Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears

Shiping Liu; Eline D Lorenzen; Matteo Fumagalli; Bo Li; Kelley Harris; Zijun Xiong; Long Zhou; Thorfinn Sand Korneliussen; Mehmet Somel; Courtney Babbitt; Greg Wray; Jianwen Li; Weiming He; Zhuo Wang; Wenjing Fu; Xueyan Xiang; Claire C Morgan; Aoife Doherty; Mary J O'Connell; James O McInerney; Erik W Born; Love Dalén; Rune Dietz; Ludovic Orlando; Christian Sonne; Guojie Zhang; Rasmus Nielsen; Eske Willerslev; Jun Wang

doi:10.1016/j.cell.2014.03.054

Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears

Cell. 2014 May 8;157(4):785-94. doi: 10.1016/j.cell.2014.03.054.

Authors

Shiping Liu¹, Eline D Lorenzen², Matteo Fumagalli³, Bo Li⁴, Kelley Harris⁵, Zijun Xiong⁴, Long Zhou⁴, Thorfinn Sand Korneliussen⁶, Mehmet Somel³, Courtney Babbitt⁷, Greg Wray⁷, Jianwen Li⁴, Weiming He¹, Zhuo Wang⁴, Wenjing Fu⁴, Xueyan Xiang⁸, Claire C Morgan⁹, Aoife Doherty¹⁰, Mary J O'Connell⁹, James O McInerney¹⁰, Erik W Born¹¹, Love Dalén¹², Rune Dietz¹³, Ludovic Orlando⁶, Christian Sonne¹³, Guojie Zhang¹⁴, Rasmus Nielsen¹⁵, Eske Willerslev¹⁶, Jun Wang¹⁷

Affiliations

¹ BGI-Shenzhen, Shenzhen 518083, China; School of Bioscience and Biotechnology, South China University of Technology, Guangzhou 510641, China.
² Department of Integrative Biology, 3060 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA; Centre for GeoGenetics, Natural History Museum, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen K, Denmark.
³ Department of Integrative Biology, 3060 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA.
⁴ BGI-Shenzhen, Shenzhen 518083, China.
⁵ Department of Mathematics, 970 Evans Hall, University of California, Berkeley, CA 94720, USA.
⁶ Centre for GeoGenetics, Natural History Museum, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen K, Denmark.
⁷ Department of Biology, 124 Science Drive, Duke Box # 90338, Duke University, Durham, NC 27708, USA; Institute for Genome Sciences & Policy, 101 Science Drive, DUMC Box 3382, Duke University, Durham, NC 27708, USA.
⁸ BGI-Shenzhen, Shenzhen 518083, China; College of Life Sciences, Sichuan University, Chengdu 610064, China.
⁹ Bioinformatics and Molecular Evolution Group, School of Biotechnology, Dublin City University, Glasnevin, Dublin 9, Ireland.
¹⁰ Bioinformatics and Molecular Evolution Unit, Department of Biology, National University of Ireland, Maynooth, Co. Kildare, Ireland.
¹¹ Greenland Institute of Natural Resources, c/o Government of Greenland Representation in Denmark, Strandgade 91, 3. Floor, PO Box 2151, 1016 Copenhagen K, Denmark.
¹² Department of Bioinformatics and Genetics, Swedish Museum of Natural History, PO Box 50007, 10405, Stockholm, Sweden.
¹³ Department of Bioscience, Arctic Research Centre, Aarhus University, Frederiksborgvej 399, PO Box 358, 4000 Roskilde, Denmark.
¹⁴ BGI-Shenzhen, Shenzhen 518083, China; Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark.
¹⁵ BGI-Shenzhen, Shenzhen 518083, China; Department of Integrative Biology, 3060 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA; Department of Statistics, 367 Evans Hall, University of California, Berkeley, CA 94720, USA; Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, 2200 Copenhagen Ø, Denmark. Electronic address: rasmus_nielsen@berkeley.edu.
¹⁶ Centre for GeoGenetics, Natural History Museum, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen K, Denmark. Electronic address: ewillerslev@snm.ku.dk.
¹⁷ BGI-Shenzhen, Shenzhen 518083, China; Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, 2200 Copenhagen Ø, Denmark; Princess Al Jawhara Center of Excellence in the Research of Hereditary Disorders, King Abdulaziz University, Jeddah 21589, Saudi Arabia; Macau University of Science and Technology, Avenida Wai Long, Taipa, Macau 999078, China; Department of Medicine, University of Hong Kong, Sassoon Road, Pokfulam, Hong Kong. Electronic address: wangj@genomics.org.cn.

Abstract

Polar bears are uniquely adapted to life in the High Arctic and have undergone drastic physiological changes in response to Arctic climates and a hyper-lipid diet of primarily marine mammal prey. We analyzed 89 complete genomes of polar bear and brown bear using population genomic modeling and show that the species diverged only 479-343 thousand years BP. We find that genes on the polar bear lineage have been under stronger positive selection than in brown bears; nine of the top 16 genes under strong positive selection are associated with cardiomyopathy and vascular disease, implying important reorganization of the cardiovascular system. One of the genes showing the strongest evidence of selection, APOB, encodes the primary lipoprotein component of low-density lipoprotein (LDL); functional mutations in APOB may explain how polar bears are able to cope with life-long elevated LDL levels that are associated with high risk of heart disease in humans.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Adaptation, Physiological
Adipose Tissue / metabolism
Animals
Apolipoproteins B / chemistry
Apolipoproteins B / metabolism
Arctic Regions
Biological Evolution*
Fatty Acids / metabolism
Gene Flow
Genetics, Population
Genome
Ursidae / classification*
Ursidae / genetics*
Ursidae / physiology

Substances

Apolipoproteins B
Fatty Acids

Abstract

Publication types

MeSH terms

Substances

Grants and funding