Tsviya Olender; Doron Lancet; Arian F.A. Smit; Robert Hubley; Miriam K. Konkel; Jerilyn A. Walker; Mark A. Batzer; Wanjun Gu; David D. Pollock; Lin Chen; Ze Cheng; Evan E. Eichler; Jessica Stapley; Jon Slate; Robert Ekblom; Tim Birkhead; Terry Burke; David Burt; Constance Scharff; Iris Adam; Hugues Richard; Marc Sultan; Alexey Soldatov; Hans Lehrach; Scott V. Edwards; Shiaw Pyng Yang; Xiaoching Li; Tina Graves; Lucinda Fulton; Joanne Nelson; Asif Chinwalla; Shunfeng Hou; Elaine R. Mardis; Richard K. Wilson

doi:10.1038/nature08819

The genome of a songbird

Wesley C. Warren, David F. Clayton, Hans Ellegren, Arthur P. Arnold, Ladeana W. Hillier, Axel Künstner, Steve Searle, Simon White, Albert J. Vilella, Susan Fairley, Andreas Heger, Lesheng Kong, Chris P. Ponting, Erich D. Jarvis, Claudio V. Mello, Pat Minx, Peter Lovell, Tarciso A.F. Velho, Margaret Ferris, Christopher N. BalakrishnanSaurabh Sinha, Charles Blatti, Sarah E. London, Yun Li, Ya Chi Lin, Julia George, Jonathan Sweedler, Bruce Southey, Preethi Gunaratne, Michael Watson, Kiwoong Nam, Niclas Backström, Linnea Smeds, Benoit Nabholz, Yuichiro Itoh, Osceola Whitney, Andreas R. Pfenning, Jason Howard, Martin Völker, Bejamin M. Skinner, Darren K. Griffin, Liang Ye, William M. McLaren, Paul Flicek, Victor Quesada, Gloria Velasco, Carlos Lopez-Otin, Xose S. Puente, Tsviya Olender, Doron Lancet, Arian F.A. Smit, Robert Hubley, Miriam K. Konkel, Jerilyn A. Walker, Mark A. Batzer, Wanjun Gu, David D. Pollock, Lin Chen, Ze Cheng, Evan E. Eichler, Jessica Stapley, Jon Slate, Robert Ekblom, Tim Birkhead, Terry Burke, David Burt, Constance Scharff, Iris Adam, Hugues Richard, Marc Sultan, Alexey Soldatov, Hans Lehrach, Scott V. Edwards, Shiaw Pyng Yang, Xiaoching Li, Tina Graves, Lucinda Fulton, Joanne Nelson, Asif Chinwalla, Shunfeng Hou, Elaine R. Mardis, Richard K. Wilson

Behavioral Neuroscience

Research output: Contribution to journal › Article › peer-review

654 Scopus citations

Abstract

The zebra finch is an important model organism in several fields with unique relevance to human neuroscience. Like other songbirds, the zebra finch communicates through learned vocalizations, an ability otherwise documented only in humans and a few other animals and lacking in the chickenthe only bird with a sequenced genome until now. Here we present a structural, functional and comparative analysis of the genome sequence of the zebra finch (Taeniopygia guttata), which is a songbird belonging to the large avian order Passeriformes. We find that the overall structures of the genomes are similar in zebra finch and chicken, but they differ in many intrachromosomal rearrangements, lineage-specific gene family expansions, the number of long-terminal-repeat- based retrotransposons, and mechanisms of sex chromosome dosage compensation. We show that song behaviour engages gene regulatory networks in the zebra finch brain, altering the expression of long non-coding RNAs, microRNAs, transcription factors and their targets. We also show evidence for rapid molecular evolution in the songbird lineage of genes that are regulated during song experience. These results indicate an active involvement of the genome in neural processes underlying vocal communication and identify potential genetic substrates for the evolution and regulation of this behaviour.

