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Dense sampling of bird diversity increases power of comparative genomics

Feng S 1 , Stiller J 2 , Deng Y 1 , Armstrong J 3 , Fang Q 1 , Reeve AH 4 Show all authors , Xie D 1 , Chen G 1 , Guo C 1 , Faircloth BC 5 , Petersen B 6 , Wang Z 1 , Zhou Q 7 , Diekhans M 3 , Chen W 1 , Andreu-Sánchez S 2 , Margaryan A 8 , Howard JT 9 , Parent C 10 , Pacheco G 8 , Sinding MS 8 , Puetz L 8 , Cavill E 8 , Ribeiro ÂM 4 , Eckhart L 11 , Fjeldså J 4 , Hosner PA 4 , Brumfield RT 5 , Christidis L 12 , Bertelsen MF 13 , Sicheritz-Ponten T 6 , Tietze DT 14 , Robertson BC 15 , Song G 16 , Borgia G 17 , Claramunt S 18 , Lovette IJ 19 , Cowen SJ 20 , Njoroge P 21 , Dumbacher JP 22 , Ryder OA 23 , Fuchs J 24 , Bunce M 25 , Burt DW 26 , Cracraft J 27 , Meng G 1 , Hackett SJ 28 , Ryan PG 29 , Jønsson KA 4 , Jamieson IG 15 , da Fonseca RR 30 , Braun EL 31 , Houde P 32 , Mirarab S 33 , Suh A 34 , Hansson B 35 , Ponnikas S 35 , Sigeman H 35 , Stervander M 35 , Frandsen PB 36 , van der Zwan H 37 , van der Sluis R 37 , Visser C 38 , Balakrishnan CN 39 , Clark AG 40 , Fitzpatrick JW 19 , Bowman R 41 , Chen N 42 , Cloutier A 43 , Sackton TB 44 , Edwards SV 43 , Foote DJ 39 , Shakya SB 5 , Sheldon FH 5 , Vignal A 45 , Soares AER 46 , Shapiro B 47 , González-Solís J 48 , Ferrer-Obiol J 48 , Rozas J 48 , Riutort M 48 , Tigano A 49 , Friesen V 50 , Dalén L 51 , Urrutia AO 52 , Székely T 52 , Liu Y 53 , Campana MG 54 , Corvelo A 55 , Fleischer RC 54 , Rutherford KM 56 , Gemmell NJ 56 , Dussex N 51 , Mouritsen H 57 , Thiele N 57 , Delmore K 58 , Liedvogel M 59 , Franke A 60 , Hoeppner MP 60 , Krone O 61 , Fudickar AM 62 , Milá B 63 , Ketterson ED 64 , Fidler AE 65 , Friis G 66 , Parody-Merino ÁM 67 , Battley PF 67 , Cox MP 68 , Lima NCB 46 , Prosdocimi F 69 , Parchman TL 70 , Schlinger BA 71 , Loiselle BA 72 , Blake JG 72 , Lim HC 54 , Day LB 73 , Fuxjager MJ 74 , Baldwin MW 75 , Braun MJ 76 , Wirthlin M 77 , Dikow RB 78 , Ryder TB 79 , Camenisch G 80 , Keller LF 80 , DaCosta JM 81 , Hauber ME 82 , Louder MIM 39 , Witt CC 83 , McGuire JA 84 , Mudge J 85 , Megna LC 86 , Carling MD 86 , Wang B 87 , Taylor SA 88 , Del-Rio G 89 , Aleixo A 90 , Vasconcelos ATR 46 , Mello CV 91 , Weir JT 18 , Haussler D 3 , Li Q 1 , Yang H 92 , Wang J 92 , Lei F 16 , Rahbek C 30 , Gilbert MTP 8 , Graves GR 30 , Jarvis ED 10 , Paten B 93 , Zhang G 94

