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1. Towards complete and error-free genome assemblies of all vertebrate species.

Author

Rhie, Arang, Rhie, Arang, McCarthy, Shane A, Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William, Fungtammasan, Arkarachai, Kim, Juwan, Lee, Chul, Ko, Byung June, Chaisson, Mark, Gedman, Gregory L, Cantin, Lindsey J, Thibaud-Nissen, Francoise, Haggerty, Leanne, Bista, Iliana, Smith, Michelle, Haase, Bettina, Mountcastle, Jacquelyn, Winkler, Sylke, Paez, Sadye, Howard, Jason, Vernes, Sonja C, Lama, Tanya M, Grutzner, Frank, Warren, Wesley C, Balakrishnan, Christopher N, Burt, Dave, George, Julia M, Biegler, Matthew T, Iorns, David, Digby, Andrew, Eason, Daryl, Robertson, Bruce, Edwards, Taylor, Wilkinson, Mark, Turner, George, Meyer, Axel, Kautt, Andreas F, Franchini, Paolo, Detrich, H William, Svardal, Hannes, Wagner, Maximilian, Naylor, Gavin JP, Pippel, Martin, Malinsky, Milan, Mooney, Mark, Simbirsky, Maria, Hannigan, Brett T, Pesout, Trevor, Houck, Marlys, Misuraca, Ann, Kingan, Sarah B, Hall, Richard, Kronenberg, Zev, Sović, Ivan, Dunn, Christopher, Ning, Zemin, Hastie, Alex, Lee, Joyce, Selvaraj, Siddarth, Green, Richard E, Putnam, Nicholas H, Gut, Ivo, Ghurye, Jay, Garrison, Erik, Sims, Ying, Collins, Joanna, Pelan, Sarah, Torrance, James, Tracey, Alan, Wood, Jonathan, Dagnew, Robel E, Guan, Dengfeng, London, Sarah E, Clayton, David F, Mello, Claudio V, Friedrich, Samantha R, Lovell, Peter V, Osipova, Ekaterina, Al-Ajli, Farooq O, Secomandi, Simona, Kim, Heebal, Theofanopoulou, Constantina, Hiller, Michael, Zhou, Yang, Harris, Robert S, Makova, Kateryna D, Medvedev, Paul, Hoffman, Jinna, Masterson, Patrick, Clark, Karen, Martin, Fergal, Howe, Kevin, Flicek, Paul, Walenz, Brian P, Kwak, Woori, Clawson, Hiram, Rhie, Arang, Rhie, Arang, McCarthy, Shane A, Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William, Fungtammasan, Arkarachai, Kim, Juwan, Lee, Chul, Ko, Byung June, Chaisson, Mark, Gedman, Gregory L, Cantin, Lindsey J, Thibaud-Nissen, Francoise, Haggerty, Leanne, Bista, Iliana, Smith, Michelle, Haase, Bettina, Mountcastle, Jacquelyn, Winkler, Sylke, Paez, Sadye, Howard, Jason, Vernes, Sonja C, Lama, Tanya M, Grutzner, Frank, Warren, Wesley C, Balakrishnan, Christopher N, Burt, Dave, George, Julia M, Biegler, Matthew T, Iorns, David, Digby, Andrew, Eason, Daryl, Robertson, Bruce, Edwards, Taylor, Wilkinson, Mark, Turner, George, Meyer, Axel, Kautt, Andreas F, Franchini, Paolo, Detrich, H William, Svardal, Hannes, Wagner, Maximilian, Naylor, Gavin JP, Pippel, Martin, Malinsky, Milan, Mooney, Mark, Simbirsky, Maria, Hannigan, Brett T, Pesout, Trevor, Houck, Marlys, Misuraca, Ann, Kingan, Sarah B, Hall, Richard, Kronenberg, Zev, Sović, Ivan, Dunn, Christopher, Ning, Zemin, Hastie, Alex, Lee, Joyce, Selvaraj, Siddarth, Green, Richard E, Putnam, Nicholas H, Gut, Ivo, Ghurye, Jay, Garrison, Erik, Sims, Ying, Collins, Joanna, Pelan, Sarah, Torrance, James, Tracey, Alan, Wood, Jonathan, Dagnew, Robel E, Guan, Dengfeng, London, Sarah E, Clayton, David F, Mello, Claudio V, Friedrich, Samantha R, Lovell, Peter V, Osipova, Ekaterina, Al-Ajli, Farooq O, Secomandi, Simona, Kim, Heebal, Theofanopoulou, Constantina, Hiller, Michael, Zhou, Yang, Harris, Robert S, Makova, Kateryna D, Medvedev, Paul, Hoffman, Jinna, Masterson, Patrick, Clark, Karen, Martin, Fergal, Howe, Kevin, Flicek, Paul, Walenz, Brian P, Kwak, Woori, and Clawson, Hiram

Abstract

High-quality and complete reference genome assemblies are fundamental for the application of genomics to biology, disease, and biodiversity conservation. However, such assemblies are available for only a few non-microbial species1-4. To address this issue, the international Genome 10K (G10K) consortium5,6 has worked over a five-year period to evaluate and develop cost-effective methods for assembling highly accurate and nearly complete reference genomes. Here we present lessons learned from generating assemblies for 16 species that represent six major vertebrate lineages. We confirm that long-read sequencing technologies are essential for maximizing genome quality, and that unresolved complex repeats and haplotype heterozygosity are major sources of assembly error when not handled correctly. Our assemblies correct substantial errors, add missing sequence in some of the best historical reference genomes, and reveal biological discoveries. These include the identification of many false gene duplications, increases in gene sizes, chromosome rearrangements that are specific to lineages, a repeated independent chromosome breakpoint in bat genomes, and a canonical GC-rich pattern in protein-coding genes and their regulatory regions. Adopting these lessons, we have embarked on the Vertebrate Genomes Project (VGP), an international effort to generate high-quality, complete reference genomes for all of the roughly 70,000 extant vertebrate species and to help to enable a new era of discovery across the life sciences.