Original language	English (US)
Pages (from-to)	757-762
Number of pages	6
Journal	Nature
Volume	464
Issue number	7289
DOIs	https://doi.org/10.1038/nature08819
State	Published - Apr 1 2010

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Warren, W. C., Clayton, D. F., Ellegren, H., Arnold, A. P., Hillier, L. W., Künstner, A., Searle, S., White, S., Vilella, A. J., Fairley, S., Heger, A., Kong, L., Ponting, C. P., Jarvis, E. D., Mello, C. V., Minx, P., Lovell, P., Velho, T. A. F., Ferris, M., ... Wilson, R. K. (2010). The genome of a songbird. Nature, 464(7289), 757-762. https://doi.org/10.1038/nature08819

Warren, WC, Clayton, DF, Ellegren, H, Arnold, AP, Hillier, LW, Künstner, 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, YC, George, J, Sweedler, J, Southey, B, Gunaratne, P, Watson, M, Nam, K, Backström, N, Smeds, L, Nabholz, B, Itoh, Y, Whitney, O, Pfenning, AR, Howard, J, Völker, M, Skinner, BM, Griffin, DK, Ye, L, McLaren, WM, Flicek, P, Quesada, V, Velasco, G, Lopez-Otin, C, Puente, XS, Olender, T, Lancet, D, Smit, AFA, Hubley, R, Konkel, MK, Walker, JA, Batzer, MA, Gu, W, Pollock, DD, Chen, L, Cheng, Z, Eichler, EE, Stapley, J, Slate, J, Ekblom, R, Birkhead, T, Burke, T, Burt, D, Scharff, C, Adam, I, Richard, H, Sultan, M, Soldatov, A, Lehrach, H, Edwards, SV, Yang, SP, Li, X, Graves, T, Fulton, L, Nelson, J, Chinwalla, A, Hou, S, Mardis, ER & Wilson, RK 2010, 'The genome of a songbird', Nature, vol. 464, no. 7289, pp. 757-762. https://doi.org/10.1038/nature08819

@article{4b7f9f307c7d4a81a6385672b318a35a,

title = "The genome of a songbird",

abstract = "The zebra finch is an important model organism in several fields with unique relevance to human neuroscience. Like other songbirds, the zebra finch communicates through learned vocalizations, an ability otherwise documented only in humans and a few other animals and lacking in the chickenthe only bird with a sequenced genome until now. Here we present a structural, functional and comparative analysis of the genome sequence of the zebra finch (Taeniopygia guttata), which is a songbird belonging to the large avian order Passeriformes. We find that the overall structures of the genomes are similar in zebra finch and chicken, but they differ in many intrachromosomal rearrangements, lineage-specific gene family expansions, the number of long-terminal-repeat- based retrotransposons, and mechanisms of sex chromosome dosage compensation. We show that song behaviour engages gene regulatory networks in the zebra finch brain, altering the expression of long non-coding RNAs, microRNAs, transcription factors and their targets. We also show evidence for rapid molecular evolution in the songbird lineage of genes that are regulated during song experience. These results indicate an active involvement of the genome in neural processes underlying vocal communication and identify potential genetic substrates for the evolution and regulation of this behaviour.",

author = "Warren, {Wesley C.} and Clayton, {David F.} and Hans Ellegren and Arnold, {Arthur P.} and Hillier, {Ladeana W.} and Axel K{\"u}nstner and Steve Searle and Simon White and Vilella, {Albert J.} and Susan Fairley and Andreas Heger and Lesheng Kong and Ponting, {Chris P.} and Jarvis, {Erich D.} and Mello, {Claudio V.} and Pat Minx and Peter Lovell and Velho, {Tarciso A.F.} and Margaret Ferris and Balakrishnan, {Christopher N.} and Saurabh Sinha and Charles Blatti and London, {Sarah E.} and Yun Li and Lin, {Ya Chi} and Julia George and Jonathan Sweedler and Bruce Southey and Preethi Gunaratne and Michael Watson and Kiwoong Nam and Niclas Backstr{\"o}m and Linnea Smeds and Benoit Nabholz and Yuichiro Itoh and Osceola Whitney and Pfenning, {Andreas R.} and Jason Howard and Martin V{\"o}lker and Skinner, {Bejamin M.} and Griffin, {Darren K.} and Liang Ye and McLaren, {William M.} and Paul Flicek and Victor Quesada and Gloria Velasco and Carlos Lopez-Otin and Puente, {Xose S.} and Tsviya Olender and Doron Lancet and Smit, {Arian F.A.} and Robert Hubley and Konkel, {Miriam K.} and Walker, {Jerilyn A.} and Batzer, {Mark A.} and Wanjun Gu and Pollock, {David D.} and Lin Chen and Ze Cheng and Eichler, {Evan E.} and Jessica Stapley and Jon Slate and Robert Ekblom and Tim Birkhead and Terry Burke and David Burt and Constance Scharff and Iris Adam and Hugues Richard and Marc Sultan and Alexey Soldatov and Hans Lehrach and Edwards, {Scott V.} and Yang, {Shiaw Pyng} and Xiaoching Li and Tina Graves and Lucinda Fulton and Joanne Nelson and Asif Chinwalla and Shunfeng Hou and Mardis, {Elaine R.} and Wilson, {Richard K.}",

