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Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation


The panda lineage dates back to the late Miocene1 and ultimately leads to only one extant species, the giant panda (Ailuropoda melanoleuca). Although global climate change and anthropogenic disturbances are recognized to shape animal population demography2,3 their contribution to panda population dynamics remains largely unknown. We sequenced the whole genomes of 34 pandas at an average 4.7-fold coverage and used this data set together with the previously deep-sequenced panda genome4 to reconstruct a continuous demographic history of pandas from their origin to the present. We identify two population expansions, two bottlenecks and two divergences. Evidence indicated that, whereas global changes in climate were the primary drivers of population fluctuation for millions of years, human activities likely underlie recent population divergence and serious decline. We identified three distinct panda populations that show genetic adaptation to their environments. However, in all three populations, anthropogenic activities have negatively affected pandas for 3,000 years.

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Figure 1: Current geographic populations of the giant panda and inferred genetic populations.
Figure 2: Demographic history of the giant panda reconstructed from the reference and population resequencing genomes.
Figure 3: Annotation of genes containing selected SNPs on the basis of the KEGG database.

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  1. Qiu, Z. & Qi, G. Ailuropoda found from the late Miocene deposits in Lufeng, Yunnan. Vertebrata Palasiatica 27, 153–169 (1989).

    Google Scholar 

  2. Root, T.L. & Schneider, S.H. Ecology and climate: research strategies and implications. Science 269, 334–341 (1995).

    CAS  Article  Google Scholar 

  3. Hewitt, G. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913 (2000).

    CAS  Article  Google Scholar 

  4. Li, R. et al. The complete genome sequence of the giant panda. Nature 463, 311–317 (2010).

    CAS  Article  Google Scholar 

  5. State Forestry Administration. The 3rd National Survey Report on Giant Panda in China (Science Press, Beijing, 2006).

  6. Yi, X. et al. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329, 75–78 (2010).

    CAS  Article  Google Scholar 

  7. Tang, H., Peng, J., Wang, P. & Risch, N.J. Estimation of individual admixture: analytical and study design considerations. Genet. Epidemiol. 28, 289–301 (2005).

    Article  Google Scholar 

  8. Alexander, D.H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009).

    CAS  Article  Google Scholar 

  9. Zhang, B. et al. Genetic viability and population history of the giant panda, putting an end to the ''Evolutionary Dead End''? Mol. Biol. Evol. 24, 1801–1810 (2007).

    CAS  Article  Google Scholar 

  10. Weir, B.S. & Cockerham, C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358 (1984).

    CAS  Google Scholar 

  11. Patterson, N., Price, A.L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).

    Article  Google Scholar 

  12. The Bovine HapMap Consortium. Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science 324, 528–532 (2009).

  13. Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011).

    CAS  Article  Google Scholar 

  14. Wang, J. On the taxonomic status of species, geological distribution and evolutionary history of Ailuropoda. Acta Zool. Sinica 20, 191–201 (1974).

    Google Scholar 

  15. Sun, Y.B. & An, Z.S. Late Pliocene-Pleistocene changes in mass accumulation rates of eolian deposits on the central Chinese Loess Plateau. J. Geophys. Res. 110, D23101 (2005).

    Article  Google Scholar 

  16. Pei, W. Evolutionary history of giant pandas. Acta Zool. Sinica 20, 188–190 (1974).

    Google Scholar 

  17. Jin, C. et al. The first skull of the earliest giant panda. Proc. Natl. Acad. Sci. USA 104, 10932–10937 (2007).

    CAS  Article  Google Scholar 

  18. Zhao, H., Yang, J., Xu, H. & Zhang, J. Pseudogenization of the umami taste receptor gene Tas1r1 in the giant panda coincided with its dietary switch to bamboo. Mol. Biol. Evol. 27, 2669–2673 (2010).

    CAS  Article  Google Scholar 

  19. Zheng, B., Xu, Q. & Shen, Y. The relationship between climate change and Quaternary glacial cycles on the Qinghai-Tibetan Plateau: review and speculation. Quat. Int. 9798, 93–101 (2002).

    Article  Google Scholar 

  20. Hu, J. & Wei, F. Comparative ecology of giant pandas in the five mountain ranges of their distribution in China. in Giant Pandas: Biology and Conservation (eds. Lindburg, D. & Baragona, K.) 137–148 (University of California Press, London, 2004).

  21. Zhan, X., Zheng, Y., Wei, F., Bruford, M.W. & Jia, C. Molecular evidence for Pleistocene refugia at the eastern edge of the Tibetan Plateau. Mol. Ecol. 20, 3014–3026 (2011).

    Article  Google Scholar 

  22. Gutenkunst, R.N., Hernandez, R.D., Williamson, S.H. & Bustamante, C.D. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5, e1000695 (2009).

    Article  Google Scholar 

  23. Ren, G. & Beug, H.J. Mapping Holocene pollen data and vegetation of China. Quat. Sci. Rev. 21, 1395–1422 (2002).

    Article  Google Scholar 

  24. Ren, G. Decline of the mid-to-late Holocene forests in China: climatic change or human impact? J. Quaternary Sci. 15, 273–281 (2000).