Published
2021

2. Towards complete and error-free genome assemblies of all vertebrate species.

Author

Rhie, Arang, Rhie, Arang, McCarthy, Shane A, Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William, Fungtammasan, Arkarachai, Kim, Juwan, Lee, Chul, Ko, Byung June, Chaisson, Mark, Gedman, Gregory L, Cantin, Lindsey J, Thibaud-Nissen, Francoise, Haggerty, Leanne, Bista, Iliana, Smith, Michelle, Haase, Bettina, Mountcastle, Jacquelyn, Winkler, Sylke, Paez, Sadye, Howard, Jason, Vernes, Sonja C, Lama, Tanya M, Grutzner, Frank, Warren, Wesley C, Balakrishnan, Christopher N, Burt, Dave, George, Julia M, Biegler, Matthew T, Iorns, David, Digby, Andrew, Eason, Daryl, Robertson, Bruce, Edwards, Taylor, Wilkinson, Mark, Turner, George, Meyer, Axel, Kautt, Andreas F, Franchini, Paolo, Detrich, H William, Svardal, Hannes, Wagner, Maximilian, Naylor, Gavin JP, Pippel, Martin, Malinsky, Milan, Mooney, Mark, Simbirsky, Maria, Hannigan, Brett T, Pesout, Trevor, Houck, Marlys, Misuraca, Ann, Kingan, Sarah B, Hall, Richard, Kronenberg, Zev, Sović, Ivan, Dunn, Christopher, Ning, Zemin, Hastie, Alex, Lee, Joyce, Selvaraj, Siddarth, Green, Richard E, Putnam, Nicholas H, Gut, Ivo, Ghurye, Jay, Garrison, Erik, Sims, Ying, Collins, Joanna, Pelan, Sarah, Torrance, James, Tracey, Alan, Wood, Jonathan, Dagnew, Robel E, Guan, Dengfeng, London, Sarah E, Clayton, David F, Mello, Claudio V, Friedrich, Samantha R, Lovell, Peter V, Osipova, Ekaterina, Al-Ajli, Farooq O, Secomandi, Simona, Kim, Heebal, Theofanopoulou, Constantina, Hiller, Michael, Zhou, Yang, Harris, Robert S, Makova, Kateryna D, Medvedev, Paul, Hoffman, Jinna, Masterson, Patrick, Clark, Karen, Martin, Fergal, Howe, Kevin, Flicek, Paul, Walenz, Brian P, Kwak, Woori, Clawson, Hiram, Rhie, Arang, Rhie, Arang, McCarthy, Shane A, Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William, Fungtammasan, Arkarachai, Kim, Juwan, Lee, Chul, Ko, Byung June, Chaisson, Mark, Gedman, Gregory L, Cantin, Lindsey J, Thibaud-Nissen, Francoise, Haggerty, Leanne, Bista, Iliana, Smith, Michelle, Haase, Bettina, Mountcastle, Jacquelyn, Winkler, Sylke, Paez, Sadye, Howard, Jason, Vernes, Sonja C, Lama, Tanya M, Grutzner, Frank, Warren, Wesley C, Balakrishnan, Christopher N, Burt, Dave, George, Julia M, Biegler, Matthew T, Iorns, David, Digby, Andrew, Eason, Daryl, Robertson, Bruce, Edwards, Taylor, Wilkinson, Mark, Turner, George, Meyer, Axel, Kautt, Andreas F, Franchini, Paolo, Detrich, H William, Svardal, Hannes, Wagner, Maximilian, Naylor, Gavin JP, Pippel, Martin, Malinsky, Milan, Mooney, Mark, Simbirsky, Maria, Hannigan, Brett T, Pesout, Trevor, Houck, Marlys, Misuraca, Ann, Kingan, Sarah B, Hall, Richard, Kronenberg, Zev, Sović, Ivan, Dunn, Christopher, Ning, Zemin, Hastie, Alex, Lee, Joyce, Selvaraj, Siddarth, Green, Richard E, Putnam, Nicholas H, Gut, Ivo, Ghurye, Jay, Garrison, Erik, Sims, Ying, Collins, Joanna, Pelan, Sarah, Torrance, James, Tracey, Alan, Wood, Jonathan, Dagnew, Robel E, Guan, Dengfeng, London, Sarah E, Clayton, David F, Mello, Claudio V, Friedrich, Samantha R, Lovell, Peter V, Osipova, Ekaterina, Al-Ajli, Farooq O, Secomandi, Simona, Kim, Heebal, Theofanopoulou, Constantina, Hiller, Michael, Zhou, Yang, Harris, Robert S, Makova, Kateryna D, Medvedev, Paul, Hoffman, Jinna, Masterson, Patrick, Clark, Karen, Martin, Fergal, Howe, Kevin, Flicek, Paul, Walenz, Brian P, Kwak, Woori, and Clawson, Hiram

Abstract

High-quality and complete reference genome assemblies are fundamental for the application of genomics to biology, disease, and biodiversity conservation. However, such assemblies are available for only a few non-microbial species1-4. To address this issue, the international Genome 10K (G10K) consortium5,6 has worked over a five-year period to evaluate and develop cost-effective methods for assembling highly accurate and nearly complete reference genomes. Here we present lessons learned from generating assemblies for 16 species that represent six major vertebrate lineages. We confirm that long-read sequencing technologies are essential for maximizing genome quality, and that unresolved complex repeats and haplotype heterozygosity are major sources of assembly error when not handled correctly. Our assemblies correct substantial errors, add missing sequence in some of the best historical reference genomes, and reveal biological discoveries. These include the identification of many false gene duplications, increases in gene sizes, chromosome rearrangements that are specific to lineages, a repeated independent chromosome breakpoint in bat genomes, and a canonical GC-rich pattern in protein-coding genes and their regulatory regions. Adopting these lessons, we have embarked on the Vertebrate Genomes Project (VGP), an international effort to generate high-quality, complete reference genomes for all of the roughly 70,000 extant vertebrate species and to help to enable a new era of discovery across the life sciences.