note = "Funding Information: Acknowledgements The sequencing of zebra finch was funded by the National Human Genome Research Institute (NHGRI). Further research support included grants to D.F.C. (NIH RO1 NS045264 and RO1 NS051820), H.E. (Swedish Research Council and Knut and Alice Wallenberg Foundation), E.D.J. (HHMI, NIH Directors Pioneer Award and R01 DC007218), M.A.B. (NIH RO1 GM59290) and J.S. (Biotechnology and Biological Sciences Research Council grant number BBE0175091). Resources for exploring the sequence and annotation data are available on browser displays available at UCSC (http://genome.ucsc.edu), Ensembl (http://www.ensembl.org), the NCBI (http://www.ncbi.nlm.nih.gov) and http://aviangenomes.org. We thank K. Lindblad-Toh for permission to use the green anole lizard genome assembly, the Production Sequencing Group of The Genome Center at Washington University School of Medicine for generating all the sequence reads used for genome assembly, and the Clemson University Genome Institute for the construction of the BAC library. We would like to recognize all the important published work that we were unable to cite owing to space limitations.",

year = "2010",

month = apr,

day = "1",

doi = "10.1038/nature08819",

language = "English (US)",

volume = "464",

pages = "757--762",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7289",

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TY - JOUR

T1 - The genome of a songbird

AU - Warren, Wesley C.

AU - Clayton, David F.

AU - Ellegren, Hans

AU - Arnold, Arthur P.

AU - Hillier, Ladeana W.

AU - Künstner, Axel

AU - Searle, Steve

AU - White, Simon

AU - Vilella, Albert J.

AU - Fairley, Susan

AU - Heger, Andreas

AU - Kong, Lesheng

AU - Ponting, Chris P.

AU - Jarvis, Erich D.

AU - Mello, Claudio V.

AU - Minx, Pat

AU - Lovell, Peter

AU - Velho, Tarciso A.F.

AU - Ferris, Margaret

AU - Balakrishnan, Christopher N.

AU - Sinha, Saurabh

AU - Blatti, Charles

AU - London, Sarah E.

AU - Li, Yun

AU - Lin, Ya Chi

AU - George, Julia

AU - Sweedler, Jonathan

AU - Southey, Bruce

AU - Gunaratne, Preethi

AU - Watson, Michael

AU - Nam, Kiwoong

AU - Backström, Niclas

AU - Smeds, Linnea

AU - Nabholz, Benoit

AU - Itoh, Yuichiro

AU - Whitney, Osceola

AU - Pfenning, Andreas R.

AU - Howard, Jason

AU - Völker, Martin

AU - Skinner, Bejamin M.

AU - Griffin, Darren K.

AU - Ye, Liang

AU - McLaren, William M.

AU - Flicek, Paul

AU - Quesada, Victor

AU - Velasco, Gloria

AU - Lopez-Otin, Carlos

AU - Puente, Xose S.

AU - Olender, Tsviya

AU - Lancet, Doron

AU - Smit, Arian F.A.

AU - Hubley, Robert

AU - Konkel, Miriam K.

AU - Walker, Jerilyn A.

AU - Batzer, Mark A.

AU - Gu, Wanjun

AU - Pollock, David D.

