TY - JOUR
T1 - Six reference-quality genomes reveal evolution of bat adaptations
AU - Jebb, David
AU - Huang, Zixia
AU - Pippel, Martin
AU - Hughes, Graham M.
AU - Lavrichenko, Ksenia
AU - Devanna, Paolo
AU - Winkler, Sylke
AU - Jermiin, Lars S.
AU - Skirmuntt, Emilia C.
AU - Katzourakis, Aris
AU - Burkitt-Gray, Lucy
AU - Ray, David A.
AU - Sullivan, Kevin A.M.
AU - Roscito, Juliana G.
AU - Kirilenko, Bogdan M.
AU - Dávalos, Liliana M.
AU - Corthals, Angelique P.
AU - Power, Megan L.
AU - Jones, Gareth
AU - Ransome, Roger D.
AU - Dechmann, Dina K.N.
AU - Locatelli, Andrea G.
AU - Puechmaille, Sébastien J.
AU - Fedrigo, Olivier
AU - Jarvis, Erich D.
AU - Hiller, Michael
AU - Vernes, Sonja C.
AU - Myers, Eugene W.
AU - Teeling, Emma C.
N1 - Funding Information:
Acknowledgements 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. We thank Stony Brook Research Computing and Cyberinfrastructure, and the Institute for Advanced Computational Science at Stony Brook University for access to the high-performance SeaWulf computing system (which was made possible by a National Science Foundation grant (no. 1531492)); the Long Read Team of the DRESDEN-concept Genome Center, DFG NGS Competence Center, part of the Center for Molecular and Cellular Bioengineering (CMCB), Technische Universität Dresden; S. Kuenzel and his team of the Max Planck Institute of Evolutionary Biology; members of the Vertebrate Genomes Laboratory at The Rockefeller University for their support; L. Wiegrebe, U. Firzlaff and M. Yartsev, who gave us access to captive colonies of Phyllostomus and Rousettus bats and aided with tissue sample collection; and M. Springer, for completing the SVDquartet analyses, and providing phylogenetic input and expertise.
Publisher Copyright:
© 2020, The Author(s).
PY - 2020/7/23
Y1 - 2020/7/23
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85088399759&partnerID=8YFLogxK
U2 - 10.1038/s41586-020-2486-3
DO - 10.1038/s41586-020-2486-3
M3 - Article
C2 - 32699395
AN - SCOPUS:85088399759
VL - 583
SP - 578
EP - 584
JO - Nature
JF - Nature
SN - 0028-0836
IS - 7817
ER -