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1. 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 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

Subjects
Biological Sciences, Bioinformatics and Computational Biology, Genetics, Human Genome, Biotechnology, Generic health relevance, Animals, Birds, Gene Library, Genome, Genome Size, Genome, Mitochondrial, Genomics, Haplotypes, High-Throughput Nucleotide Sequencing, Molecular Sequence Annotation, Sequence Alignment, Sequence Analysis, DNA, Sex Chromosomes, Vertebrates, General Science & Technology
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. Bird song comparison using deep learning trained from avian perceptual judgments.

Author

Zandberg, Lies, Morfi, Veronica, George, Julia M., Clayton, David F., Stowell, Dan, and Lachlan, Robert F.

Subjects
OPERANT conditioning, BIRDSONGS, ZEBRA finch, ANIMAL communication, SONGBIRDS, DEEP learning
Abstract

Our understanding of bird song, a model system for animal communication and the neurobiology of learning, depends critically on making reliable, validated comparisons between the complex multidimensional syllables that are used in songs. However, most assessments of song similarity are based on human inspection of spectrograms, or computational methods developed from human intuitions. Using a novel automated operant conditioning system, we collected a large corpus of zebra finches' (Taeniopygia guttata) decisions about song syllable similarity. We use this dataset to compare and externally validate similarity algorithms in widely-used publicly available software (Raven, Sound Analysis Pro, Luscinia). Although these methods all perform better than chance, they do not closely emulate the avian assessments. We then introduce a novel deep learning method that can produce perceptual similarity judgements trained on such avian decisions. We find that this new method outperforms the established methods in accuracy and more closely approaches the avian assessments. Inconsistent (hence ambiguous) decisions are a common occurrence in animal behavioural data; we show that a modification of the deep learning training that accommodates these leads to the strongest performance. We argue this approach is the best way to validate methods to compare song similarity, that our dataset can be used to validate novel methods, and that the general approach can easily be extended to other species. Author summary: How do birds hear the differences between their songs? This fascinating question carries implications, since the study of bird song, a model system for the neurobiology of learning and animal communication, depends critically on our ability to assess the similarity of songs. Traditionally, researchers compare sounds by human assessment, or use computational methods based on human intuitions about similarity. However, neither approach is connected to birds' own perception of sound similarity. Here, using a novel automated operant conditioning system, we recorded many thousands of acoustic judgments of similarity from zebra finches, and used this perceptual decision data for the first time to train a deep learning system. The trained system outperforms other computational methods for the task of making the same judgments as birds. This algorithm to compare song similarity, together with the potential of extending the general approach to other species, places the study of bird song on a firmer footing. [ABSTRACT FROM AUTHOR]

Published
2024
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6. Parental developmental experience affects vocal learning in offspring.

Author

Kraft, Fanny-Linn H., Crino, Ondi L., Adeniran-Obey, Saidat O., Moraney, Raven A., Clayton, David F., George, Julia M., and Buchanan, Katherine L.

Subjects
BIRDSONGS, HEREDITY, GENE expression, SOCIAL learning, COGNITIVE learning, ZEBRA finch
Abstract

Cultural and genetic inheritance combine to enable rapid changes in trait expression, but their relative importance in determining trait expression across generations is not clear. Birdsong is a socially learned cognitive trait that is subject to both cultural and genetic inheritance, as well as being affected by early developmental conditions. We sought to test whether early-life conditions in one generation can affect song acquisition in the next generation. We exposed one generation (F1) of nestlings to elevated corticosterone (CORT) levels, allowed them to breed freely as adults, and quantified their son's (F2) ability to copy the song of their social father. We also quantified the neurogenetic response to song playback through immediate early gene (IEG) expression in the auditory forebrain. F2 males with only one corticosterone-treated parent copied their social father's song less accurately than males with two control parents. Expression of ARC in caudomedial nidopallium (NCM) correlated with father-son song similarity, and patterns of expression levels of several IEGs in caudomedial mesopallium (CMM) in response to father song playback differed between control F2 sons and those with a CORT-treated father only. This is the first study to demonstrate that developmental conditions can affect social learning and neurogenetic responses in a subsequent generation. [ABSTRACT FROM AUTHOR]