    Article  Google Scholar 

  25. Ren, N. Illustrations and Annotations of Huayang Guo Zhi (Shanghai Ancient Books Publishing House, Shanghai, 1987).

  26. Excoffier, L. & Lischer, H.E.L. Arlequin suite ver3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).

    Article  Google Scholar 

  27. Beaumont, M.A. & Nichols, R.A. Evaluating loci for use in the genetic analysis of population structure. P. Roy. Soc. Lond. B. Bio. 263, 1619–1626 (1996).

    Article  Google Scholar 

  28. Foll, M. & Gaggiotti, O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180, 977–993 (2008).

    Article  Google Scholar 

  29. Cockerham, C.C. & Weir, B. Estimation of gene flow from F-statistics. Evolution 47, 855–863 (1993).

    PubMed  Google Scholar 

  30. Meyerhof, W. et al. The molecular receptive ranges of human TAS2R bitter taste receptors. Chem. Senses 35, 157–170 (2010).

    CAS  Article  Google Scholar 

  31. Sabeti, P.C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913–918 (2007).

    CAS  Article  Google Scholar 

  32. Schaller, G.B., Hu, J., Pan, W. & Zhu, J. The Giant Panda of Wolong (University of Chicago Press, Chicago, 1985).

  33. Pan, W. et al. A Chance for Lasting Survival (Beijing University Press, Beijing, 2001).

  34. Swaisgood, R.R. et al. Chemical communication in giant pandas. in Giant Pandas: Biology and Conservation (eds. Lindburg, D.G. & Baragona, K.) 106–120 (University of California Press, Berkeley, CA, 2004).

  35. Hagey, L. & MacDonald, E. Chemical cues identify gender and individuality in giant pandas (Ailuropoda melanoleuca). J. Chem. Ecol. 29, 1479–1488 (2003).

    CAS  Article  Google Scholar 

  36. Zhan, X. et al. Molecular censusing doubles giant panda population estimate in a key nature reserve. Curr. Biol. 16, R451–R452 (2006).

    CAS  Article  Google Scholar 

  37. Zhu, L. et al. Drastic reduction of the smallest and most isolated giant panda population: implications for conservation. Conserv. Biol. 24, 1299–1306 (2010).

    Article  Google Scholar 

  38. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    CAS  Article  Google Scholar 

  39. Tajima, F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Watterson, G.A. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256–276 (1975).

    CAS  Article  Google Scholar 

  41. Barrett, J.C. et al. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263–265 (2005).

    CAS  Article  Google Scholar 

  42. Wei, F. et al. A study on the life table of wild giant pandas. Acta Theriol. Sinica 9, 81–86 (1989).

    Google Scholar 

  43. Hwang, D.G. & Green, P. Bayesian Markov chain Monte Carlo sequence analysis reveals varying neutral substitution patterns in mammalian evolution. Proc. Natl. Acad. Sci. USA 101, 13994–14001 (2004).

    CAS  Article  Google Scholar 

  44. Storey, J.D. A direct approach to false discovery rates. J. R. Stat. Soc., B 64, 479–498 (2002).

    Article  Google Scholar 

  45. Huang, K., Whitlock, R., Press, M.C. & Scholes, J.D. Variation for host range within and among populations of the parasitic plant Striga hermonthica. Heredity 108, 96–104 (2012).

    CAS  Article  Google Scholar 

  46. Buckley, J., Butlin, R.K. & Bridle, J.R. Evidence for evolutionary change associated with the recent range expansion of the British butterfly, Aricia agestis, in response to climate change. Mol. Ecol. 21, 267–280 (2012).

    Article  Google Scholar 

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This study was supported by grants from the National Natural Science Foundation of China (31230011), the Knowledge Innovation Program of the Chinese Academy of Sciences (KSCX2-EW-Z-4) and the State Forestry Administration of China. We thank the Chongqing Zoo, the Fuzhou Research Center of the Giant Panda, the Shanghai Zoo, the Shanghai Wildlife Park and the Zhengzhou Zoo for assistance during sample collection. We acknowledge T. Meng for generation of the panda distribution map, R.N. Gutenkunst for suggestions on analysis with ∂a∂i, H. Li for suggestions on PSMC simulations and L. Goodman, J. Elser, M. Holyoak, S. Kumar and R.R. Swaisgood for comments and revisions of this manuscript. We also thank G. Tian, M. Jian, H. Jiang, M. Zhao, Q. Zhang, B. Wang, Y. Huang, G. Wang, C. Lin and F. Xi for laboratory assistance and B. Li for assistance on polar bear data analysis.

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Authors and Affiliations



F.W. designed the research and interpreted data. Jun Wang led the genome sequencing and supervised the analysis. P.Z., S. Zhang, L.Z., H.Z., Z.Z., X.J. and J.Z. prepared the samples. S. Zhao, P.Z., X. Zhan, Y.H., Jian Wang and H.Y. performed research. S. Zhao, Q.W., S.D., X. Zhan, P.Z., X.G., W.H., W.F., D.L., X. Zhang and Q.C. analyzed the data. X. Zhan, F.W., P.Z., S. Zhao, Q.W. and S.D. wrote and revised the manuscript.

Corresponding authors

Correspondence to Jun Wang or Fuwen Wei.

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The authors declare no competing financial interests.

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Supplementary Figures 1–9, Supplementary Tables 1–14 and Supplementary Note (PDF 7812 kb)

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Zhao, S., Zheng, P., Dong, S. et al. Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nat Genet 45, 67–71 (2013).

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