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Six new reference-quality bat genomes illuminate the molecular basis and evolution of bat adaptations

David Jebb, Zixia Huang, Martin Pippel, Graham M. Hughes, Ksenia Lavrichenko, Paolo Devanna, Sylke Winkler, Lars S. Jermiin, Emilia C. Skirmuntt, Aris Katzourakis, Lucy Burkitt-Gray, David A. Ray, Kevin A. M. Sullivan, Juliana G. Roscito, Bogdan M. Kirilenko, Liliana M. Dávalos, Angelique P. Corthals, Megan L. Power, Gareth Jones, Roger D. Ransome, Dina Dechmann, Andrea G. Locatelli, Sebastien J. Puechmaille, Olivier Fedrigo, Erich D. Jarvis, Mark S. Springer, Michael Hiller, View ORCID ProfileSonja C. Vernes, Eugene W. Myers, Emma C. Teeling
doi: https://doi.org/10.1101/836874
David Jebb
1Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
2Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
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Zixia Huang
4School of Biology and Environmental Science, University College Dublin, Dublin, Ireland
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Martin Pippel
1Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
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Graham M. Hughes
4School of Biology and Environmental Science, University College Dublin, Dublin, Ireland
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Ksenia Lavrichenko
5Neurogenetics of Vocal Communication Group, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
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Paolo Devanna
5Neurogenetics of Vocal Communication Group, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
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Sylke Winkler
1Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
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Lars S. Jermiin
4School of Biology and Environmental Science, University College Dublin, Dublin, Ireland
6Research School of Biology, Australian National University, Canberra, ACT, Australia
7Earth Institute, University College Dublin, Dublin, Ireland
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Emilia C. Skirmuntt
8Peter Medawar Building for Pathogen Research, Department of Zoology, University of Oxford, Oxford, United Kingdom
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Aris Katzourakis
8Peter Medawar Building for Pathogen Research, Department of Zoology, University of Oxford, Oxford, United Kingdom
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Lucy Burkitt-Gray
9Conway Institute of Biomolecular and Biomedical Science, University College Dublin, Dublin, Ireland
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David A. Ray
10Department of Biological Sciences, Texas Tech University, Lubbock, USA
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Kevin A. M. Sullivan
10Department of Biological Sciences, Texas Tech University, Lubbock, USA
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Juliana G. Roscito
1Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
2Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
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Bogdan M. Kirilenko
1Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
2Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
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Liliana M. Dávalos
11Department of Ecology and Evolution, Stony Brook University, Stony Brook, Stony Brook, USA
12Consortium for Inter Disciplinary Environmental Research, Stony Brook University, Stony Brook, USA
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Angelique P. Corthals
13Department of Sciences, John Jay College of Criminal Justice, New York, USA
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Megan L. Power
4School of Biology and Environmental Science, University College Dublin, Dublin, Ireland
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Gareth Jones
14School of Biological Sciences, University of Bristol, Bristol, United Kingdom
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Roger D. Ransome
14School of Biological Sciences, University of Bristol, Bristol, United Kingdom
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Dina Dechmann
15Department of Migration and Immuno-Ecology, Max Planck Institute of Animal Behavior, Radolfzell, Germany
16Department of Biology, University of Konstanz, Konstanz, Germany
17Smithsonian Tropical Research Institute; Panama City, Panama
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Andrea G. Locatelli
4School of Biology and Environmental Science, University College Dublin, Dublin, Ireland
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Sebastien J. Puechmaille
18ISEM, University of Montpellier, Montpellier, France
19Zoological Institute and Museum, University of Greifswald, Greifswald, Germany
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Olivier Fedrigo
20Vertebrate Genomes Laboratory, The Rockefeller University, New York, NY, USA
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Erich D. Jarvis
21Laboratory of Neurogenetics of Language, The Rockefeller University, New York, NY, USA
22Howard Hughes Medical Institute, Chevy Chase, MD, USA
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Mark S. Springer
23Department of Biology, University of California, Riverside, CA, USA
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Michael Hiller
1Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
2Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
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  • For correspondence: hiller@mpi-cbg.de sonja.vernes@mpi.nl gene@mpi-cbg.de emma.teeling@ucd.ie
Sonja C. Vernes
5Neurogenetics of Vocal Communication Group, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands
24Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
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  • For correspondence: hiller@mpi-cbg.de sonja.vernes@mpi.nl gene@mpi-cbg.de emma.teeling@ucd.ie
Eugene W. Myers
1Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
25Faculty of Computer Science, Technical University Dresden, Dresden, Germany
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  • For correspondence: hiller@mpi-cbg.de sonja.vernes@mpi.nl gene@mpi-cbg.de emma.teeling@ucd.ie
Emma C. Teeling
4School of Biology and Environmental Science, University College Dublin, Dublin, Ireland
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  • For correspondence: hiller@mpi-cbg.de sonja.vernes@mpi.nl gene@mpi-cbg.de emma.teeling@ucd.ie
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Abstract