Published
2024
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7. Concurrent invasions of European starlings in Australia and North America reveal population‐specific differentiation in shared genomic regions

Author

Hofmeister, Natalie R., primary, Stuart, Katarina C., additional, Warren, Wesley C., additional, Werner, Scott J., additional, Bateson, Melissa, additional, Ball, Gregory F., additional, Buchanan, Katherine L., additional, Burt, David W., additional, Cardilini, Adam P. A., additional, Cassey, Phillip, additional, De Meyer, Tim, additional, George, Julia, additional, Meddle, Simone L., additional, Rowland, Hannah M., additional, Sherman, Craig D. H., additional, Sherwin, William B., additional, Vanden Berghe, Wim, additional, Rollins, Lee Ann, additional, and Clayton, David F., additional

Published
2023
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10. Transcript‐ and annotation‐guided genome assembly of the European starling

Author

Stuart, Katarina C., primary, Edwards, Richard J., additional, Cheng, Yuanyuan, additional, Warren, Wesley C., additional, Burt, David W., additional, Sherwin, William B., additional, Hofmeister, Natalie R., additional, Werner, Scott J., additional, Ball, Gregory F., additional, Bateson, Melissa, additional, Brandley, Matthew C., additional, Buchanan, Katherine L., additional, Cassey, Phillip, additional, Clayton, David F., additional, De Meyer, Tim, additional, Meddle, Simone L., additional, and Rollins, Lee A., additional

Published
2022
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11. Concurrent invasions by European starlings (Sturnus vulgaris) suggest selection on shared genomic regions even after genetic bottlenecks

Author

Hofmeister, Natalie R., primary, Stuart, Katarina, additional, Warren, Wesley C., additional, Werner, Scott J., additional, Bateson, Melissa, additional, Ball, Gregory F., additional, Buchanan, Katherine L., additional, Burt, David W., additional, Cardilini, Adam P.A., additional, Cassey, Phillip, additional, De Meyer, Tim, additional, George, Julia, additional, Meddle, Simone L., additional, Rowland, Hannah M., additional, Sherman, Craig D.H., additional, Sherwin, William, additional, Berghe, Wim Vanden, additional, Rollins, Lee Ann, additional, and Clayton, David F., additional

Published
2021
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12. 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

13. Transcript- and annotation-guided genome assembly of the European starling

Author

Stuart, Katarina C., primary, Edwards, Richard J., additional, Cheng, Yuanyuan, additional, Warren, Wesley C., additional, Burt, David W., additional, Sherwin, William B., additional, Hofmeister, Natalie R., additional, Werner, Scott J., additional, Ball, Gregory F., additional, Bateson, Melissa, additional, Brandley, Matthew C., additional, Buchanan, Katherine L., additional, Cassey, Phillip, additional, Clayton, David F., additional, De Meyer, Tim, additional, Meddle, Simone L., additional, and Rollins, Lee A., additional

Published
2021
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15. Additional file 2 of Song exposure regulates known and novel microRNAs in the zebra finch auditory forebrain

Author

Preethi H Gunaratne, Ya-Chi Lin, Benham, Ashley L, Drnevich, Jenny, Coarfa, Cristian, Jayantha B Tennakoon, Creighton, Chad J, Kim, Jong H, Milosavljevic, Aleksandar, Watson, Michael, Griffiths-Jones, Sam, and Clayton, David F

