Pangolin genomes and the evolution of mammalian scales and immunity
- Siew Woh Choo1,15,
- Mike Rayko2,
- Tze King Tan1,
- Ranjeev Hari1,
- Aleksey Komissarov2,
- Wei Yee Wee1,
- Andrey Yurchenko2,
- Sergey Kliver2,
- Gaik Tamazian2,
- Agostinho Antunes3,
- Richard K. Wilson4,
- Wesley C. Warren4,
- Klaus-Peter Koepfli5,
- Patrick Minx4,
- Ksenia Krasheninnikova2,
- Antoinette Kotze6,
- Desire L. Dalton6,
- Elaine Vermaak7,
- Ian C. Paterson1,
- Pavel Dobrynin2,
- Frankie Thomas Sitam8,
- Jeffrine Rovie Ryan Japning8,
- Warren E. Johnson5,
- Aini Mohamed Yusoff1,
- Shu-Jin Luo9,
- Kayal Vizi Karuppannan8,
- Gang Fang10,
- Deyou Zheng11,
- Mark B. Gerstein12,
- Leonard Lipovich13,
- Stephen J. O'Brien14 and
- Guat Jah Wong1
- 1 University of Malaya;
- 2 Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, Russia;
- 3 University of Porto;
- 4 McDonnell Genome Institute, Washington University;
- 5 Smithsonian Conservation Biology Institute;
- 6 University of the Free State;
- 7 National Zoological Gardens of South Africa;
- 8 Department of Wildlife and National Parks, Malaysia;
- 9 Peking University;
- 10 NYU Shanghai;
- 11 Albert Einstein College of Medicine, USA;
- 12 Yale University;
- 13 Wayne State University;
- 14 Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University
- ↵* Corresponding author; email: csw1978{at}hotmail.com
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 (IFN-ε), exclusively expressed in epithelial cells and important in skin and mucosal immunity, is pseudogenised 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 IFN-ε-deficient animal model for studying mammalian immunity.
- Received December 17, 2015.
- Accepted August 4, 2016.
- Published by Cold Spring Harbor Laboratory Press
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/.
