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Nature genetics
08, 2016;48 (8): 947-52.

Genomic analysis of snub-nosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation.

Li Yu, Guo-Dong Wang, Jue Ruan, Yong-Bin Chen, Cui-Ping Yang, Xue Cao, Hong Wu, Yan-Hu Liu, Zheng-Lin Du, Xiao-Ping Wang, Jing Yang, Shao-Chen Cheng, Li Zhong, Lu Wang, Xuan Wang, Jing-Yang Hu, Lu Fang, Bing Bai, Kai-Le Wang, Na Yuan, Shi-Fang Wu, Bao-Guo Li, Jin-Guo Zhang, Ye-Qin Yang, Cheng-Lin Zhang, Yong-Cheng Long, Hai-Shu Li, Jing-Yuan Yang, David M Irwin, Oliver A Ryder, Ying Li, Chung-I Wu, Ya-Ping Zhang
Author Information
  1. Li Yu: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  2. Guo-Dong Wang: State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
  3. Jue Ruan: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  4. Yong-Bin Chen: Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences and Yunnan Province, Kunming Institute of Zoology, Kunming, China.
  5. Cui-Ping Yang: Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences and Yunnan Province, Kunming Institute of Zoology, Kunming, China.
  6. Xue Cao: State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
  7. Hong Wu: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  8. Yan-Hu Liu: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  9. Zheng-Lin Du: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  10. Xiao-Ping Wang: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  11. Jing Yang: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  12. Shao-Chen Cheng: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  13. Li Zhong: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  14. Lu Wang: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  15. Xuan Wang: State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
  16. Jing-Yang Hu: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  17. Lu Fang: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  18. Bing Bai: State Key Laboratory for Conservation and Utilization of Bio-resource in Yunnan, Yunnan University, Kunming, China.
  19. Kai-Le Wang: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  20. Na Yuan: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  21. Shi-Fang Wu: State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
  22. Bao-Guo Li: College of Life Sciences, Northwest University, Xi'an, China.
  23. Jin-Guo Zhang: Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo, Beijing, China.
  24. Ye-Qin Yang: Fanjing Mountain National Nature Reserve, Guizhou, China.
  25. Cheng-Lin Zhang: Beijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo, Beijing, China.
  26. Yong-Cheng Long: Institue of Primatology and Human Evolution, Sun Yat-Sen University, Guangzhou, China.
  27. Hai-Shu Li: Nujiang Prefecture Forestry Bureau, Yunnan, China.
  28. Jing-Yuan Yang: Shennongjia National Nature Reserve, Hubei, China.
  29. David M Irwin: Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada.
  30. Oliver A Ryder: San Diego Zoo Institute for Conservation Research, Escondido, California, USA.
  31. Ying Li: Institute of Animal Genetics and Breeding, Sichuan Agricultural University, Ya'an, China.
  32. Chung-I Wu: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  33. Ya-Ping Zhang: State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
PMID: 27399969 DOI: 10.1038/ng.3615

Abstract

The snub-nosed monkey genus Rhinopithecus includes five closely related species distributed across altitudinal gradients from 800 to 4,500 m. Rhinopithecus bieti, Rhinopithecus roxellana, and Rhinopithecus strykeri inhabit high-altitude habitats, whereas Rhinopithecus brelichi and Rhinopithecus avunculus inhabit lowland regions. We report the de novo whole-genome sequence of R. bieti and genomic sequences for the four other species. Eight shared substitutions were found in six genes related to lung function, DNA repair, and angiogenesis in the high-altitude snub-nosed monkeys. Functional assays showed that the high-altitude variant of CDT1 (Ala537Val) renders cells more resistant to UV irradiation, and the high-altitude variants of RNASE4 (Asn89Lys and Thr128Ile) confer enhanced ability to induce endothelial tube formation in vitro. Genomic scans in the R. bieti and R. roxellana populations identified signatures of selection between and within populations at genes involved in functions relevant to high-altitude adaptation. These results provide valuable insights into the adaptation to high altitude in the snub-nosed monkeys.

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MeSH Term

Adaptation, Physiological
Amino Acid Sequence
Animals
Colobinae
Genetic Markers
Genome
Genomics
Phylogeny
Sequence Homology, Amino Acid

Chemicals

Genetic Markers
Journal Article Research Support, Non-U.S. Gov't
Article has an altmetric score of 83

Word Cloud

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