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Molecular early burst associated with the diversification of birds at the K–Pg boundary

View ORCID ProfileJacob S. Berv, View ORCID ProfileSonal Singhal, View ORCID ProfileDaniel J. Field, View ORCID ProfileNathanael Walker-Hale, View ORCID ProfileSean W. McHugh, View ORCID ProfileJ. Ryan Shipley, View ORCID ProfileEliot T. Miller, View ORCID ProfileRebecca T. Kimball, View ORCID ProfileEdward L. Braun, View ORCID ProfileAlex Dornburg, View ORCID ProfileC. Tomomi Parins-Fukuchi, View ORCID ProfileRichard O. Prum, View ORCID ProfileBenjamin M. Winger, View ORCID ProfileMatt Friedman, View ORCID ProfileStephen A. Smith
doi: https://doi.org/10.1101/2022.10.21.513146
Jacob S. Berv
1Department of Ecology and Evolutionary Biology, 1105 North University Avenue, Biological Sciences Building, University of Michigan, Ann Arbor, Michigan, 48109-1085, USA
2University of Michigan Museum of Paleontology, 1105 North University Avenue, Biological Sciences Building, University of Michigan, Ann Arbor, Michigan, 48109-1085, USA
3University of Michigan Museum of Zoology, 1105 North University Avenue, Biological Sciences Building, University of Michigan, Ann Arbor, Michigan, 48109-1085, USA
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  • For correspondence: jberv@umich.edu jacob.berv@gmail.com
Sonal Singhal
4Department of Biology, California State University, Dominguez Hills, Carson, California 90747, USA
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Daniel J. Field
5Department of Earth Sciences, Downing Street, University of Cambridge, Cambridge CB2 3EQ, UK
6Museum of Zoology, Downing Street, University of Cambridge, Cambridge CB2 3EJ, UK
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Nathanael Walker-Hale
7Department of Plant Sciences, Downing Street, University of Cambridge, Cambridge, CB2 3EA, UK
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Sean W. McHugh
8Department of Evolution, Ecology, and Population Biology, Washington University in St Louis, St Louis, Missouri, USA
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J. Ryan Shipley
9Department of Forest Dynamics Swiss Federal Institute for Forest, Snow, and Landscape Research WSL Zürcherstrasse 111 8903 Birmensdorf, Switzerland
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Eliot T. Miller
10Macaulay Library, Cornell Lab of Ornithology, Ithaca, New York, 14850, USA
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Rebecca T. Kimball
11Department of Biology, University of Florida, Gainesville, Florida 32611, USA
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Edward L. Braun
11Department of Biology, University of Florida, Gainesville, Florida 32611, USA
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Alex Dornburg
12Department of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte, North Carolina, USA
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C. Tomomi Parins-Fukuchi
13Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada, M5S 3B2
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Richard O. Prum
14Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, 06520, USA
15Peabody Museum of Natural History, Yale University, New Haven, Connecticut, 06520, USA
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Benjamin M. Winger
1Department of Ecology and Evolutionary Biology, 1105 North University Avenue, Biological Sciences Building, University of Michigan, Ann Arbor, Michigan, 48109-1085, USA
3University of Michigan Museum of Zoology, 1105 North University Avenue, Biological Sciences Building, University of Michigan, Ann Arbor, Michigan, 48109-1085, USA
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Matt Friedman
2University of Michigan Museum of Paleontology, 1105 North University Avenue, Biological Sciences Building, University of Michigan, Ann Arbor, Michigan, 48109-1085, USA
16Department of Earth and Environmental Sciences, 1100 North University Avenue, University of Michigan, Ann Arbor, Michigan, 48109-1085, USA
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Stephen A. Smith
1Department of Ecology and Evolutionary Biology, 1105 North University Avenue, Biological Sciences Building, University of Michigan, Ann Arbor, Michigan, 48109-1085, USA
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Abstract

Complex patterns of genome and life-history evolution associated with the end-Cretaceous (K– Pg) mass extinction event limit our understanding of the early evolutionary history of crown group birds [1-9]. Here, we assess molecular heterogeneity across living birds using a technique enabling inferred sequence substitution models to transition across the history of a clade [10]. Our approach identifies distinct and contrasting regimes of molecular evolution across exons, introns, untranslated regions, and mitochondrial genomes. Up to fifteen shifts in the mode of avian molecular evolution map to rapidly diversifying clades near the Cretaceous-Palaeogene boundary, demonstrating a burst of genomic disparity early in the evolutionary history of crown birds [11-13]. Using simulation and machine learning techniques, we show that shifts in developmental mode [14] or adult body mass [4] best explain transitions in the mode of nucleotide substitution. These patterns are related, in turn, to macroevolutionary shifts in the allometric scaling relationship between basal metabolic rate and body mass [15, 16]. In agreement with theoretical predictions, this scaling relationship appears to have weakened across the end-Cretaceous transition. Overall, our study provides evidence that the Chicxulub bolide impact [17] triggered integrated patterns of evolution across avian genomes, physiology, and life history that structured the evolutionary potential of modern birds.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The manuscript has been updated to include a brief description of the Janus algorithm (supplementary appendix). Several minor corrections have been incorporated.

  • https://github.com/jakeberv/avian_molecular_shifts

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Molecular early burst associated with the diversification of birds at the K–Pg boundary
Jacob S. Berv, Sonal Singhal, Daniel J. Field, Nathanael Walker-Hale, Sean W. McHugh, J. Ryan Shipley, Eliot T. Miller, Rebecca T. Kimball, Edward L. Braun, Alex Dornburg, C. Tomomi Parins-Fukuchi, Richard O. Prum, Benjamin M. Winger, Matt Friedman, Stephen A. Smith
bioRxiv 2022.10.21.513146; doi: https://doi.org/10.1101/2022.10.21.513146
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Molecular early burst associated with the diversification of birds at the K–Pg boundary
Jacob S. Berv, Sonal Singhal, Daniel J. Field, Nathanael Walker-Hale, Sean W. McHugh, J. Ryan Shipley, Eliot T. Miller, Rebecca T. Kimball, Edward L. Braun, Alex Dornburg, C. Tomomi Parins-Fukuchi, Richard O. Prum, Benjamin M. Winger, Matt Friedman, Stephen A. Smith
bioRxiv 2022.10.21.513146; doi: https://doi.org/10.1101/2022.10.21.513146

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