Bats account for ~20% of all extant mammal species and are considered exceptional given their extraordinary adaptations, including biosonar, true flight, extreme longevity, and unparalleled immune systems. To understand these adaptations, we generated reference-quality genomes of six species representing the key divergent lineages. We assembled these genomes with a novel pipeline incorporating state-of-the-art long-read and long-range sequencing and assembly techniques. The genomes were annotated using a maximal evidence approach, de novo predictions, protein/mRNA alignments, Iso-seq long read and RNA-seq short read transcripts, and gene projections from our new TOGA pipeline, retrieving virtually all (>99%) mammalian BUSCO genes. Phylogenetic analyses of 12,931 protein coding-genes and 10,857 conserved non-coding elements identified across 48 mammalian genomes helped to resolve bats’ closest extant relatives within Laurasiatheria, supporting a basal position for bats within Scrotifera. Genome-wide screens along the bat ancestral branch revealed (a) selection on hearing-involved genes (e.g LRP2, SERPINB6, TJP2), which suggest that laryngeal echolocation is a shared ancestral trait of bats; (b) selection (e.g INAVA, CXCL13, NPSR1) and loss of immunity related proteins (e.g. LRRC70, IL36G), including pro-inflammatory NF-kB signalling; and (c) expansion of the APOBEC family, associated with restricting viral infection, transposon activity and interferon signalling. We also identified unique integrated viruses, indicating that bats have a history of tolerating viral pathogens, lethal to other mammal species. Non-coding RNA analyses identified variant and novel microRNAs, revealing regulatory relationships that may contribute to phenotypic diversity in bats. Together, our reference-quality genomes, high-quality annotations, genome-wide screens and in-vitro tests revealed previously unknown genomic adaptations in bats that may explain their extraordinary traits.

Footnotes

  • ↵^ Joint first authors

  • https://genome-public.pks.mpg.de

  • http://bat1k.com

  • https://vertebrategenomesproject.org/

  • https://dazzlerblog.wordpress.com/

  • https://vgp.github.io/genomeark/

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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-NC 4.0 International license.
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Six new reference-quality bat genomes illuminate the molecular basis and evolution of bat adaptations
David Jebb, Zixia Huang, Martin Pippel, Graham M. Hughes, Ksenia Lavrichenko, Paolo Devanna, Sylke Winkler, Lars S. Jermiin, Emilia C. Skirmuntt, Aris Katzourakis, Lucy Burkitt-Gray, David A. Ray, Kevin A. M. Sullivan, Juliana G. Roscito, Bogdan M. Kirilenko, Liliana M. Dávalos, Angelique P. Corthals, Megan L. Power, Gareth Jones, Roger D. Ransome, Dina Dechmann, Andrea G. Locatelli, Sebastien J. Puechmaille, Olivier Fedrigo, Erich D. Jarvis, Mark S. Springer, Michael Hiller, Sonja C. Vernes, Eugene W. Myers, Emma C. Teeling
bioRxiv 836874; doi: https://doi.org/10.1101/836874
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Six new reference-quality bat genomes illuminate the molecular basis and evolution of bat adaptations
David Jebb, Zixia Huang, Martin Pippel, Graham M. Hughes, Ksenia Lavrichenko, Paolo Devanna, Sylke Winkler, Lars S. Jermiin, Emilia C. Skirmuntt, Aris Katzourakis, Lucy Burkitt-Gray, David A. Ray, Kevin A. M. Sullivan, Juliana G. Roscito, Bogdan M. Kirilenko, Liliana M. Dávalos, Angelique P. Corthals, Megan L. Power, Gareth Jones, Roger D. Ransome, Dina Dechmann, Andrea G. Locatelli, Sebastien J. Puechmaille, Olivier Fedrigo, Erich D. Jarvis, Mark S. Springer, Michael Hiller, Sonja C. Vernes, Eugene W. Myers, Emma C. Teeling
bioRxiv 836874; doi: https://doi.org/10.1101/836874

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