Affiliations 

  • 1 China National GeneBank, BGI-Shenzhen, Shenzhen, China
  • 2 Villum Centre for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark
  • 3 UC Santa Cruz Genomics Institute, UC Santa Cruz, Santa Cruz, CA, USA
  • 4 Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
  • 5 Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA
  • 6 Centre of Excellence for Omics-Driven Computational Biodiscovery (COMBio), Faculty of Applied Sciences, AIMST University, Kedah, Malaysia
  • 7 MOE Laboratory of Biosystems Homeostasis and Protection, Life Sciences Institute, Zhejiang University, Hangzhou, China
  • 8 Section for Evolutionary Genomics, The GLOBE Institute, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
  • 9 Novogene, Durham, NC, USA
  • 10 Duke University Medical Center, Durham, NC, USA
  • 11 Department of Dermatology, Medical University of Vienna, Vienna, Austria
  • 12 Southern Cross University, Coffs Harbour, New South Wales, Australia
  • 13 Centre for Zoo and Wild Animal Health, Copenhagen Zoo, Frederiksberg, Denmark
  • 14 Center of Natural History, Universität Hamburg, Hamburg, Germany
  • 15 Department of Zoology, University of Otago, Dunedin, New Zealand
  • 16 Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
  • 17 Department of Biology, University of Maryland, College Park, MD, USA
  • 18 Department of Natural History, Royal Ontario Museum, Toronto, Ontario, Canada
  • 19 Cornell Lab of Ornithology, Cornell University, Ithaca, NY, USA
  • 20 Biodiversity and Conservation Science, Department of Biodiversity Conservation and Attractions, Perth, Western Australia, Australia
  • 21 Ornithology Section, Zoology Department, National Museums of Kenya, Nairobi, Kenya
  • 22 Ornithology and Mammalogy, California Academy of Sciences, San Francisco, CA, USA
  • 23 San Diego Zoo Institute for Conservation Research, Escondido, CA, USA
  • 24 Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Paris, France
  • 25 Trace and Environmental DNA (TrEnD) Laboratory, School of Molecular and Life Sciences, Curtin University, Western Australia, Perth, Australia
  • 26 UQ Genomics, University of Queensland, Brisbane, Queensland, Australia
  • 27 Department of Ornithology, American Museum of Natural History, New York, NY, USA
  • 28 Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA
  • 29 FitzPatrick Institute of African Ornithology, University of Cape Town, Cape Town, South Africa
  • 30 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, Copenhagen, Denmark
  • 31 Department of Biology, University of Florida, Gainesville, FL, USA
  • 32 Department of Biology, New Mexico State University, Las Cruces, NM, USA
  • 33 Department of Electrical and Computer Engineering, University of California San Diego, La Jolla, CA, USA
  • 34 Department of Ecology and Genetics - Evolutionary Biology, Evolutionary Biology Centre (EBC), Science for Life Laboratory, Uppsala University, Uppsala, Sweden
  • 35 Department of Biology, Lund University, Lund, Sweden
  • 36 Department of Plant and Wildlife Sciences, Brigham Young University, Provo, UT, USA
  • 37 Focus Area for Human Metabolomics, North-West University, Potchefstroom, South Africa
  • 38 Department of Animal Sciences, University of Pretoria, Pretoria, South Africa
  • 39 Department of Biology, East Carolina University, Greenville, NC, USA
  • 40 Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, USA
  • 41 Avian Ecology Program, Archbold Biological Station, Venus, FL, USA
  • 42 Department of Biology, University of Rochester, Rochester, NY, USA
  • 43 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA
  • 44 Informatics Group, Harvard University, Cambridge, MA, USA
  • 45 GenPhySE, INRA, INPT, INP-ENVT, Université de Toulouse, Castanet-Tolosan, France
  • 46 Laboratório Nacional de Computação Científica, Petrópolis, Brazil
  • 47 Department of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA, USA
  • 48 Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
  • 49 Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, NH, USA
  • 50 Department of Biology, Queen's University, Kingston, Ontario, Canada
  • 51 Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden
  • 52 Milner Centre for Evolution, University of Bath, Bath, UK
  • 53 State Key Laboratory of Biocontrol, School of Ecology, Sun Yat-sen University, Guangzhou, China
  • 54 Center for Conservation Genomics, Smithsonian Conservation Biology Institute, Smithsonian Institution, Washington, DC, USA
  • 55 New York Genome Center, New York, NY, USA
  • 56 Department of Anatomy, University of Otago, Dunedin, New Zealand
  • 57 AG Neurosensory Sciences, Institut für Biologie und Umweltwissenschaften, University of Oldenburg, Oldenburg, Germany