Published
2021

3. Towards complete and error-free genome assemblies of all vertebrate species

Author

Rhie, Arang, McCarthy, Shane A., Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William, Fungtammasan, Arkarachai, Kim, Juwan, Lee, Chul, Ko, Byung June, Chaisson, Mark, Gedman, Gregory L., Cantin, Lindsey J., Thibaud-Nissen, Francoise, Haggerty, Leanne, Bista, Iliana, Smith, Michelle, Haase, Bettina, Mountcastle, Jacquelyn, Winkler, Sylke, Paez, Sadye, Howard, Jason, Vernes, Sonja C., Lama, Tanya M., Grutzner, Frank, Warren, Wesley C., Balakrishnan, Christopher N., Burt, Dave, George, Julia M., Biegler, Matthew T., Iorns, David, Digby, Andrew, Eason, Daryl, Robertson, Bruce, Edwards, Taylor, Wilkinson, Mark, Turner, George, Meyer, Axel, Kautt, Andreas F., Franchini, Paolo, Detrich, H. William, Svardal, Hannes, Wagner, Maximilian, Naylor, Gavin J.P., Pippel, Martin, Malinsky, Milan, Mooney, Mark, Simbirsky, Maria, Hannigan, Brett T., Pesout, Trevor, Houck, Marlys, Misuraca, Ann, Kingan, Sarah B., Hall, Richard, Kronenberg, Zev, Sović, Ivan, Dunn, Christopher, Ning, Zemin, Hastie, Alex, Lee, Joyce, Selvaraj, Siddarth, Green, Richard E., Putnam, Nicholas H., Gut, Ivo, Ghurye, Jay, Garrison, Erik, Sims, Ying, Collins, Joanna, Pelan, Sarah, Torrance, James, Tracey, Alan, Wood, Jonathan, Dagnew, Robel E., Guan, Dengfeng, London, Sarah E., Clayton, David F., Mello, Claudio V., Friedrich, Samantha R., Lovell, Peter V., Osipova, Ekaterina, Al-Ajli, Farooq O., Secomandi, Simona, Kim, Heebal, Theofanopoulou, Constantina, Hiller, Michael, Zhou, Yang, Harris, Robert S., Makova, Kateryna D., Medvedev, Paul, Hoffman, Jinna, Masterson, Patrick, Clark, Karen, Martin, Fergal, Howe, Kevin, Flicek, Paul, Walenz, Brian P., Kwak, Woori, Clawson, Hiram, Diekhans, Mark, Nassar, Luis, Paten, Benedict, Kraus, Robert H. S., Crawford, Andrew J., Gilbert, M. Thomas P., Zhang, Guojie, Venkatesh, Byrappa, Murphy, Robert W., Koepfli, Klaus-Peter, Shapiro, Beth, Johnson, Warren E., Di Palma, Federica, Marques-Bonet, Tomas, Teeling, Emma C., Warnow, Tandy, Graves, Jennifer Marshall, Ryder, Oliver A., Haussler, David, O’Brien, Stephen J., Korlach, Jonas, Lewin, Harris A., Howe, Kerstin, Myers, Eugene W., Durbin, Richard, Phillippy, Adam M., Jarvis, Erich D., Rhie, Arang, McCarthy, Shane A., Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William, Fungtammasan, Arkarachai, Kim, Juwan, Lee, Chul, Ko, Byung June, Chaisson, Mark, Gedman, Gregory L., Cantin, Lindsey J., Thibaud-Nissen, Francoise, Haggerty, Leanne, Bista, Iliana, Smith, Michelle, Haase, Bettina, Mountcastle, Jacquelyn, Winkler, Sylke, Paez, Sadye, Howard, Jason, Vernes, Sonja C., Lama, Tanya M., Grutzner, Frank, Warren, Wesley C., Balakrishnan, Christopher N., Burt, Dave, George, Julia M., Biegler, Matthew T., Iorns, David, Digby, Andrew, Eason, Daryl, Robertson, Bruce, Edwards, Taylor, Wilkinson, Mark, Turner, George, Meyer, Axel, Kautt, Andreas F., Franchini, Paolo, Detrich, H. William, Svardal, Hannes, Wagner, Maximilian, Naylor, Gavin J.P., Pippel, Martin, Malinsky, Milan, Mooney, Mark, Simbirsky, Maria, Hannigan, Brett T., Pesout, Trevor, Houck, Marlys, Misuraca, Ann, Kingan, Sarah B., Hall, Richard, Kronenberg, Zev, Sović, Ivan, Dunn, Christopher, Ning, Zemin, Hastie, Alex, Lee, Joyce, Selvaraj, Siddarth, Green, Richard E., Putnam, Nicholas H., Gut, Ivo, Ghurye, Jay, Garrison, Erik, Sims, Ying, Collins, Joanna, Pelan, Sarah, Torrance, James, Tracey, Alan, Wood, Jonathan, Dagnew, Robel E., Guan, Dengfeng, London, Sarah E., Clayton, David F., Mello, Claudio V., Friedrich, Samantha R., Lovell, Peter V., Osipova, Ekaterina, Al-Ajli, Farooq O., Secomandi, Simona, Kim, Heebal, Theofanopoulou, Constantina, Hiller, Michael, Zhou, Yang, Harris, Robert S., Makova, Kateryna D., Medvedev, Paul, Hoffman, Jinna, Masterson, Patrick, Clark, Karen, Martin, Fergal, Howe, Kevin, Flicek, Paul, Walenz, Brian P., Kwak, Woori, Clawson, Hiram, Diekhans, Mark, Nassar, Luis, Paten, Benedict, Kraus, Robert H. S., Crawford, Andrew J., Gilbert, M. Thomas P., Zhang, Guojie, Venkatesh, Byrappa, Murphy, Robert W., Koepfli, Klaus-Peter, Shapiro, Beth, Johnson, Warren E., Di Palma, Federica, Marques-Bonet, Tomas, Teeling, Emma C., Warnow, Tandy, Graves, Jennifer Marshall, Ryder, Oliver A., Haussler, David, O’Brien, Stephen J., Korlach, Jonas, Lewin, Harris A., Howe, Kerstin, Myers, Eugene W., Durbin, Richard, Phillippy, Adam M., and Jarvis, Erich D.

