Genomic consequences of population decline in critically endangered pangolins and their demographic histories

Jing-Yang Hu; Zi-Qian Hao; Laurent Frantz; Shi-Fang Wu; Wu Chen; Yun-Fang Jiang; Hong Wu; Wei-Min Kuang; Haipeng Li; Ya-Ping Zhang; Li Yu

doi:10.1093/nsr/nwaa031

Genomic consequences of population decline in critically endangered pangolins and their demographic histories

Natl Sci Rev. 2020 Apr;7(4):798-814. doi: 10.1093/nsr/nwaa031. Epub 2020 Feb 27.

Authors

Jing-Yang Hu^{1

2

3}, Zi-Qian Hao^{4

5}, Laurent Frantz^{6

7}, Shi-Fang Wu², Wu Chen⁸, Yun-Fang Jiang⁹, Hong Wu¹, Wei-Min Kuang¹, Haipeng Li^{4

10}, Ya-Ping Zhang^{1

2

3

10}, Li Yu¹

Affiliations

¹ State Key Laboratory for Conservation and Utilization of Bio-Resource in Yunnan, School of Life Sciences, Yunnan University, Kunming 650091, China.
² State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
³ Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming 650204, China.
⁴ CAS Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai Institute of Nutrition and Health, Chinese Academy of Sciences, Shanghai 200031, China.
⁵ University of Chinese Academy of Sciences, Beijing 100049, China.
⁶ School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, UK.
⁷ The Palaeogenomics and Bio-Archaeology Research Network, Department of Archaeology, University of Oxford, Oxford OX1 3TG, UK.
⁸ Guangzhou Zoo, Guangzhou 510070, China.
⁹ Lushui Management and Conservation Branch of Gaoligong Mountain National Nature Reserve, Nujiang 673100, China.
¹⁰ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China.

Abstract

Pangolins are among the most critically endangered animals due to heavy poaching and worldwide trafficking. However, their demographic histories and the genomic consequences of their recent population declines remain unknown. We generated high-quality de novo reference genomes for critically endangered Malayan (Manis javanica, MJ) and Chinese (M. pentadactyla, MP) pangolins and re-sequencing population genomic data from 74 MJs and 23 MPs. We recovered the population identities of illegally traded pangolins and previously unrecognized genetic populations that should be protected as evolutionarily distinct conservation units. Demographic reconstruction suggested environmental changes have resulted in a population size fluctuation of pangolins. Additionally, recent population size declines due to human activities have resulted in an increase in inbreeding and genetic load. Deleterious mutations were enriched in genes related to cancer/diseases and cholesterol homeostasis, which may have increased their susceptibility to diseases and decreased their survival potential to adapt to environmental changes and high-cholesterol diets. This comprehensive study provides not only high-quality pangolin reference genomes, but also valuable information concerning the driving factors of long-term population size fluctuations and the genomic impact of recent population size declines due to human activities, which is essential for pangolin conservation management and global action planning.

Keywords: demographic history; genetic diversity; genetic load; inbreeding; pangolins; population declines; population genomics.