  • 58 Biology Department, Texas A&M University, College Station, TX, USA
  • 59 MPRG Behavioural Genomics, Max Planck Institute for Evolutionary Biology, Plön, Germany
  • 60 Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, Kiel, Germany
  • 61 Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
  • 62 Environmental Resilience Institute, Indiana University, Bloomington, IN, USA
  • 63 National Museum of Natural Sciences, Spanish National Research Council (CSIC), Madrid, Spain
  • 64 Department of Biology, Indiana University, Bloomington, IN, USA
  • 65 Institute of Marine Science, University of Auckland, Auckland, New Zealand
  • 66 Center for Genomics and Systems Biology, Department of Biology, New York University - Abu Dhabi, Abu Dhabi, UAE
  • 67 Wildlife and Ecology Group, Massey University, Palmerston North, New Zealand
  • 68 School of Fundamental Sciences, Massey University, Palmerston North, New Zealand
  • 69 Laboratório de Genômica e Biodiversidade, Instituto de Bioquímica Médica Leopoldo de Meis, Rio de Janeiro, Brazil
  • 70 Department of Biology, University of Nevada Reno, Reno, NV, USA
  • 71 Department of Integrative Biology and Physiology, UCLA, Los Angeles, CA, USA
  • 72 Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL, USA
  • 73 Department of Biology and Neuroscience Minor, University of Mississippi, University, MS, USA
  • 74 Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA
  • 75 Max Planck Institute for Ornithology, Seewiesen, Germany
  • 76 Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA
  • 77 Computational Biology Department, Carnegie Mellon University, Pittsburgh, PA, USA
  • 78 Data Science Lab, Office of the Chief Information Officer, Smithsonian Institution, Washington, DC, USA
  • 79 Migratory Bird Center, Smithsonian National Zoological Park and Conservation Biology Institute, Washington, DC, USA
  • 80 Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland
  • 81 Biology Department, Boston College, Chestnut Hill, MA, USA
  • 82 Department of Evolution, Ecology, and Behavior, School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
  • 83 Museum of Southwestern Biology, Department of Biology, University of New Mexico, Albuquerque, NM, USA
  • 84 Museum of Vertebrate Zoology, Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, USA
  • 85 National Center for Genome Resources, Santa Fe, NM, USA
  • 86 Department of Zoology and Physiology, University of Wyoming, Laramie, WY, USA
  • 87 School of BioSciences, The University of Melbourne, Melbourne, Victoria, Australia
  • 88 Department of Ecology and Evolutionary Biology, University of Colorado Boulder, Boulder, CO, USA
  • 89 Museum of Natural Science, Louisiana State University, Baton Rouge, LA, USA
  • 90 Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland
  • 91 Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR, USA
  • 92 BGI-Shenzhen, Shenzhen, China
  • 93 UC Santa Cruz Genomics Institute, UC Santa Cruz, Santa Cruz, CA, USA. bpaten@ucsc.edu
  • 94 China National GeneBank, BGI-Shenzhen, Shenzhen, China. guojie.zhang@bio.ku.dk
Nature, 2020 11;587(7833):252-257.
PMID: 33177665 DOI: 10.1038/s41586-020-2873-9

Abstract

Whole-genome sequencing projects are increasingly populating the tree of life and characterizing biodiversity1-4. Sparse taxon sampling has previously been proposed to confound phylogenetic inference5, and captures only a fraction of the genomic diversity. Here we report a substantial step towards the dense representation of avian phylogenetic and molecular diversity, by analysing 363 genomes from 92.4% of bird families-including 267 newly sequenced genomes produced for phase II of the Bird 10,000 Genomes (B10K) Project. We use this comparative genome dataset in combination with a pipeline that leverages a reference-free whole-genome alignment to identify orthologous regions in greater numbers than has previously been possible and to recognize genomic novelties in particular bird lineages. The densely sampled alignment provides a single-base-pair map of selection, has more than doubled the fraction of bases that are confidently predicted to be under conservation and reveals extensive patterns of weak selection in predominantly non-coding DNA. Our results demonstrate that increasing the diversity of genomes used in comparative studies can reveal more shared and lineage-specific variation, and improve the investigation of genomic characteristics. We anticipate that this genomic resource will offer new perspectives on evolutionary processes in cross-species comparative analyses and assist in efforts to conserve species.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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