Abstract

High-quality and complete reference genome assemblies are fundamental for the application of genomics to biology, disease, and biodiversity conservation. However, such assemblies are available for only a few non-microbial species1–4. To address this issue, the international Genome 10K (G10K) consortium5,6 has worked over a five-year period to evaluate and develop cost-effective methods for assembling highly accurate and nearly complete reference genomes. Here we present lessons learned from generating assemblies for 16 species that represent six major vertebrate lineages. We confirm that long-read sequencing technologies are essential for maximizing genome quality, and that unresolved complex repeats and haplotype heterozygosity are major sources of assembly error when not handled correctly. Our assemblies correct substantial errors, add missing sequence in some of the best historical reference genomes, and reveal biological discoveries. These include the identification of many false gene duplications, increases in gene sizes, chromosome rearrangements that are specific to lineages, a repeated independent chromosome breakpoint in bat genomes, and a canonical GC-rich pattern in protein-coding genes and their regulatory regions. Adopting these lessons, we have embarked on the Vertebrate Genomes Project (VGP), an international effort to generate high-quality, complete reference genomes for all of the roughly 70,000 extant vertebrate species and to help to enable a new era of discovery across the life sciences.

Published
2021

4. Towards complete and error-free genome assemblies of all vertebrate species

Author

National Institutes of Health (US), National Human Genome Research Institute (US), Ministry of Health and Welfare (South Korea), Wellcome Trust, European Molecular Biology Laboratory, Howard Hughes Medical Institute, Rockefeller University, Robert and Rosabel Osborne Endowment, European Commission, National Library of Medicine (US), Korea Institute of Marine Science & Technology, Ministry of Oceans and Fisheries (South Korea), Alfred P. Sloan Foundation, Max Planck Society, Maine Department of Inland Fisheries & Wildlife, National Science Foundation (US), University of Queensland, Science Exchange, Northeastern University (US), Federal Ministry of Education and Research (Germany), EMBO, National Key Research and Development Program (China), Qatar Society of Al-Gannas (Algannas), Katara Cultural Village, Government of Qatar, Monash University Malaysia, Hessen State Ministry of Higher Education, Research and the Arts, Ministry of Science, Research and Art Baden-Württemberg, Agency for Science, Technology and Research A*STAR (Singapore), European Research Council, Ministerio de Ciencia, Innovación y Universidades (España), Fundación la Caixa, Generalitat de Catalunya, Irish Research Council, Danish National Research Foundation, Australian Research Council, Rhie, Arang, McCarthy, Shane A., Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William, Fungtammasan, Arkarachai, Kim, Juwan, Lee, Chul, Haase, Bettina, Mountcastle, Jacquelyn, Winkler, Sylke, Paez, Sadye, Howard, Jason, Vernes, Sonja C, Lama, Tanya M, Grützner, Frank, Warren, Wesley C., Balakrishnan, Christopher N., Pippel, Martin, Burt, Dave, George, Julia M., Biegler, Matthew T., Iorns, David, Digby, Andrew, Eason, Daryl, Robertson, Bruce, Edwards, Taylor, Wilkinson, Mark, Turner, George, Malinsky, Milan, Meyer, Axel, Kautt, Andreas F., Franchini, Paolo, Detrich III, H. William, Svardal, Hannes, Wagner, Maximilian, Naylor, Gavin J. P., Mooney, Mark, Simbirsky, Maria, Hannigan, Brett T., Pesout, Trevor, Houck, Marlys L., Misuraca, Ann, Kingan, Sarah B., Hall, Richard, Wood, Jonathan, Kronenberg, Zev, Sović, Ivan, Dunn, Christopher, Ning, Zemin, Hastie, Alex, Lee, Joyce, Selvaraj, Siddarth, Green, Richard E., Putnam, Nicholas H., Gut, Ivo, Dagnew, Robel E., Ghurye, Jay, Garrison, Erik, Sims, Ying, Collins, Joanna, Pelan, Sarah, Torrance, James, Tracey, Alan, Guan, Dengfeng, London, Sarah E., Clayton, David F., Mello, Claudio V., Friedrich, Samantha R., Lovell, Peter V., Osipova, Ekaterina, Al-Ajli, Farooq O., Diekhans, Mark, Secomandi, Simona, Kim, Heebal, Theofanopoulou, Constantina, Hiller, Michael, Zhou, Yang, Harris, Robert S., Makova, Kateryna D., Medvedev, Paul, Hoffman, Jinna, Masterson, Patrick, Nassar, Luis, Clark, Karen, Martin, Fergal, Howe, Kevin, Flicek, Paul, Walenz, Brian P., Kwak, Woori, Clawson, Hiram, Paten, Benedict, Kraus, Robert H. S., Crawford, Andrew J., Gilbert, M. Thomas P., Zhang, Guojie, Venkatesh, Byrappa, Murphy, Robert W., Koepfli, Klaus-Peter, Ko, Byung June, Shapiro, Beth, Johnson, Warren E., Di Palma, Federica, Marqués-Bonet, Tomàs, Teeling, Emma C., Warnow, Tandy, Marshall Graves, Jennifer, Ryder, Oliver A., Haussler, David, O’Brien, Stephen J., Chaisson, Mark, Korlach, Jonas, Lewin, Harris A., Howe, Kerstin, Myers, Eugene W., Durbin, Richard, Phillippy, Adam M., Jarvis, Erich D., Gedman, Gregory L., Cantin, Lindsey J., Thibaud-Nissen, Francoise, Haggerty, Leanne, Bista, Iliana, Smith, Michelle, National Institutes of Health (US), National Human Genome Research Institute (US), Ministry of Health and Welfare (South Korea), Wellcome Trust, European Molecular Biology Laboratory, Howard Hughes Medical Institute, Rockefeller University, Robert and Rosabel Osborne Endowment, European Commission, National Library of Medicine (US), Korea Institute of Marine Science & Technology, Ministry of Oceans and Fisheries (South Korea), Alfred P. Sloan Foundation, Max Planck Society, Maine Department of Inland Fisheries & Wildlife, National Science Foundation (US), University of Queensland, Science Exchange, Northeastern University (US), Federal Ministry of Education and Research (Germany), EMBO, National Key Research and Development Program (China), Qatar Society of Al-Gannas (Algannas), Katara Cultural Village, Government of Qatar, Monash University Malaysia, Hessen State Ministry of Higher Education, Research and the Arts, Ministry of Science, Research and Art Baden-Württemberg, Agency for Science, Technology and Research A*STAR (Singapore), European Research Council, Ministerio de Ciencia, Innovación y Universidades (España), Fundación la Caixa, Generalitat de Catalunya, Irish Research Council, Danish National Research Foundation, Australian Research Council, Rhie, Arang, McCarthy, Shane A., Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William, Fungtammasan, Arkarachai, Kim, Juwan, Lee, Chul, Haase, Bettina, Mountcastle, Jacquelyn, Winkler, Sylke, Paez, Sadye, Howard, Jason, Vernes, Sonja C, Lama, Tanya M, Grützner, Frank, Warren, Wesley C., Balakrishnan, Christopher N., Pippel, Martin, Burt, Dave, George, Julia M., Biegler, Matthew T., Iorns, David, Digby, Andrew, Eason, Daryl, Robertson, Bruce, Edwards, Taylor, Wilkinson, Mark, Turner, George, Malinsky, Milan, Meyer, Axel, Kautt, Andreas F., Franchini, Paolo, Detrich III, H. William, Svardal, Hannes, Wagner, Maximilian, Naylor, Gavin J. P., Mooney, Mark, Simbirsky, Maria, Hannigan, Brett T., Pesout, Trevor, Houck, Marlys L., Misuraca, Ann, Kingan, Sarah B., Hall, Richard, Wood, Jonathan, Kronenberg, Zev, Sović, Ivan, Dunn, Christopher, Ning, Zemin, Hastie, Alex, Lee, Joyce, Selvaraj, Siddarth, Green, Richard E., Putnam, Nicholas H., Gut, Ivo, Dagnew, Robel E., Ghurye, Jay, Garrison, Erik, Sims, Ying, Collins, Joanna, Pelan, Sarah, Torrance, James, Tracey, Alan, Guan, Dengfeng, London, Sarah E., Clayton, David F., Mello, Claudio V., Friedrich, Samantha R., Lovell, Peter V., Osipova, Ekaterina, Al-Ajli, Farooq O., Diekhans, Mark, Secomandi, Simona, Kim, Heebal, Theofanopoulou, Constantina, Hiller, Michael, Zhou, Yang, Harris, Robert S., Makova, Kateryna D., Medvedev, Paul, Hoffman, Jinna, Masterson, Patrick, Nassar, Luis, Clark, Karen, Martin, Fergal, Howe, Kevin, Flicek, Paul, Walenz, Brian P., Kwak, Woori, Clawson, Hiram, Paten, Benedict, Kraus, Robert H. S., Crawford, Andrew J., Gilbert, M. Thomas P., Zhang, Guojie, Venkatesh, Byrappa, Murphy, Robert W., Koepfli, Klaus-Peter, Ko, Byung June, Shapiro, Beth, Johnson, Warren E., Di Palma, Federica, Marqués-Bonet, Tomàs, Teeling, Emma C., Warnow, Tandy, Marshall Graves, Jennifer, Ryder, Oliver A., Haussler, David, O’Brien, Stephen J., Chaisson, Mark, Korlach, Jonas, Lewin, Harris A., Howe, Kerstin, Myers, Eugene W., Durbin, Richard, Phillippy, Adam M., Jarvis, Erich D., Gedman, Gregory L., Cantin, Lindsey J., Thibaud-Nissen, Francoise, Haggerty, Leanne, Bista, Iliana, and Smith, Michelle

Abstract

High-quality and complete reference genome assemblies are fundamental for the application of genomics to biology, disease, and biodiversity conservation. However, such assemblies are available for only a few non-microbial species1,2,3,4. To address this issue, the international Genome 10K (G10K) consortium5,6 has worked over a five-year period to evaluate and develop cost-effective methods for assembling highly accurate and nearly complete reference genomes. Here we present lessons learned from generating assemblies for 16 species that represent six major vertebrate lineages. We confirm that long-read sequencing technologies are essential for maximizing genome quality, and that unresolved complex repeats and haplotype heterozygosity are major sources of assembly error when not handled correctly. Our assemblies correct substantial errors, add missing sequence in some of the best historical reference genomes, and reveal biological discoveries. These include the identification of many false gene duplications, increases in gene sizes, chromosome rearrangements that are specific to lineages, a repeated independent chromosome breakpoint in bat genomes, and a canonical GC-rich pattern in protein-coding genes and their regulatory regions. Adopting these lessons, we have embarked on the Vertebrate Genomes Project (VGP), an international effort to generate high-quality, complete reference genomes for all of the roughly 70,000 extant vertebrate species and to help to enable a new era of discovery across the life sciences.

Published
2021

5. Towards complete and error-free genome assemblies of all vertebrate species

Author

Rhie, Arang, McCarthy, Shane A., Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William, Fungtammasan, Arkarachai, Kim, Juwan, Lee, Chul, Ko, Byung June, Chaisson, Mark, Gedman, Gregory L., Cantin, Lindsey J., Thibaud-Nissen, Francoise, Haggerty, Leanne, Bista, Iliana, Smith, Michelle, Haase, Bettina, Mountcastle, Jacquelyn, Winkler, Sylke, Paez, Sadye, Howard, Jason, Vernes, Sonja C., Lama, Tanya M., Grutzner, Frank, Warren, Wesley C., Balakrishnan, Christopher N., Burt, Dave, George, Julia M., Biegler, Matthew T., Iorns, David, Digby, Andrew, Eason, Daryl, Robertson, Bruce, Edwards, Taylor, Wilkinson, Mark, Turner, George, Meyer, Axel, Kautt, Andreas F., Franchini, Paolo, Detrich, H. William, Svardal, Hannes, Wagner, Maximilian, Naylor, Gavin J.P., Pippel, Martin, Malinsky, Milan, Mooney, Mark, Simbirsky, Maria, Hannigan, Brett T., Pesout, Trevor, Houck, Marlys, Misuraca, Ann, Kingan, Sarah B., Hall, Richard, Kronenberg, Zev, Sović, Ivan, Dunn, Christopher, Ning, Zemin, Hastie, Alex, Lee, Joyce, Selvaraj, Siddarth, Green, Richard E., Putnam, Nicholas H., Gut, Ivo, Ghurye, Jay, Garrison, Erik, Sims, Ying, Collins, Joanna, Pelan, Sarah, Torrance, James, Tracey, Alan, Wood, Jonathan, Dagnew, Robel E., Guan, Dengfeng, London, Sarah E., Clayton, David F., Mello, Claudio V., Friedrich, Samantha R., Lovell, Peter V., Osipova, Ekaterina, Al-Ajli, Farooq O., Secomandi, Simona, Kim, Heebal, Theofanopoulou, Constantina, Hiller, Michael, Zhou, Yang, Harris, Robert S., Makova, Kateryna D., Medvedev, Paul, Hoffman, Jinna, Masterson, Patrick, Clark, Karen, Martin, Fergal, Howe, Kevin, Flicek, Paul, Walenz, Brian P., Kwak, Woori, Clawson, Hiram, Diekhans, Mark, Nassar, Luis, Paten, Benedict, Kraus, Robert H. S., Crawford, Andrew J., Gilbert, M. Thomas P., Zhang, Guojie, Venkatesh, Byrappa, Murphy, Robert W., Koepfli, Klaus-Peter, Shapiro, Beth, Johnson, Warren E., Di Palma, Federica, Marques-Bonet, Tomas, Teeling, Emma C., Warnow, Tandy, Graves, Jennifer Marshall, Ryder, Oliver A., Haussler, David, O’Brien, Stephen J., Korlach, Jonas, Lewin, Harris A., Howe, Kerstin, Myers, Eugene W., Durbin, Richard, Phillippy, Adam M., Jarvis, Erich D., Rhie, Arang, McCarthy, Shane A., Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William, Fungtammasan, Arkarachai, Kim, Juwan, Lee, Chul, Ko, Byung June, Chaisson, Mark, Gedman, Gregory L., Cantin, Lindsey J., Thibaud-Nissen, Francoise, Haggerty, Leanne, Bista, Iliana, Smith, Michelle, Haase, Bettina, Mountcastle, Jacquelyn, Winkler, Sylke, Paez, Sadye, Howard, Jason, Vernes, Sonja C., Lama, Tanya M., Grutzner, Frank, Warren, Wesley C., Balakrishnan, Christopher N., Burt, Dave, George, Julia M., Biegler, Matthew T., Iorns, David, Digby, Andrew, Eason, Daryl, Robertson, Bruce, Edwards, Taylor, Wilkinson, Mark, Turner, George, Meyer, Axel, Kautt, Andreas F., Franchini, Paolo, Detrich, H. William, Svardal, Hannes, Wagner, Maximilian, Naylor, Gavin J.P., Pippel, Martin, Malinsky, Milan, Mooney, Mark, Simbirsky, Maria, Hannigan, Brett T., Pesout, Trevor, Houck, Marlys, Misuraca, Ann, Kingan, Sarah B., Hall, Richard, Kronenberg, Zev, Sović, Ivan, Dunn, Christopher, Ning, Zemin, Hastie, Alex, Lee, Joyce, Selvaraj, Siddarth, Green, Richard E., Putnam, Nicholas H., Gut, Ivo, Ghurye, Jay, Garrison, Erik, Sims, Ying, Collins, Joanna, Pelan, Sarah, Torrance, James, Tracey, Alan, Wood, Jonathan, Dagnew, Robel E., Guan, Dengfeng, London, Sarah E., Clayton, David F., Mello, Claudio V., Friedrich, Samantha R., Lovell, Peter V., Osipova, Ekaterina, Al-Ajli, Farooq O., Secomandi, Simona, Kim, Heebal, Theofanopoulou, Constantina, Hiller, Michael, Zhou, Yang, Harris, Robert S., Makova, Kateryna D., Medvedev, Paul, Hoffman, Jinna, Masterson, Patrick, Clark, Karen, Martin, Fergal, Howe, Kevin, Flicek, Paul, Walenz, Brian P., Kwak, Woori, Clawson, Hiram, Diekhans, Mark, Nassar, Luis, Paten, Benedict, Kraus, Robert H. S., Crawford, Andrew J., Gilbert, M. Thomas P., Zhang, Guojie, Venkatesh, Byrappa, Murphy, Robert W., Koepfli, Klaus-Peter, Shapiro, Beth, Johnson, Warren E., Di Palma, Federica, Marques-Bonet, Tomas, Teeling, Emma C., Warnow, Tandy, Graves, Jennifer Marshall, Ryder, Oliver A., Haussler, David, O’Brien, Stephen J., Korlach, Jonas, Lewin, Harris A., Howe, Kerstin, Myers, Eugene W., Durbin, Richard, Phillippy, Adam M., and Jarvis, Erich D.

Abstract

High-quality and complete reference genome assemblies are fundamental for the application of genomics to biology, disease, and biodiversity conservation. However, such assemblies are available for only a few non-microbial species1–4. To address this issue, the international Genome 10K (G10K) consortium5,6 has worked over a five-year period to evaluate and develop cost-effective methods for assembling highly accurate and nearly complete reference genomes. Here we present lessons learned from generating assemblies for 16 species that represent six major vertebrate lineages. We confirm that long-read sequencing technologies are essential for maximizing genome quality, and that unresolved complex repeats and haplotype heterozygosity are major sources of assembly error when not handled correctly. Our assemblies correct substantial errors, add missing sequence in some of the best historical reference genomes, and reveal biological discoveries. These include the identification of many false gene duplications, increases in gene sizes, chromosome rearrangements that are specific to lineages, a repeated independent chromosome breakpoint in bat genomes, and a canonical GC-rich pattern in protein-coding genes and their regulatory regions. Adopting these lessons, we have embarked on the Vertebrate Genomes Project (VGP), an international effort to generate high-quality, complete reference genomes for all of the roughly 70,000 extant vertebrate species and to help to enable a new era of discovery across the life sciences.

Published
2021

6. Variation in Reproductive Success Across Captive Populations:Methodological Differences, Potential Biases and Opportunities

Author

Griffith, Simon C., Crino, Ondi L., Andrew, Samuel C., Nomano, Fumiaki Y., Adkins-Regan, Elizabeth, Alonso-Alvarez, Carlos, Bailey, Ida E., Bittner, Stephanie S., Bolton, Peri E., Boner, Winnie, Boogert, Neeltje, Boucaud, Ingrid C.A., Briga, Michael, Buchanan, Katherine L., Caspers, Barbara A., Cichoń, Mariusz, Clayton, David F., Derégnaucourt, Sebastien, Forstmeier, Wolfgang, Guillette, Lauren M., Hartley, Ian R., Healy, Susan D., Hill, Davina L., Holveck, Marie Jeanne, Hurley, Laura L., Ihle, Malika, Tobias Krause, E., Mainwaring, Mark C., Marasco, Valeria, Mariette, Mylene M., Martin-Wintle, Meghan S., McCowan, Luke S.C., McMahon, Maeve, Monaghan, Pat, Nager, Ruedi G., Naguib, Marc, Nord, Andreas, Potvin, Dominique A., Prior, Nora H., Riebel, Katharina, Romero-Haro, Ana A., Royle, Nick J., Rutkowska, Joanna, Schuett, Wiebke, Swaddle, John P., Tobler, Michael, Trompf, Larissa, Varian-Ramos, Claire W., Vignal, Clémentine, Villain, Avelyne S., Griffith, Simon C., Crino, Ondi L., Andrew, Samuel C., Nomano, Fumiaki Y., Adkins-Regan, Elizabeth, Alonso-Alvarez, Carlos, Bailey, Ida E., Bittner, Stephanie S., Bolton, Peri E., Boner, Winnie, Boogert, Neeltje, Boucaud, Ingrid C.A., Briga, Michael, Buchanan, Katherine L., Caspers, Barbara A., Cichoń, Mariusz, Clayton, David F., Derégnaucourt, Sebastien, Forstmeier, Wolfgang, Guillette, Lauren M., Hartley, Ian R., Healy, Susan D., Hill, Davina L., Holveck, Marie Jeanne, Hurley, Laura L., Ihle, Malika, Tobias Krause, E., Mainwaring, Mark C., Marasco, Valeria, Mariette, Mylene M., Martin-Wintle, Meghan S., McCowan, Luke S.C., McMahon, Maeve, Monaghan, Pat, Nager, Ruedi G., Naguib, Marc, Nord, Andreas, Potvin, Dominique A., Prior, Nora H., Riebel, Katharina, Romero-Haro, Ana A., Royle, Nick J., Rutkowska, Joanna, Schuett, Wiebke, Swaddle, John P., Tobler, Michael, Trompf, Larissa, Varian-Ramos, Claire W., Vignal, Clémentine, and Villain, Avelyne S.

Abstract

Our understanding of fundamental organismal biology has been disproportionately influenced by studies of a relatively small number of ‘model’ species extensively studied in captivity. Laboratory populations of model species are commonly subject to a number of forms of past and current selection that may affect experimental outcomes. Here, we examine these processes and their outcomes in one of the most widely used vertebrate species in the laboratory – the zebra finch (Taeniopygia guttata). This important model species is used for research across a broad range of fields, partly due to the ease with which it can be bred in captivity. However despite this perceived amenability, we demonstrate extensive variation in the success with which different laboratories and studies bred their subjects, and overall only 64% of all females that were given the opportunity, bred successfully in the laboratory. We identify and review several environmental, husbandry, life-history and behavioural factors that potentially contribute to this variation. The variation in reproductive success across individuals could lead to biases in experimental outcomes and drive some of the heterogeneity in research outcomes across studies. The zebra finch remains an excellent captive animal system and our aim is to sharpen the insight that future studies of this species can provide, both to our understanding of this species and also with respect to the reproduction of captive animals more widely. We hope to improve systematic reporting methods and that further investigation of the issues we raise will lead both to advances in our fundamental understanding of avian reproduction as well as to improvements in future welfare and experimental efficiency.

Published
2017

7. Variation in reproductive success across captive populations: Methodological differences, potential biases and opportunities

Author

Griffith, Simon C., Crino, Ondi L., Andrew, Samuel C., Nomano, Fumiaki Y., Adkins-Regan, Elizabeth, Alonso-Álvarez, Carlos, Bailey, Ida E., Bittner, Stephanie S., Bolton, Peri E., Boner, Winnie, Boogert, Neeltje, Boucaud, Ingrid C. A., Briga, Michael, Buchanan, Katherine L., Caspers, Barbara A., Cichón, Mariusz, Clayton, David F., Derégnaucourt, Sebastien, Forstmeier, Wolfgang, Guillette, Lauren M., Hartley, Ian R., Healy, Susan D., Hill, Davina L., Holveck, Marie-Jeanne, Hurley, Laura L., Ihle, Malika, Krause, E. Tobias, Mainwaring, Mark C., Marasco, Valeria, Mariette, Mylene M., Martin-Wintle, Meghan S., McCowan, Luke S. C., McMahon, Maeve, Monaghan, Pat, Nager, Ruedi G., Naguib, Marc, Nord, Andreas, Potvin, Dominique A., Prior, Nora H., Riebel, Katharina, Romero-Haro, Ana A., Royle, Nick J., Rutkowska, Joanna, Schuett, Wiebke, Swaddle, John P., Tobler, Michael, Trompf, Larissa, Varian-Ramos, Claire W., Vignal, Clémentine, Villain, Avelyne S., Williams, Tony D., Griffith, Simon C., Crino, Ondi L., Andrew, Samuel C., Nomano, Fumiaki Y., Adkins-Regan, Elizabeth, Alonso-Álvarez, Carlos, Bailey, Ida E., Bittner, Stephanie S., Bolton, Peri E., Boner, Winnie, Boogert, Neeltje, Boucaud, Ingrid C. A., Briga, Michael, Buchanan, Katherine L., Caspers, Barbara A., Cichón, Mariusz, Clayton, David F., Derégnaucourt, Sebastien, Forstmeier, Wolfgang, Guillette, Lauren M., Hartley, Ian R., Healy, Susan D., Hill, Davina L., Holveck, Marie-Jeanne, Hurley, Laura L., Ihle, Malika, Krause, E. Tobias, Mainwaring, Mark C., Marasco, Valeria, Mariette, Mylene M., Martin-Wintle, Meghan S., McCowan, Luke S. C., McMahon, Maeve, Monaghan, Pat, Nager, Ruedi G., Naguib, Marc, Nord, Andreas, Potvin, Dominique A., Prior, Nora H., Riebel, Katharina, Romero-Haro, Ana A., Royle, Nick J., Rutkowska, Joanna, Schuett, Wiebke, Swaddle, John P., Tobler, Michael, Trompf, Larissa, Varian-Ramos, Claire W., Vignal, Clémentine, Villain, Avelyne S., and Williams, Tony D.

Abstract

Our understanding of fundamental organismal biology has been disproportionately influenced by studies of a relatively small number of ‘model’ species extensively studied in captivity. Laboratory populations of model species are commonly subject to a number of forms of past and current selection that may affect experimental outcomes. Here, we examine these processes and their outcomes in one of the most widely used vertebrate species in the laboratory – the zebra finch (Taeniopygia guttata). This important model species is used for research across a broad range of fields, partly due to the ease with which it can be bred in captivity. However despite this perceived amenability, we demonstrate extensive variation in the success with which different laboratories and studies bred their subjects, and overall only 64% of all females that were given the opportunity, bred successfully in the laboratory. We identify and review several environmental, husbandry, life-history and behavioural factors that potentially contribute to this variation. The variation in reproductive success across individuals could lead to biases in experimental outcomes and drive some of the heterogeneity in research outcomes across studies. The zebra finch remains an excellent captive animal system and our aim is to sharpen the insight that future studies of this species can provide, both to our understanding of this species and also with respect to the reproduction of captive animals more widely. We hope to improve systematic reporting methods and that further investigation of the issues we raise will lead both to advances in our fundamental understanding of avian reproduction as well as to improvements in future welfare and experimental efficiency.

Published
2017

8. Brain transcriptome sequencing and assembly of three songbird model systems for the study of social behavior.

Author

Balakrishnan, Christopher N, Balakrishnan, Christopher N, Mukai, Motoko, Gonser, Rusty A, Wingfield, John C, London, Sarah E, Tuttle, Elaina M, Clayton, David F, Balakrishnan, Christopher N, Balakrishnan, Christopher N, Mukai, Motoko, Gonser, Rusty A, Wingfield, John C, London, Sarah E, Tuttle, Elaina M, and Clayton, David F

Abstract

Emberizid sparrows (emberizidae) have played a prominent role in the study of avian vocal communication and social behavior. We present here brain transcriptomes for three emberizid model systems, song sparrow Melospiza melodia, white-throated sparrow Zonotrichia albicollis, and Gambel's white-crowned sparrow Zonotrichia leucophrys gambelii. Each of the assemblies covered fully or in part, over 89% of the previously annotated protein coding genes in the zebra finch Taeniopygia guttata, with 16,846, 15,805, and 16,646 unique BLAST hits in song, white-throated and white-crowned sparrows, respectively. As in previous studies, we find tissue of origin (auditory forebrain versus hypothalamus and whole brain) as an important determinant of overall expression profile. We also demonstrate the successful isolation of RNA and RNA-sequencing from post-mortem samples from building strikes and suggest that such an approach could be useful when traditional sampling opportunities are limited. These transcriptomes will be an important resource for the study of social behavior in birds and for data driven annotation of forthcoming whole genome sequences for these and other bird species.

