Complexity of avian evolution revealed by family-level genomes

Stiller J 1 , Feng S 2 , Chowdhury AA 3 , Rivas-González I 4 , Duchêne DA 5 , Fang Q 6 Show all authors , Deng Y 6 , Kozlov A 7 , Stamatakis A 7 , Claramunt S 8 , Nguyen JMT 9 , Ho SYW 3 , Faircloth BC 10 , Haag J 7 , Houde P 11 , Cracraft J 12 , Balaban M 13 , Mai U 14 , Chen G 6 , Gao R 6 , Zhou C 6 , Xie Y 2 , Huang Z 2 , Cao Z 15 , Yan Z 15 , Ogilvie HA 15 , Nakhleh L 15 , Lindow B 16 , Morel B 7 , Fjeldså J 16 , Hosner PA 16 , da Fonseca RR 17 , Petersen B 5 , Tobias JA 18 , Székely T 19 , Kennedy JD 20 , Reeve AH 16 , Liker A 21 , Stervander M 22 , Antunes A 23 , Tietze DT 24 , Bertelsen M 25 , Lei F 26 , Rahbek C 17 , Graves GR 20 , Schierup MH 4 , Warnow T 27 , Braun EL 28 , Gilbert MTP 5 , Jarvis ED 29 , Mirarab S 30 , Zhang G 31

Affiliations 

  • 1 Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark. josefin.stiller@bio.ku.dk
  • 2 Center for Evolutionary & Organismal Biology, & Women's Hospital, Zhejiang University School of Medicine, Hangzhou, China
  • 3 School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia
  • 4 Bioinformatics Research Centre, Aarhus University, Aarhus, Denmark
  • 5 Center for Evolutionary Hologenomics, The Globe Institute, University of Copenhagen, Copenhagen, Denmark
  • 6 BGI-Shenzhen, Beishan Industrial Zone, Shenzhen, China
  • 7 Computational Molecular Evolution Group, Heidelberg Institute for Theoretical Studies, Heidelberg, Germany
  • 8 Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada
  • 9 College of Science and Engineering, Flinders University, Bedford Park, South Australia, Australia
  • 10 Department of Biological Sciences and Museum of Natural Science, Louisiana State University, Baton Rouge, LA, USA
  • 11 Department of Biology, New Mexico State University, Las Cruces, NM, USA
  • 12 Department of Ornithology, American Museum of Natural History, New York, NY, USA
  • 13 Bioinformatics and Systems Biology Graduate Program, University of California San Diego, La Jolla, CA, USA
  • 14 Computer Science and Engineering, University of California San Diego, La Jolla, CA, USA
  • 15 Department of Computer Science, Rice University, Houston, TX, USA
  • 16 Natural History Museum Denmark, University of Copenhagen, Copenhagen, Denmark
  • 17 Center for Global Mountain Biodiversity, Globe Institute, University of Copenhagen, Copenhagen, Denmark
  • 18 Department of Life Sciences, Imperial College London, Silwood Park, Ascot, UK
  • 19 Milner Centre for Evolution, University of Bath, Bath, UK
  • 20 Center for Macroecology, Evolution, and Climate, The Globe Institute, University of Copenhagen, Copenhagen, Denmark
  • 21 HUN-REN-PE Evolutionary Ecology Research Group, University of Pannonia, Veszprém, Hungary
  • 22 Bird Group, Natural History Museum, Akeman St, Tring, Hertfordshire, United Kingdom
  • 23 CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Porto, Portugal
  • 24 NABU, Berlin, Germany
  • 25 Centre for Zoo and Wild Animal Health, Copenhagen Zoo, Frederiksberg, Denmark
  • 26 Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
  • 27 University of Illinois Urbana-Champaign, Champaign, IL, USA
  • 28 Department of Biology, University of Florida, Gainesville, FL, USA
  • 29 Vertebrate Genome Lab, The Rockefeller University, New York, NY, USA
  • 30 University of California, San Diego, San Diego, CA, USA. smirarabbaygi@ucsd.edu
  • 31 Center for Evolutionary & Organismal Biology, & Women's Hospital, Zhejiang University School of Medicine, Hangzhou, China. guojiezhang@zju.edu.cn
Nature, 2024 Apr 01.
PMID: 38560995 DOI: 10.1038/s41586-024-07323-1

Abstract

Despite tremendous efforts in the past decades, relationships among main avian lineages remain heavily debated without a clear resolution. Discrepancies have been attributed to diversity of species sampled, phylogenetic method, and the choice of genomic regions 1-3. Here, we address these issues by analyzing genomes of 363 bird species 4 (218 taxonomic families, 92% of total). Using intergenic regions and coalescent methods, we present a well-supported tree but also a remarkable degree of discordance. The tree confirms that Neoaves experienced rapid radiation at or near the Cretaceous-Paleogene (K-Pg) boundary. Sufficient loci rather than extensive taxon sampling were more effective in resolving difficult nodes. Remaining recalcitrant nodes involve species that challenge modeling due to extreme GC content, variable substitution rates, incomplete lineage sorting, or complex evolutionary events such as ancient hybridization. Assessment of the impacts of different genomic partitions showed high heterogeneity across the genome. We discovered sharp increases in effective population size, substitution rates, and relative brain size following the K-Pg extinction event, supporting the hypothesis that emerging ecological opportunities catalyzed the diversification of modern birds. The resulting phylogenetic estimate offers novel insights into the rapid radiation of modern birds and provides a taxon-rich backbone tree for future comparative studies.

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

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