Subjects
animal structures, behavior and behavior mechanisms
Abstract

Additional file 2: Supplemental figures.doc. This one file contains all three supplemental figures. Figure S1 is a Venn diagram of numbers of miRNAs with significant differential expression in response to novel song in three Illumina experiments. Figure S2 shows a comparative mapping in other avian transcriptomes of tgu-mir-2954. Figure S3 demonstrates the song-specificity of the miRNA response, using TaqMan to compare the levels of specific miRNAs in animals from groups that heard song, matching song-enveloped noise, or silence. (DOC 698 KB)

Published
2020
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17. Additional file of Song exposure regulates known and novel microRNAs in the zebra finch auditory forebrain

Author

Preethi H Gunaratne, Ya-Chi Lin, Benham, Ashley L, Drnevich, Jenny, Coarfa, Cristian, Jayantha B Tennakoon, Creighton, Chad J, Kim, Jong H, Milosavljevic, Aleksandar, Watson, Michael, Griffiths-Jones, Sam, and Clayton, David F

Subjects
animal structures, nervous system, behavior and behavior mechanisms, reproductive and urinary physiology, psychological phenomena and processes
Abstract

Additional file of Song exposure regulates known and novel microRNAs in the zebra finch auditory forebrain

Published
2020
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19. Towards complete and error-free genome assemblies of all vertebrate species

Author

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

Published
2020
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26. Acute social isolation alters neurogenomic state insongbird forebrain.

Author

George, Julia M., Bell, Zachary W., Condliffe, Daniel, Dohrer, Kirstin, Abaurrea, Teresa, Spencer, Karen, Leitão, Albertine, Gahr, Manfred, Hurd, Paul J., and Clayton, David F.

Subjects
SOCIAL isolation, PROSENCEPHALON, ZEBRA finch, GENE expression, DNA methylation
Abstract

Prolonged social isolation has negative effects on brain and behavior in humans and other social organisms, but neural mechanisms leading to these effects are not understood. Here we tested the hypothesis that even brief periods of social isolation can alter gene expression and DNA methylation in higher cognitive centers of the brain, focusing on the auditory/associative forebrain of the highly social zebra finch. Using RNA sequencing, we first identified genes that individually increase or decrease expression after isolation and observed general repression of gene sets annotated for neurotrophin pathways and axonal guidance functions. We then pursued 4 genes of large effect size: EGR1 and BDNF (decreased by isolation) and FKBP5 and UTS2B (increased). By in situ hybridization, each gene responded in different cell subsets, arguing against a single cellular mechanism. To test whether effects were specific to the social component of the isolation experience, we compared gene expression in birds isolated either alone or with a single familiar partner. Partner inclusion ameliorated the effect of solo isolation on EGR1 and BDNF, but not on FKBP5 and UTS2B nor on circulating corticosterone. By bisulfite sequencing analysis of auditory forebrain DNA, isolation caused changes in methylation of a subset of differentially expressed genes, including BDNF. Thus, social isolation has rapid consequences on gene activity in a higher integrative center of the brain, triggering epigenetic mechanisms that may influence processing of ongoing experience. [ABSTRACT FROM AUTHOR]

Published
2020
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28. 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

29. 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

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

Author

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

Published
2016
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32. Functional genomic analysis and neuroanatomical localization of miR-2954, a song-responsive sex-linked microRNA in the zebra finch.

Author

Ya-Chi Lin, Balakrishnan, Christopher N., and Clayton, David F.

Subjects
RNA sequencing, ZEBRA finch, MOLECULAR genetics, FUNCTIONAL genomics, MICRORNA genetics, MITOGEN-activated protein kinases
Abstract