Published
2014

9. Brain transcriptome sequencing and assembly of three songbird model systems for the study of social behavior.

Author

Balakrishnan, Christopher N, Balakrishnan, Christopher N, Mukai, Motoko, Gonser, Rusty A, Wingfield, John C, London, Sarah E, Tuttle, Elaina M, Clayton, David F, Balakrishnan, Christopher N, Balakrishnan, Christopher N, Mukai, Motoko, Gonser, Rusty A, Wingfield, John C, London, Sarah E, Tuttle, Elaina M, and Clayton, David F

Abstract

Emberizid sparrows (emberizidae) have played a prominent role in the study of avian vocal communication and social behavior. We present here brain transcriptomes for three emberizid model systems, song sparrow Melospiza melodia, white-throated sparrow Zonotrichia albicollis, and Gambel's white-crowned sparrow Zonotrichia leucophrys gambelii. Each of the assemblies covered fully or in part, over 89% of the previously annotated protein coding genes in the zebra finch Taeniopygia guttata, with 16,846, 15,805, and 16,646 unique BLAST hits in song, white-throated and white-crowned sparrows, respectively. As in previous studies, we find tissue of origin (auditory forebrain versus hypothalamus and whole brain) as an important determinant of overall expression profile. We also demonstrate the successful isolation of RNA and RNA-sequencing from post-mortem samples from building strikes and suggest that such an approach could be useful when traditional sampling opportunities are limited. These transcriptomes will be an important resource for the study of social behavior in birds and for data driven annotation of forthcoming whole genome sequences for these and other bird species.

Published
2014

10. The genome of a songbird

Author

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

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 chicken-the 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.

Published
2010
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11. Molecular evolution of genes in avian genomes

Author

Nam, Kiwoong, Mugal, Carina, Nabholz, Benoit, Schielzeth, Holger, Wolf, Jochen B. W., Backström, Niclas, Künstner, Axel, Balakrishnan, Christopher N., Heger, Andreas, Ponting, Chris P., Clayton, David F., Ellegren, Hans, Nam, Kiwoong, Mugal, Carina, Nabholz, Benoit, Schielzeth, Holger, Wolf, Jochen B. W., Backström, Niclas, Künstner, Axel, Balakrishnan, Christopher N., Heger, Andreas, Ponting, Chris P., Clayton, David F., and Ellegren, Hans

Abstract

Background: Obtaining a draft genome sequence of the zebra finch (Taeniopygia guttata), the second bird genome to be sequenced, provides the necessary resource for whole-genome comparative analysis of gene sequence evolution in a non-mammalian vertebrate lineage. To analyze basic molecular evolutionary processes during avian evolution, and to contrast these with the situation in mammals, we aligned the protein-coding sequences of 8,384 1: 1 orthologs of chicken, zebra finch, a lizard and three mammalian species. Results: We found clear differences in the substitution rate at fourfold degenerate sites, being lowest in the ancestral bird lineage, intermediate in the chicken lineage and highest in the zebra finch lineage, possibly reflecting differences in generation time. We identified positively selected and/or rapidly evolving genes in avian lineages and found an over-representation of several functional classes, including anion transporter activity, calcium ion binding, cell adhesion and microtubule cytoskeleton. Conclusions: Focusing specifically on genes of neurological interest and genes differentially expressed in the unique vocal control nuclei of the songbird brain, we find a number of positively selected genes, including synaptic receptors. We found no evidence that selection for beneficial alleles is more efficient in regions of high recombination; in fact, there was a weak yet significant negative correlation between omega and recombination rate, which is in the direction predicted by the Hill-Robertson effect if slightly deleterious mutations contribute to protein evolution. These findings set the stage for studies of functional genetics of avian genes.

Published
2010
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12. Natural selection in protein-coding genes expressed in avian brain

Author

Axelsson, Erik, Hultin-Rosenberg, Lina, Brandström, Mikael, Zwalen, Martin, Clayton, David F., Ellegren, Hans, Axelsson, Erik, Hultin-Rosenberg, Lina, Brandström, Mikael, Zwalen, Martin, Clayton, David F., and Ellegren, Hans

Abstract

The evolution of birds from theropod dinosaurs took place approximately 150 million years ago, and was associated with a number of specific adaptations that are still evident among extant birds, including feathers, song and extravagant secondary sexual characteristics. Knowledge about the molecular evolutionary background to such adaptations is lacking. Here, we analyse the evolution of > 5000 protein-coding gene sequences expressed in zebra finch brain by comparison to orthologous sequences in chicken. Mean d(N)/d(S) is 0.085 and genes with their maximal expression in the eye and central nervous system have the lowest mean d(N)/d(S) value, while those expressed in digestive and reproductive tissues exhibit the highest. We find that fast-evolving genes (those which have higher than expected rate of nonsynonymous substitution, indicative of adaptive evolution) are enriched for biological functions such as fertilization, muscle contraction, defence response, response to stress, wounding and endogenous stimulus, and cell death. After alignment to mammalian orthologues, we identify a catalogue of 228 genes that show a significantly higher rate of protein evolution in the two bird lineages than in mammals. These accelerated bird genes, representing candidates for avian-specific adaptations, include genes implicated in vocal learning and other cognitive processes. Moreover, colouration genes evolve faster in birds than in mammals, which may have been driven by sexual selection for extravagant plumage characteristics.

Published
2008
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13. The Songbird Neurogenomics (SoNG) Initiative: community-based tools and strategies for study of brain gene function and evolution.

Author

Replogle, Kirstin, Replogle, Kirstin, Arnold, Arthur P, Ball, Gregory F, Band, Mark, Bensch, Staffan, Brenowitz, Eliot A, Dong, Shu, Drnevich, Jenny, Ferris, Margaret, George, Julia M, Gong, George, Hasselquist, Dennis, Hernandez, Alvaro G, Kim, Ryan, Lewin, Harris A, Liu, Lei, Lovell, Peter V, Mello, Claudio V, Naurin, Sara, Rodriguez-Zas, Sandra, Thimmapuram, Jyothi, Wade, Juli, Clayton, David F, Replogle, Kirstin, Replogle, Kirstin, Arnold, Arthur P, Ball, Gregory F, Band, Mark, Bensch, Staffan, Brenowitz, Eliot A, Dong, Shu, Drnevich, Jenny, Ferris, Margaret, George, Julia M, Gong, George, Hasselquist, Dennis, Hernandez, Alvaro G, Kim, Ryan, Lewin, Harris A, Liu, Lei, Lovell, Peter V, Mello, Claudio V, Naurin, Sara, Rodriguez-Zas, Sandra, Thimmapuram, Jyothi, Wade, Juli, and Clayton, David F

Abstract

BackgroundSongbirds hold great promise for biomedical, environmental and evolutionary research. A complete draft sequence of the zebra finch genome is imminent, yet a need remains for application of genomic resources within a research community traditionally focused on ethology and neurobiological methods. In response, we developed a core set of genomic tools and a novel collaborative strategy to probe gene expression in diverse songbird species and natural contexts.ResultsWe end-sequenced cDNAs from zebra finch brain and incorporated additional sequences from community sources into a database of 86,784 high quality reads. These assembled into 31,658 non-redundant contigs and singletons, which we annotated via BLAST search of chicken and human databases. The results are publicly available in the ESTIMA:Songbird database. We produced a spotted cDNA microarray with 20,160 addresses representing 17,214 non-redundant products of an estimated 11,500-15,000 genes, validating it by analysis of immediate-early gene (zenk) gene activation following song exposure and by demonstrating effective cross hybridization to genomic DNAs of other songbird species in the Passerida Parvorder. Our assembly was also used in the design of the "Lund-zfa" Affymetrix array representing approximately 22,000 non-redundant sequences. When the two arrays were hybridized to cDNAs from the same set of male and female zebra finch brain samples, both arrays detected a common set of regulated transcripts with a Pearson correlation coefficient of 0.895. To stimulate use of these resources by the songbird research community and to maintain consistent technical standards, we devised a "Community Collaboration" mechanism whereby individual birdsong researchers develop experiments and provide tissues, but a single individual in the community is responsible for all RNA extractions, labelling and microarray hybridizations.ConclusionImmediately, these results set the foundation for a coordinated set of 25 pla

Published
2008

14. The Songbird Neurogenomics (SoNG) Initiative: community-based tools and strategies for study of brain gene function and evolution.