AU - Chen, Lin

AU - Cheng, Ze

AU - Eichler, Evan E.

AU - Stapley, Jessica

AU - Slate, Jon

AU - Ekblom, Robert

AU - Birkhead, Tim

AU - Burke, Terry

AU - Burt, David

AU - Scharff, Constance

AU - Adam, Iris

AU - Richard, Hugues

AU - Sultan, Marc

AU - Soldatov, Alexey

AU - Lehrach, Hans

AU - Edwards, Scott V.

AU - Yang, Shiaw Pyng

AU - Li, Xiaoching

AU - Graves, Tina

AU - Fulton, Lucinda

AU - Nelson, Joanne

AU - Chinwalla, Asif

AU - Hou, Shunfeng

AU - Mardis, Elaine R.

AU - Wilson, Richard K.

N1 - Funding Information: Acknowledgements The sequencing of zebra finch was funded by the National Human Genome Research Institute (NHGRI). Further research support included grants to D.F.C. (NIH RO1 NS045264 and RO1 NS051820), H.E. (Swedish Research Council and Knut and Alice Wallenberg Foundation), E.D.J. (HHMI, NIH Directors Pioneer Award and R01 DC007218), M.A.B. (NIH RO1 GM59290) and J.S. (Biotechnology and Biological Sciences Research Council grant number BBE0175091). Resources for exploring the sequence and annotation data are available on browser displays available at UCSC (http://genome.ucsc.edu), Ensembl (http://www.ensembl.org), the NCBI (http://www.ncbi.nlm.nih.gov) and http://aviangenomes.org. We thank K. Lindblad-Toh for permission to use the green anole lizard genome assembly, the Production Sequencing Group of The Genome Center at Washington University School of Medicine for generating all the sequence reads used for genome assembly, and the Clemson University Genome Institute for the construction of the BAC library. We would like to recognize all the important published work that we were unable to cite owing to space limitations.

PY - 2010/4/1

Y1 - 2010/4/1

N2 - The zebra finch is an important model organism in several fields with unique relevance to human neuroscience. Like other songbirds, the zebra finch communicates through learned vocalizations, an ability otherwise documented only in humans and a few other animals and lacking in the chickenthe only bird with a sequenced genome until now. Here we present a structural, functional and comparative analysis of the genome sequence of the zebra finch (Taeniopygia guttata), which is a songbird belonging to the large avian order Passeriformes. We find that the overall structures of the genomes are similar in zebra finch and chicken, but they differ in many intrachromosomal rearrangements, lineage-specific gene family expansions, the number of long-terminal-repeat- based retrotransposons, and mechanisms of sex chromosome dosage compensation. We show that song behaviour engages gene regulatory networks in the zebra finch brain, altering the expression of long non-coding RNAs, microRNAs, transcription factors and their targets. We also show evidence for rapid molecular evolution in the songbird lineage of genes that are regulated during song experience. These results indicate an active involvement of the genome in neural processes underlying vocal communication and identify potential genetic substrates for the evolution and regulation of this behaviour.

AB - The zebra finch is an important model organism in several fields with unique relevance to human neuroscience. Like other songbirds, the zebra finch communicates through learned vocalizations, an ability otherwise documented only in humans and a few other animals and lacking in the chickenthe only bird with a sequenced genome until now. Here we present a structural, functional and comparative analysis of the genome sequence of the zebra finch (Taeniopygia guttata), which is a songbird belonging to the large avian order Passeriformes. We find that the overall structures of the genomes are similar in zebra finch and chicken, but they differ in many intrachromosomal rearrangements, lineage-specific gene family expansions, the number of long-terminal-repeat- based retrotransposons, and mechanisms of sex chromosome dosage compensation. We show that song behaviour engages gene regulatory networks in the zebra finch brain, altering the expression of long non-coding RNAs, microRNAs, transcription factors and their targets. We also show evidence for rapid molecular evolution in the songbird lineage of genes that are regulated during song experience. These results indicate an active involvement of the genome in neural processes underlying vocal communication and identify potential genetic substrates for the evolution and regulation of this behaviour.

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The genome of a songbird

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