Natural experience can cause complex changes in gene expression in brain centers for cognition and perception, but the mechanisms that link perceptual experience and neurogenomic regulation are not understood. MicroRNAs (miRNAs or miRs) have the potential to regulate large gene expression networks, and a previous study showed that a natural perceptual stimulus (hearing the sound of birdsong in zebra finches) triggers rapid changes in expression of several miRs in the auditory forebrain. Here we evaluate the functional potential of one of these, miR-2954, which has been found so far only in birds and is encoded on the Z sex chromosome. Using fluorescence in situ hybridization and immunohistochemistry, we show that miR-2954 is present in subsets of cells in the sexually dimorphic brain regions involved in song production and perception, with notable enrichment in cell nuclei.We then probe its regulatory function by inhibiting its expression in a zebra finch cell line (G266) and measuring effects on endogenous gene expression using Illumina RNA sequencing (RNA-seq). Approximately 1000 different mRNAs change in expression by 1.5-fold or more (adjusted p < 0.01), with increases in some but not all of the targets that had been predicted by Targetscan. The population of RNAs that increase after miR-2954 inhibition is notably enriched for ones involved in the MAP Kinase (MAPK) pathway, whereas the decreasing population is dominated by genes involved in ribosomes and mitochondrial function. Since song stimulation itself triggers a decrease in miR-2954 expression followed by a delayed decrease in genes encoding ribosomal and mitochondrial functions, we suggest that miR-2954 may mediate some of the neurogenomic effects of song habituation. [ABSTRACT FROM AUTHOR]

Published
2014
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33. Towards complete and error-free genome assemblies of all vertebrate species