Author

Replogle, Kirstin, Replogle, Kirstin, Arnold, Arthur P, Ball, Gregory F, Band, Mark, Bensch, Staffan, Brenowitz, Eliot A, Dong, Shu, Drnevich, Jenny, Ferris, Margaret, George, Julia M, Gong, George, Hasselquist, Dennis, Hernandez, Alvaro G, Kim, Ryan, Lewin, Harris A, Liu, Lei, Lovell, Peter V, Mello, Claudio V, Naurin, Sara, Rodriguez-Zas, Sandra, Thimmapuram, Jyothi, Wade, Juli, Clayton, David F, Replogle, Kirstin, Replogle, Kirstin, Arnold, Arthur P, Ball, Gregory F, Band, Mark, Bensch, Staffan, Brenowitz, Eliot A, Dong, Shu, Drnevich, Jenny, Ferris, Margaret, George, Julia M, Gong, George, Hasselquist, Dennis, Hernandez, Alvaro G, Kim, Ryan, Lewin, Harris A, Liu, Lei, Lovell, Peter V, Mello, Claudio V, Naurin, Sara, Rodriguez-Zas, Sandra, Thimmapuram, Jyothi, Wade, Juli, and Clayton, David F

Abstract

BackgroundSongbirds hold great promise for biomedical, environmental and evolutionary research. A complete draft sequence of the zebra finch genome is imminent, yet a need remains for application of genomic resources within a research community traditionally focused on ethology and neurobiological methods. In response, we developed a core set of genomic tools and a novel collaborative strategy to probe gene expression in diverse songbird species and natural contexts.ResultsWe end-sequenced cDNAs from zebra finch brain and incorporated additional sequences from community sources into a database of 86,784 high quality reads. These assembled into 31,658 non-redundant contigs and singletons, which we annotated via BLAST search of chicken and human databases. The results are publicly available in the ESTIMA:Songbird database. We produced a spotted cDNA microarray with 20,160 addresses representing 17,214 non-redundant products of an estimated 11,500-15,000 genes, validating it by analysis of immediate-early gene (zenk) gene activation following song exposure and by demonstrating effective cross hybridization to genomic DNAs of other songbird species in the Passerida Parvorder. Our assembly was also used in the design of the "Lund-zfa" Affymetrix array representing approximately 22,000 non-redundant sequences. When the two arrays were hybridized to cDNAs from the same set of male and female zebra finch brain samples, both arrays detected a common set of regulated transcripts with a Pearson correlation coefficient of 0.895. To stimulate use of these resources by the songbird research community and to maintain consistent technical standards, we devised a "Community Collaboration" mechanism whereby individual birdsong researchers develop experiments and provide tissues, but a single individual in the community is responsible for all RNA extractions, labelling and microarray hybridizations.ConclusionImmediately, these results set the foundation for a coordinated set of 25 pla

Published
2008

15. Dosage compensation is less effective in birds than in mammals.

Author

Itoh, Yuichiro, Itoh, Yuichiro, Melamed, Esther, Yang, Xia, Kampf, Kathy, Wang, Susanna, Yehya, Nadir, Van Nas, Atila, Replogle, Kirstin, Band, Mark R, Clayton, David F, Schadt, Eric E, Lusis, Aldons J, Arnold, Arthur P, Itoh, Yuichiro, Itoh, Yuichiro, Melamed, Esther, Yang, Xia, Kampf, Kathy, Wang, Susanna, Yehya, Nadir, Van Nas, Atila, Replogle, Kirstin, Band, Mark R, Clayton, David F, Schadt, Eric E, Lusis, Aldons J, and Arnold, Arthur P

Abstract

BackgroundIn animals with heteromorphic sex chromosomes, dosage compensation of sex-chromosome genes is thought to be critical for species survival. Diverse molecular mechanisms have evolved to effectively balance the expressed dose of X-linked genes between XX and XY animals, and to balance expression of X and autosomal genes. Dosage compensation is not understood in birds, in which females (ZW) and males (ZZ) differ in the number of Z chromosomes.ResultsUsing microarray analysis, we compared the male:female ratio of expression of sets of Z-linked and autosomal genes in two bird species, zebra finch and chicken, and in two mammalian species, mouse and human. Male:female ratios of expression were significantly higher for Z genes than for autosomal genes in several finch and chicken tissues. In contrast, in mouse and human the male:female ratio of expression of X-linked genes is quite similar to that of autosomal genes, indicating effective dosage compensation even in humans, in which a significant percentage of genes escape X-inactivation.ConclusionBirds represent an unprecedented case in which genes on one sex chromosome are expressed on average at constitutively higher levels in one sex compared with the other. Sex-chromosome dosage compensation is surprisingly ineffective in birds, suggesting that some genomes can do without effective sex-specific sex-chromosome dosage compensation mechanisms.

Published
2007

16. Dosage compensation is less effective in birds than in mammals.

Author

Itoh, Yuichiro, Itoh, Yuichiro, Melamed, Esther, Yang, Xia, Kampf, Kathy, Wang, Susanna, Yehya, Nadir, Van Nas, Atila, Replogle, Kirstin, Band, Mark R, Clayton, David F, Schadt, Eric E, Lusis, Aldons J, Arnold, Arthur P, Itoh, Yuichiro, Itoh, Yuichiro, Melamed, Esther, Yang, Xia, Kampf, Kathy, Wang, Susanna, Yehya, Nadir, Van Nas, Atila, Replogle, Kirstin, Band, Mark R, Clayton, David F, Schadt, Eric E, Lusis, Aldons J, and Arnold, Arthur P

Abstract

BackgroundIn animals with heteromorphic sex chromosomes, dosage compensation of sex-chromosome genes is thought to be critical for species survival. Diverse molecular mechanisms have evolved to effectively balance the expressed dose of X-linked genes between XX and XY animals, and to balance expression of X and autosomal genes. Dosage compensation is not understood in birds, in which females (ZW) and males (ZZ) differ in the number of Z chromosomes.ResultsUsing microarray analysis, we compared the male:female ratio of expression of sets of Z-linked and autosomal genes in two bird species, zebra finch and chicken, and in two mammalian species, mouse and human. Male:female ratios of expression were significantly higher for Z genes than for autosomal genes in several finch and chicken tissues. In contrast, in mouse and human the male:female ratio of expression of X-linked genes is quite similar to that of autosomal genes, indicating effective dosage compensation even in humans, in which a significant percentage of genes escape X-inactivation.ConclusionBirds represent an unprecedented case in which genes on one sex chromosome are expressed on average at constitutively higher levels in one sex compared with the other. Sex-chromosome dosage compensation is surprisingly ineffective in birds, suggesting that some genomes can do without effective sex-specific sex-chromosome dosage compensation mechanisms.

Published
2007

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