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Conservation genomics of the critically endangered Chinese pangolin

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Abstract

The Chinese pangolin (Manis pentadactyla, MP) has been extensively exploited and is now on the brink of extinction, but its population structure, evolutionary history, and adaptive potential are unclear. Here, we analyzed 94 genomes from three subspecies of the Chinese pangolin and identified three distinct genetic clusters (MPA, MPB, and MPC), with MPB further divided into MPB1 and MPB2 subpopulations. The divergence of these populations was driven by past climate change. For MPB2 and MPC, recent human activities have caused dramatic population decline and small population size as well as increased inbreeding, but not decrease in genomic variation and increase in genetic load probably due to strong gene flow; therefore, it is crucial to strengthen in situ habitat management for these two populations. By contrast, although human activities have a milder impact on MPA, it is at high risk of extinction due to long-term contraction and isolation, and genetic rescue is urgently needed. MPB1 exhibited a relatively healthy population status and can potentially serve as a source population. Overall, our findings provide novel insights into the conservation of the Chinese pangolin and biogeography of the mammals of eastern Asia.

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Data availability

The raw whole genome resequencing reads have been deposited in the CNGB Sequence Archive of China National GeneBank DataBase (CNGBdb) (accession number: CNP0001723).

References

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Challender, D.W.S., Harrop, S.R., and MacMillan, D.C. (2015). Understanding markets to conserve trade-threatened species in CITES. Biol Conservation 187, 249–259.

    Article  Google Scholar 

  • Challender, D.W., and Hywood, L. (2011). Asian pangolins: increasing affluence driving hunting pressure. Traffic Bull 23, 92–93.

    Google Scholar 

  • Challender, D.W., Nash, H.C., and Waterman, C. (2019). Pangolins: Science, Society and Conservation. London: Academic Press.

    Google Scholar 

  • Chen, S., Zhou, Y., Chen, Y., and Gu, J. (2018). fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng, F., Tian, J., He, J., He, H., Liu, G., Zhang, Z., and Zhou, L. (2023). The spatial and temporal distribution of China’s forest carbon. Front Ecol Evol 11, 1110594.

    Article  Google Scholar 

  • Cingolani, P., Platts, A., Wang, L.L., Coon, M., Nguyen, T., Wang, L., Land, S.J., Lu, X., and Ruden, D.M. (2012). A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly 6, 80–92.

    Article  CAS  PubMed  Google Scholar 

  • Danecek, P., Auton, A., Abecasis, G., Albers, C.A., Banks, E., DePristo, M.A., Handsaker, R.E., Lunter, G., Marth, G.T., Sherry, S.T., et al. (2011). The variant call format and VCFtools. Bioinformatics 27, 2156–2158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Do, C., Waples, R.S., Peel, D., Macbeth, G.M., Tillett, B.J., and Ovenden, J.R. (2014). NEESTIMATOR v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resources 14, 209–214.

    Article  CAS  Google Scholar 

  • Do, R., Balick, D., Li, H., Adzhubei, I., Sunyaev, S., and Reich, D. (2015). No evidence that selection has been less effective at removing deleterious mutations in Europeans than in Africans. Nat Genet 47, 126–131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dobrynin, P., Liu, S., Tamazian, G., **ong, Z., Yurchenko, A.A., Krasheninnikova, K., Kliver, S., Schmidt-Küntzel, A., Koepfli, K.P., Johnson, W., et al. (2015). Genomic legacy of the African cheetah, Acinonyx jubatus. Genome Biol 16, 1–20.

    Article  Google Scholar 

  • Durand, E.Y., Patterson, N., Reich, D., and Slatkin, M. (2011). Testing for ancient admixture between closely related populations. Mol Biol Evol 28, 2239–2252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edge, P., and Bansal, V. (2019). Longshot enables accurate variant calling in diploid genomes from single-molecule long read sequencing. Nat Commun 10, 4660.

    Article  PubMed  PubMed Central  Google Scholar 

  • Excoffier, L., and Foll, M. (2011). Fastsimcoal: a continuous-time coalescent simulator of genomic diversity under arbitrarily complex evolutionary scenarios. