Revealing extensive inbreeding and less-efficient purging of deleterious mutations in wild Amur tigers in China

Tianming Lan; Haimeng Li; Boyang Liu; Minhui Shi; Yinping Tian; Sunil Kumar Sahu; Liangyu Cui; Nicolas Dussex; Dan Liu; Yue Ma; Weiyao Kong; Shanlin Liu; Jiale Fan; Yue Zhao; Yuan Fu; Qiye Li; Chen Lin; Love Dalén; Huan Liu; Le Zhang; Guangshun Jiang; Yanchun Xu

doi:10.1016/j.jgg.2024.12.004

Revealing extensive inbreeding and less-efficient purging of deleterious mutations in wild Amur tigers in China

J Genet Genomics. 2024 Dec 12:S1673-8527(24)00336-9. doi: 10.1016/j.jgg.2024.12.004. Online ahead of print.

Authors

Tianming Lan¹, Haimeng Li², Boyang Liu³, Minhui Shi⁴, Yinping Tian³, Sunil Kumar Sahu⁵, Liangyu Cui³, Nicolas Dussex⁶, Dan Liu⁷, Yue Ma³, Weiyao Kong⁸, Shanlin Liu⁹, Jiale Fan³, Yue Zhao³, Yuan Fu³, Qiye Li⁴, Chen Lin³, Love Dalén⁶, Huan Liu¹⁰, Le Zhang¹¹, Guangshun Jiang¹², Yanchun Xu¹³

Affiliations

¹ College of Wildlife and Protected Area, Northeast Forestry University, Harbin, Heilongjiang 150040, China; BGI Life Science Joint Research Center, Northeast Forestry University, Harbin, Heilongjiang 150040, China.
² College of Wildlife and Protected Area, Northeast Forestry University, Harbin, Heilongjiang 150040, China; State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Shenzhen, Guangdong 518083, China; Heilongjiang Key Laboratory of Complex Traits and Protein Machines in Organisms, Harbin, Heilongjiang 150040, China.
³ College of Wildlife and Protected Area, Northeast Forestry University, Harbin, Heilongjiang 150040, China.
⁴ State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Shenzhen, Guangdong 518083, China.
⁵ BGI Research, Wuhan, Hubei 430074, China.
⁶ Centre for Palaeogenetics, Svante Arrhenius väg 20C, 10691 Stockholm, Sweden; Department of Zoology, Stockholm University, Stockholm, Sweden; Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden.
⁷ Heilongjiang Siberian Tiger Park, Harbin, Heilongjiang 150000, China.
⁸ Jinlin Provincial Academy of Forestry Science, Changchun, Jilin 130033, China.
⁹ Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
¹⁰ BGI Life Science Joint Research Center, Northeast Forestry University, Harbin, Heilongjiang 150040, China; State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Shenzhen, Guangdong 518083, China; Guangdong Provincial Key Laboratory of Genome Read and Write, BGI-Shenzhen, Shenzhen, Guangdong 518120, China.
¹¹ College of Wildlife and Protected Area, Northeast Forestry University, Harbin, Heilongjiang 150040, China. Electronic address: [email protected].
¹² College of Wildlife and Protected Area, Northeast Forestry University, Harbin, Heilongjiang 150040, China. Electronic address: [email protected].
¹³ College of Wildlife and Protected Area, Northeast Forestry University, Harbin, Heilongjiang 150040, China; BGI Life Science Joint Research Center, Northeast Forestry University, Harbin, Heilongjiang 150040, China; National Forestry and Grassland Administration Research Center of Engineering Technology for Wildlife Conservation and Utilization, Harbin, Heilongjiang,150040 China. Electronic address: [email protected].

PMID: 39674273
DOI: 10.1016/j.jgg.2024.12.004

Abstract

Inbreeding increases genome homozygosity within populations, which can exacerbate inbreeding depression by exposing homozygous deleterious alleles that are responsible for declines in fitness traits. In small populations, genetic purging that occurs under pressure of natural selection acts as an opposing force, contributing to a reduction of deleterious alleles. Both inbreeding and genetic purging are paramount in the field of conservation genomics. The Amur tiger (Panthera tigris altaica) lives in small populations in the forests of Northeast Asia and is among the most endangered animals on the planet. Using genome-wide assessment and comparison, we reveal substantially higher and more extensive inbreeding in wild Amur tigers (F_ROH = 0.50) than in captive individuals (F_ROH = 0.24). However, a relatively reduced number of loss-of-function mutations in wild Amur tigers was observed when compared with captive individuals, indicating a genetic purging of relatively large-effect inbreeding load. The higher ratio of homozygous mutation load and number of fixed damaging alleles in the wild population indicate a less-efficient genetic purging, with purifying selection also contributing to this process. These findings provide valuable insights for future conservation of Amur tigers.

Keywords: Panthera tigris altaica; conservation genomics; genetic purging; inbreeding; mutational load.