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Cited by 361Bat Biology and Ecology StudiesGenomics and Phylogenetic StudiesChromosomal and Genetic Variations

Six reference-quality genomes reveal evolution of bat adaptations

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Jebb, David, Huang, Zixia, Pippel, Martin, Hughes, Graham M., Lavrichenko, Ksenia, Devanna, Paolo, Winkler, Sylke, Jermiin, Lars S. +21 more·2020·Nature
DOI 10.1038/s41586-020-2486-3PMC PMC8075899

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Abstract

Bats possess extraordinary adaptations, including flight, echolocation, extreme longevity and unique immunity. High-quality genomes are crucial for understanding the molecular basis and evolution of these traits. Here we incorporated long-read sequencing and state-of-the-art scaffolding protocols 1 to generate, to our knowledge, the first reference-quality genomes of six bat species ( Rhinolophus ferrumequinum , Rousettus aegyptiacus , Phyllostomus discolor , Myotis myotis , Pipistrellus kuhlii and Molossus molossus ). We integrated gene projections from our ‘Tool to infer Orthologs from Genome Alignments’ (TOGA) software with de novo and homology gene predictions as well as short- and long-read transcriptomics to generate highly complete gene annotations. To resolve the phylogenetic position of bats within Laurasiatheria, we applied several phylogenetic methods to comprehensive sets of orthologous protein-coding and noncoding regions of the genome, and identified a basal origin for bats within Scrotifera. Our genome-wide screens revealed positive selection on hearing-related genes in the ancestral branch of bats, which is indicative of laryngeal echolocation being an ancestral trait in this clade. We found selection and loss of immunity-related genes (including pro-inflammatory NF-κB regulators) and expansions of anti-viral APOBEC3 genes, which highlights molecular mechanisms that may contribute to the exceptional immunity of bats. Genomic integrations of diverse viruses provide a genomic record of historical tolerance to viral infection in bats. Finally, we found and experimentally validated bat-specific variation in microRNAs, which may regulate bat-specific gene-expression programs. Our reference-quality bat genomes provide the resources required to uncover and validate the genomic basis of adaptations of bats, and stimulate new avenues of research that are directly relevant to human health and disease 1 .

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  • Distinguishing orthologs and paralogs is a fundamental problem in evolutionary and molecular biology and a prerequisite for many genomic analyses.

    “Distinguishing orthologs and paralogs is a fundamental problem in evolutionary and molecular biology (1) and a prerequisite for many genomic analyses, including reconstructing phylogenetic trees, predicting gene function, investigating molecular and genome evolution, and discovering differences in genes that underlie phenotypes of the sequenced species (2–6).”

    From Integrating gene annotation with orthology inference at scale (2023) · cites this paper as [6]

    The citation is attached to the first clause, which calls distinguishing orthologs from paralogs a fundamental problem. In Methods > Phylogenomics (page unavailable), the paper uses genes classified as 1:1 orthologues to infer a species tree, showing the relevance of orthology to evolutionary analysis. It does not discuss distinguishing orthologs from paralogs or characterize that distinction as a fundamental problem. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

  • TOGA enables phylogenomic analyses as well as screens for selection patterns and gene losses that are linked to relevant phenotypes.

    “First, by detecting inactivated genes and providing orthologous sequences for codon alignments, TOGA enables phylogenomic analyses as well as screens for selection patterns and gene losses that are linked to relevant phenotypes (6, 35–38).”

    From Integrating gene annotation with orthology inference at scale (2023) · cites this paper as [6]

    The Methods > Phylogenomics section says TOGA classified 12,931 genes as orthologues for sequence alignments and phylogenomic analysis; Methods > Gene selection, loss and gain describes a selection screen of those genes. The paper also reports gene-loss screens linked to bat traits, but attributes the loss-screening procedure to a previously developed approach, not explicitly to TOGA. Our copy therefore does not establish the TOGA-enabled gene-loss part of the claim. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • For six high-quality bat genomes, annotations integrating available transcriptomics data, ab initio gene predictions, aligned proteins from closely related bats, and comparative gene predictions contained 87.7% to 95.4% of the genes in the mammalian BUSCO odb10 set.

    “For the six bats, these annotations contained 87.7% to 95.4% of the genes in the mammalian BUSCO odb10 set (Fig. 3C, Table S9).”

    From Integrating gene annotation with orthology inference at scale (2023) · cites this paper as [6]

    Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

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Authors
Jebb, D., Huang, Z., Pippel, M., Hughes, G. M., Lavrichenko, K., Devanna, P., Winkler, S., Jermiin, L. S., Skirmuntt, E. C., Katzourakis, A., Burkitt-Gray, L., Ray, D. A., Sullivan, K. A. M., Roscito, J. G., Kirilenko, B. M., Dávalos, L. M., Corthals, A. P., Power, M. L., Jones, G., Ransome, R. D., Dechmann, D. K. N., Locatelli, A. G., Puechmaille, S. J., Fedrigo, O., Jarvis, E. D., Hiller, M., Vernes, S. C., Myers, E. W., & Teeling, E. C.
Affiliations
  • Max Planck Institute for the Physics of Complex Systems (DE)
  • University College Dublin (IE)
  • Center for Systems Biology Dresden (DE)
  • Max Planck Institute for Psycholinguistics (NL)
  • Max Planck Institute of Molecular Cell Biology and Genetics (DE)
  • University of Oxford (GB)
  • Texas Tech University (US)
  • Stony Brook University (US)
  • University of Bristol (GB)
  • Smithsonian Tropical Research Institute (PA)
  • Université de Montpellier (FR)
  • Rockefeller University (US)
  • Howard Hughes Medical Institute (US)
Corresponding author
  • Hiller, Michael
  • Vernes, Sonja C.
  • Myers, Eugene W.
  • Teeling, Emma C.
ORCID
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2020-07-22
Volume
583
Issue
7817
Pages
578-584
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/s41586-020-2486-3
PMC
PMC8075899
OpenAlex
W3035280753
Cited by
361
References
6
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35.55
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Language
en
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Funders
  • National Science Foundation (1442142, 1838283, 1531492, 1838273, 1633299)
  • Howard Hughes Medical Institute
  • Wellcome Trust (204844/Z/16/Z)
  • Royal Society
  • Royal Irish Academy
  • Science Foundation Ireland (204844/Z/16/Z)
  • University College Dublin (204,844/Z/16/Z)
  • Deutsche Forschungsgemeinschaft (HI 1423/3-1)
  • Irish Research Council
  • Bundesministerium für Bildung und Forschung (01IS18026C)
  • Technische Universität Dresden
  • Max-Planck-Gesellschaft
  • Stony Brook University
  • FP7 Ideas: European Research Council (311000)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Bat Biology and Ecology Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
Keywords
bat genome, bat evolution, echolocation, positive selection, APOBEC3, NF-κB, virus tolerance, microRNA, greater horseshoe bat, Rousettus aegyptiacus, Phyllostomus discolor, Myotis myotis, Pipistrellus kuhlii, Molossus molossus, genome annotation
MeSH terms
Adaptation, Physiological, Animals, Chiroptera, DNA Transposable Elements, Immunity, Phylogeny, Reference Standards, Viruses, Reproducibility of Results, Virus Integration, Genome, Evolution, Molecular, RNA, Untranslated, Genomics, Molecular Sequence Annotation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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