Author

Richard Hall, Tandy Warnow, Tanya M. Lama, Oliver A. Ryder, David Haussler, Matthew T. Biegler, Klaus-Peter Koepfli, Ivo Gut, Paul Flicek, Mark Chaisson, James Torrance, Guojie Zhang, Andrew J. Crawford, Federica Di Palma, Michael Hiller, Jennifer A. Marshall Graves, Sadye Paez, Sarah E. London, Mark Wilkinson, Kateryna D. Makova, Byung June Ko, Jimin George, Farooq O. Al-Ajli, Emma C. Teeling, George F. Turner, Robert H. S. Kraus, Sonja C. Vernes, Zev N. Kronenberg, Michelle Smith, Jonas Korlach, Daryl Eason, Jonathan Wood, Simona Secomandi, Claudio V. Mello, Arkarachai Fungtammasan, Arang Rhie, Tomas Marques-Bonet, Benedict Paten, Ekaterina Osipova, Richard Durbin, M. Thomas P. Gilbert, Beth Shapiro, Ivan Sović, Bruce C. Robertson, Richard E. Green, Eugene W. Myers, Leanne Haggerty, Sergey Koren, Martin Pippel, Bettina Haase, Patrick Masterson, Jay Ghurye, Maria Simbirsky, Samantha R. Friedrich, Chul Hee Lee, Luis R Nassar, Lindsey J. Cantin, Kerstin Howe, Erich D. Jarvis, Marlys L. Houck, Jason T. Howard, Jacquelyn Mountcastle, Mark Mooney, Paolo Franchini, Giulio Formenti, Siddarth Selvaraj, Robel E. Dagnew, Brett T. Hannigan, Brian P. Walenz, Alan Tracey, Heebal Kim, Constantina Theofanopoulou, Nicholas H. Putnam, Karen Clark, Iliana Bista, H. William Detrich, Dengfeng Guan, David Iorns, Andrew Digby, Trevor Pesout, Zemin Ning, Gregory Gedman, Woori Kwak, Maximilian Wagner, Joanna Collins, Harris A. Lewin, Hannes Svardal, Milan Malinsky, Byrappa Venkatesh, Françoise Thibaud-Nissen, Joana Damas, Andreas F. Kautt, Olivier Fedrigo, Christopher Dunn, William Chow, Warren E. Johnson, Yang Zhou, Adam M. Phillippy, Taylor Edwards, Paul Medvedev, Peter V. Lovell, Joyce V. Lee, Sylke Winkler, Stephen J. O'Brien, Wesley C. Warren, Alex Hastie, Marcela Uliano-Silva, Kevin L. Howe, Sarah B. Kingan, Fergal J. Martin, Christopher N. Balakrishnan, David F. Clayton, Ying Sims, Robert W. Murphy, Axel Meyer, Dave W Burt, Shane A. McCarthy, Sarah Pelan, Erik Garrison, Mark Diekhans, Frank Grützner, Gavin J. P. Naylor, Robert S. Harris, Hiram Clawson, Jinna Hoffman, Ann C Misuraca, J. H. Kim, University of St Andrews. School of Biology, University of St Andrews. St Andrews Bioinformatics Unit, Rhie, Arang [0000-0002-9809-8127], Fedrigo, Olivier [0000-0002-6450-7551], Formenti, Giulio [0000-0002-7554-5991], Koren, Sergey [0000-0002-1472-8962], Uliano-Silva, Marcela [0000-0001-6723-4715], Thibaud-Nissen, Francoise [0000-0003-4957-7807], Mountcastle, Jacquelyn [0000-0003-1078-4905], Winkler, Sylke [0000-0002-0915-3316], Vernes, Sonja C. [0000-0003-0305-4584], Grutzner, Frank [0000-0002-3088-7314], Balakrishnan, Christopher N. [0000-0002-0788-0659], Burt, Dave [0000-0002-9991-1028], George, Julia M. [0000-0001-6194-6914], Digby, Andrew [0000-0002-1870-8811], Robertson, Bruce [0000-0002-5348-2731], Edwards, Taylor [0000-0002-7235-6175], Meyer, Axel [0000-0002-0888-8193], Kautt, Andreas F. [0000-0001-7792-0735], Franchini, Paolo [0000-0002-8184-1463], Detrich, H. William, III [0000-0002-0783-4505], Pippel, Martin [0000-0002-8134-5929], Malinsky, Milan [0000-0002-1462-6317], Kingan, Sarah B. [0000-0002-4900-0189], Hall, Richard [0000-0001-6490-8227], Dunn, Christopher [0000-0002-0601-3254], Lee, Joyce [0000-0002-3492-1102], Putnam, Nicholas H. [0000-0002-1315-782X], Gut, Ivo [0000-0001-7219-632X], Tracey, Alan [0000-0002-4805-9058], Guan, Dengfeng [0000-0002-6376-3940], London, Sarah E. [0000-0002-7839-2644], Clayton, David F. [0000-0002-6395-3488], Mello, Claudio V. [0000-0002-9826-8421], Friedrich, Samantha R. [0000-0003-0570-6080], Osipova, Ekaterina [0000-0002-6769-7223], Al-Ajli, Farooq O. [0000-0002-4692-7106], Secomandi, Simona [0000-0001-8597-6034], Kim, Heebal [0000-0003-3064-1303], Theofanopoulou, Constantina [0000-0003-2014-7563], Zhou, Yang [0000-0003-1247-5049], Martin, Fergal [0000-0002-1672-050X], Flicek, Paul [0000-0002-3897-7955], Walenz, Brian P. [0000-0001-8431-1428], Diekhans, Mark [0000-0002-0430-0989], Paten, Benedict [0000-0001-8863-3539], Crawford, Andrew J. [0000-0003-3153-6898], Gilbert, M. Thomas P. [0000-0002-5805-7195], Zhang, Guojie [0000-0001-6860-1521], Venkatesh, Byrappa [0000-0003-3620-0277], Shapiro, Beth [0000-0002-2733-7776], Johnson, Warren E. [0000-0002-5954-186X], Marques-Bonet, Tomas [0000-0002-5597-3075], Teeling, Emma C. [0000-0002-3309-1346], Ryder, Oliver A. [0000-0003-2427-763X], Haussler, David [0000-0003-1533-4575], Korlach, Jonas [0000-0003-3047-4250], Lewin, Harris A. [0000-0002-1043-7287], Howe, Kerstin [0000-0003-2237-513X], Myers, Eugene W. [0000-0002-6580-7839], Durbin, Richard [0000-0002-9130-1006], Phillippy, Adam M. [0000-0003-2983-8934], Jarvis, Erich D. [0000-0001-8931-5049], Apollo - University of Cambridge Repository, 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, Vernes, Sonja C [0000-0003-0305-4584], Balakrishnan, Christopher N [0000-0002-0788-0659], George, Julia M [0000-0001-6194-6914], Kautt, Andreas F [0000-0001-7792-0735], Detrich, H William [0000-0002-0783-4505], Kingan, Sarah B [0000-0002-4900-0189], Putnam, Nicholas H [0000-0002-1315-782X], London, Sarah E [0000-0002-7839-2644], Clayton, David F [0000-0002-6395-3488], Mello, Claudio V [0000-0002-9826-8421], Friedrich, Samantha R [0000-0003-0570-6080], Al-Ajli, Farooq O [0000-0002-4692-7106], Walenz, Brian P [0000-0001-8431-1428], Crawford, Andrew J [0000-0003-3153-6898], Gilbert, M Thomas P [0000-0002-5805-7195], Johnson, Warren E [0000-0002-5954-186X], Teeling, Emma C [0000-0002-3309-1346], Ryder, Oliver A [0000-0003-2427-763X], Lewin, Harris A [0000-0002-1043-7287], Myers, Eugene W [0000-0002-6580-7839], Phillippy, Adam M [0000-0003-2983-8934], and Jarvis, Erich D [0000-0001-8931-5049]

