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Six reference-quality genomes reveal evolution of bat adaptations

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Jebb_2020_Sex_reference_quality_genomes_Nature_578_CCBY.pdf (14.16Mb)
Date
23/07/2020
Author
Jebb, David
Huang, Zixia
Pippel, Martin
Hughes, Graham M
Lavrichenko, Ksenia
Devanna, Paolo
Winkler, Sylke
Jermiin, Lars S
Skirmuntt, Emilia C
Katzourakis, Aris
Burkitt-Gray, Lucy
Ray, David A
Sullivan, Kevin A M
Roscito, Juliana G
Kirilenko, Bogdan M
Dávalos, Liliana M
Corthals, Angelique P
Power, Megan L
Jones, Gareth
Ransome, Roger D
Dechmann, Dina K N
Locatelli, Andrea G
Puechmaille, Sébastien J
Fedrigo, Olivier
Jarvis, Erich D
Hiller, Michael
Vernes, Sonja C
Myers, Eugene W
Teeling, Emma C
Keywords
Adaptation, physiological/genetics
Animals
Chiroptera/classification
DNA transposable elements/genetics
Evolution, molecular
Genome/genetics
Genomics/standards
Immunity/genetics
Molecular sequence annotation/standards
Phylogeny
RNA, untranslated/genetics
Reference standards
Reproducibility of results
Virus integration/genetics
Viruses/genetics
QH426 Genetics
QR180 Immunology
QR355 Virology
DAS
SDG 3 - Good Health and Well-being
Metadata
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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 protocols1 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 disease1.
Citation
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 2020 , ' Six reference-quality genomes reveal evolution of bat adaptations ' , Nature , vol. 583 , no. 7817 , pp. 578-584 . https://doi.org/10.1038/s41586-020-2486-3
Publication
Nature
Status
Peer reviewed
DOI
https://doi.org/10.1038/s41586-020-2486-3
ISSN
0028-0836
Type
Journal article
Rights
Copyright © 2020 The Author(s). Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
Description
Funding: E.W.M. and M.P. were supported by the Max Planck Society and were partially funded by the Federal Ministry of Education and Research (grant 01IS18026C). All data produced in Dresden were funded directly by the Max Planck Society. S.C.V., P.D. and K.L. were funded by a Max Planck Research Group awarded to S.C.V. from the Max Planck Society, and a Human Frontiers Science Program (HFSP) Research grant awarded to S.C.V. (RGP0058/2016). M.H. was funded by the German Research Foundation (HI 1423/3-1) and the Max Planck Society. E.C.T. was funded by a European Research Council Research Grant (ERC-2012-StG311000), UCD Wellcome Institutional Strategic Support Fund, financed jointly by University College Dublin and SFI-HRB-Wellcome Biomedical Research Partnership (ref 204844/Z/16/Z) and Irish Research Council Consolidator Laureate Award. G.M.H. was funded by a UCD Ad Astra Fellowship. G.J. and E.C.T. were funded from the Royal Society/Royal Irish Academy cost share programme. L.M.D. was supported by NSF-DEB 1442142 and 1838273, and NSF-DGE 1633299. D.A.R. was supported by NSF-DEB 1838283. E.D.J. and O.F. were funded by the Rockefeller University and the Howard Hughes Medical Institute.
Collections
  • University of St Andrews Research
URI
http://hdl.handle.net/10023/21776

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