Pangolin genomes and the evolution of mammalian scales and immunity
- Siew Woh Choo1,2,3,22,
- Mike Rayko4,22,
- Tze King Tan1,2,
- Ranjeev Hari1,2,
- Aleksey Komissarov4,
- Wei Yee Wee1,2,
- Andrey A. Yurchenko4,
- Sergey Kliver4,
- Gaik Tamazian4,
- Agostinho Antunes5,6,
- Richard K. Wilson7,
- Wesley C. Warren7,
- Klaus-Peter Koepfli8,
- Patrick Minx7,
- Ksenia Krasheninnikova4,
- Antoinette Kotze9,10,
- Desire L. Dalton9,10,
- Elaine Vermaak9,
- Ian C. Paterson2,11,
- Pavel Dobrynin4,
- Frankie Thomas Sitam12,
- Jeffrine J. Rovie-Ryan12,
- Warren E. Johnson8,
- Aini Mohamed Yusoff1,2,
- Shu-Jin Luo13,
- Kayal Vizi Karuppannan12,
- Gang Fang14,
- Deyou Zheng15,
- Mark B. Gerstein16,17,18,
- Leonard Lipovich19,20,
- Stephen J. O'Brien4,21 and
- Guat Jah Wong1
- 1Genome Informatics Research Laboratory, Centre for Research in Biotechnology for Agriculture (CEBAR), University of Malaya, 50603 Kuala Lumpur, Malaysia;
- 2Department of Oral and Craniofacial Sciences, Faculty of Dentistry, University of Malaya, 50603 Kuala Lumpur, Malaysia;
- 3Genome Solutions Sdn Bhd, Research Management & Innovation Complex, University of Malaya, 50603 Kuala Lumpur, Malaysia;
- 4Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg, Russia 199004;
- 5CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, 4050-123 Porto, Portugal;
- 6Department of Biology, Faculty of Sciences, University of Porto, 4169-007 Porto, Portugal;
- 7McDonnell Genome Institute, Washington University, St. Louis, Missouri 63108, USA;
- 8National Zoological Park, Smithsonian Conservation Biology Institute, Washington, DC 20008, USA;
- 9National Zoological Gardens of South Africa, Pretoria 0001, South Africa;
- 10Department of Genetics, University of the Free State, Bloemfontein, 9300, South Africa;
- 11Oral Cancer Research and Coordinating Centre, Faculty of Dentistry, University of Malaya, 50603 Kuala Lumpur, Malaysia;
- 12Ex-Situ Conservation Division, Department of Wildlife and National Parks, 56100 Kuala Lumpur, Malaysia;
- 13Peking-Tsinghua Center for Life Sciences, College of Life Sciences, Peking University, Beijing, China 100871;
- 14NYU Shanghai, Pudong, Shanghai, China 200122;
- 15Department of Neurology, Albert Einstein College of Medicine, Bronx, New York 10461, USA;
- 16Program in Computational Biology and Bioinformatics, Yale University, New Haven, Connecticut 06520, USA;
- 17Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520, USA;
- 18Department of Computer Science, Yale University, New Haven, Connecticut 06520, USA;
- 19Center for Molecular Medicine and Genetics, Wayne State University, Detroit, Michigan 48201, USA;
- 20Department of Neurology, School of Medicine, Wayne State University, Detroit, Michigan 48201, USA;
- 21Oceanographic Center, Nova Southeastern University, Ft. Lauderdale, Florida 33004, USA
- Corresponding authors: l.choo{at}genomesolutions.com.my, lgdchief{at}gmail.com
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↵22 These authors contributed equally to this work.
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.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.203521.115.
- Received December 17, 2015.
- Accepted August 4, 2016.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