Subjects
QH301 Biology, Genome, 0302 clinical medicine, Genome Size, Vertebrats, Uncategorized, 64, 0303 health sciences, Sex Chromosomes, Multidisciplinary, High-Throughput Nucleotide Sequencing, Genomics, Mitochondrial, Vertebrates, Identification (biology), Engineering sciences. Technology, Sequence Analysis, Neuroinformatics, 45/23, QH426 Genetics, Biology, Article, Evolutionary genetics, 38, Birds, QH301, 03 medical and health sciences, Molecular evolution, ddc:570, Genome assembly algorithms, Animals, 631/181/735, 14. Life underwater, Genomes, QH426, Gene, Gene Library, Genome, Mitochondrial, Haplotypes, Molecular Sequence Annotation, Sequence Alignment, Sequence Analysis, DNA, 030304 developmental biology, 45/91, 631/61/212/2302, 45, Human evolutionary genetics, Haplotype, DAS, DNA, Research data, 706/648/697, 631/181/2474, Evolutionary biology, Genètica, 030217 neurology & neurosurgery, Reference genome
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., We thank them for their permission to publish. A.R., S.K., B.P.W. and A.M.P. were supported by the Intramural Research Program of the NHGRI, NIH (1ZIAHG200398). A.R. was also supported by the Korea Health Technology R&D Project through KHIDI, funded by the Ministry of Health & Welfare, Republic of Korea (HI17C2098). S.A.M., I.B. and R.D. were supported by Wellcome Trust grant WT207492; W.C., M. Smith, Z.N., Y.S., J.C., S. Pelan, J.T., A.T., J.W. and Kerstin Howe by WT206194; L.H., F.M., Kevin Howe and P. Flicek by WT108749/Z/15/Z, WT218328/B/19/Z and the European Molecular Biology Laboratory. O.F. and E.D.J. were supported by Howard Hughes Medical Institute and Rockefeller University start-up funds for this project. J.D. and H.A.L. were supported by the Robert and Rosabel Osborne Endowment. M.U.-S. received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement (750747). F.T.-N., J. Hoffman, P. Masterson and K.C. were supported by the Intramural Research Program of the NLM, NIH. C.L., B.J.K., J. Kim and H.K. were supported by the Marine Biotechnology Program of KIMST, funded by the Ministry of Ocean and Fisheries, Republic of Korea (20180430). M.C. was supported by Sloan Research Fellowship (FG-2020-12932). S.C.V. was funded by a Max Planck Research Group award from the Max Planck Society, and a Human Frontiers Science Program (HFSP) Research grant (RGP0058/2016). T.M.L., W.E.J. and the Canada lynx genome were funded by the Maine Department of Inland Fisheries & Wildlife (F11AF01099), including when W.E.J. held a National Research Council Research Associateship Award at the Walter Reed Army Institute of Research (WRAIR). C.B. was supported by the NSF (1457541 and 1456612). D.B. was funded by The University of Queensland (HFSP - RGP0030/2015). D.I. was supported by Science Exchange Inc. (Palo Alto, CA). H.W.D. was supported by NSF grants (OPP-0132032 ICEFISH 2004 Cruise, PLR-1444167 and OPP-1955368) and the Marine Science Center at Northeastern University (416). G.J.P.N. and the thorny skate genome were funded by Lenfest Ocean Program (30884). M.P. was funded by the German Federal Ministry of Education and Research (01IS18026C). M. Malinsky was supported by an EMBO fellowship (ALTF 456-2016). The following authors’ contributions were supported by the NIH: S. Selvaraj (R44HG008118); C.V.M., S.R.F., P.V.L. (R21 DC014432/DC/NIDCD); K.D.M. (R01GM130691); H.C. (5U41HG002371-19); M.D. (U41HG007234); and B.P. (R01HG010485). D.G. was supported by the National Key Research and Development Program of China (2017YFC1201201, 2018YFC0910504 and 2017YFC0907503). F.O.A. was supported by Al-Gannas Qatari Society and The Cultural Village Foundation-Katara, Doha, State of Qatar and Monash University Malaysia. C.T. was supported by The Rockefeller University. M. Hiller was supported by the LOEWE-Centre for Translational Biodiversity Genomics (TBG) funded by the Hessen State Ministry of Higher Education, Research and the Arts (HMWK). H.C. was supported by the NHGRI (5U41HG002371-19). R.H.S.K. was funded by the Max Planck Society with computational resources at the bwUniCluster and BinAC funded by the Ministry of Science, Research and the Arts Baden-Württemberg and the Universities of the State of Baden-Württemberg, Germany (bwHPC-C5). B.V. was supported by the Biomedical Research Council of A*STAR, Singapore. T.M.-B. was funded by the European Research Council under the European Union’s Horizon 2020 research and innovation programme (864203), MINECO/FEDER, UE (BFU2017-86471-P), Unidad de Excelencia María de Maeztu, AEI (CEX2018-000792-M), a Howard Hughes International Early Career award, Obra Social “La Caixa” and Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880). E.C.T. was supported by the European Research Council (ERC-2012-StG311000) and an Irish Research Council Laureate Award. M.T.P.G. was supported by an ERC Consolidator Award 681396-Extinction Genomics, and a Danish National Research Foundation Center Grant (DNRF143). T.W. was supported by the NSF (1458652). J. M. Graves was supported by the Australian Research Council (CEO561477). E.W.M. was partially supported by the German Federal Ministry of Education and Research (01IS18026C). Complementary sequencing support for the Anna’s hummingbird and several genomes was provided by Pacific Biosciences, Bionano Genomics, Dovetail Genomics, Arima Genomics, Phase Genomics, 10X Genomics, NRGene, Oxford Nanopore Technologies, Illumina, and DNAnexus. All other sequencing and assembly were conducted at the Rockefeller University, Sanger Institute, and Max Planck Institute Dresden genome labs. Part of this work used the computational resources of the NIH HPC Biowulf cluster (https://hpc.nih.gov). We acknowledge funding from the Wellcome Trust (108749/Z/15/Z) and the European Molecular Biology Laboratory., With funding from the Spanish government through the "Severo Ochoa Centre of Excellence" accreditation (CEX2018-000792-M).

Published
2021

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