Pangolin genomes and the evolution of mammalian scales and immunity

Choo SW 1 , Rayko M 2 , Tan TK 3 , Hari R 3 , Komissarov A 2 , Wee WY 3 Show all authors , Yurchenko AA 2 , Kliver S 2 , Tamazian G 2 , Antunes A 4 , Wilson RK 5 , Warren WC 5 , Koepfli KP 6 , Minx P 5 , Krasheninnikova K 2 , Kotze A 7 , Dalton DL 7 , Vermaak E 8 , Paterson IC 9 , Dobrynin P 2 , Sitam FT 10 , Rovie-Ryan JJ 10 , Johnson WE 6 , Yusoff AM 3 , Luo SJ 11 , Karuppannan KV 10 , Fang G 12 , Zheng D 13 , Gerstein MB 14 , Lipovich L 15 , O'Brien SJ 16 , Wong GJ 17

Affiliations 

  • 1 Genome Informatics Research Laboratory, Centre for Research in Biotechnology for Agriculture (CEBAR), University of Malaya, 50603 Kuala Lumpur, Malaysia; Department of Oral and Craniofacial Sciences, Faculty of Dentistry, University of Malaya, 50603 Kuala Lumpur, Malaysia; Genome Solutions Sdn Bhd, Research Management & Innovation Complex, University of Malaya, 50603 Kuala Lumpur, Malaysia
  • 2 Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg, Russia 199004
  • 3 Genome Informatics Research Laboratory, Centre for Research in Biotechnology for Agriculture (CEBAR), University of Malaya, 50603 Kuala Lumpur, Malaysia; Department of Oral and Craniofacial Sciences, Faculty of Dentistry, University of Malaya, 50603 Kuala Lumpur, Malaysia
  • 4 CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, 4050-123 Porto, Portugal; Department of Biology, Faculty of Sciences, University of Porto, 4169-007 Porto, Portugal
  • 5 McDonnell Genome Institute, Washington University, St. Louis, Missouri 63108, USA
  • 6 National Zoological Park, Smithsonian Conservation Biology Institute, Washington, DC 20008, USA
  • 7 National Zoological Gardens of South Africa, Pretoria 0001, South Africa; Department of Genetics, University of the Free State, Bloemfontein, 9300, South Africa
  • 8 National Zoological Gardens of South Africa, Pretoria 0001, South Africa
  • 9 Department of Oral and Craniofacial Sciences, Faculty of Dentistry, University of Malaya, 50603 Kuala Lumpur, Malaysia; Oral Cancer Research and Coordinating Centre, Faculty of Dentistry, University of Malaya, 50603 Kuala Lumpur, Malaysia
  • 10 Ex-Situ Conservation Division, Department of Wildlife and National Parks, 56100 Kuala Lumpur, Malaysia
  • 11 Peking-Tsinghua Center for Life Sciences, College of Life Sciences, Peking University, Beijing, China 100871
  • 12 NYU Shanghai, Pudong, Shanghai, China 200122
  • 13 Department of Neurology, Albert Einstein College of Medicine, Bronx, New York 10461, USA
  • 14 Program in Computational Biology and Bioinformatics, Yale University, New Haven, Connecticut 06520, USA; Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520, USA; Department of Computer Science, Yale University, New Haven, Connecticut 06520, USA
  • 15 Center for Molecular Medicine and Genetics, Wayne State University, Detroit, Michigan 48201, USA; Department of Neurology, School of Medicine, Wayne State University, Detroit, Michigan 48201, USA
  • 16 Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg, Russia 199004; Oceanographic Center, Nova Southeastern University, Ft. Lauderdale, Florida 33004, USA
  • 17 Genome Informatics Research Laboratory, Centre for Research in Biotechnology for Agriculture (CEBAR), University of Malaya, 50603 Kuala Lumpur, Malaysia
Genome Res, 2016 10;26(10):1312-1322.
PMID: 27510566

Abstract

Pangolins, unique mammals with scales over most of their body, no teeth, poor vision, and an acute olfactory system, comprise the only placental order (Pholidota) without a whole-genome map. To investigate pangolin biology and evolution, we developed genome assemblies of the Malayan (Manis javanica) and Chinese (M. pentadactyla) pangolins. Strikingly, we found that interferon epsilon (IFNE), exclusively expressed in epithelial cells and important in skin and mucosal immunity, is pseudogenized in all African and Asian pangolin species that we examined, perhaps impacting resistance to infection. We propose that scale development was an innovation that provided protection against injuries or stress and reduced pangolin vulnerability to infection. Further evidence of specialized adaptations was evident from positively selected genes involving immunity-related pathways, inflammation, energy storage and metabolism, muscular and nervous systems, and scale/hair development. Olfactory receptor gene families are significantly expanded in pangolins, reflecting their well-developed olfaction system. This study provides insights into mammalian adaptation and functional diversification, new research tools and questions, and perhaps a new natural IFNE-deficient animal model for studying mammalian immunity.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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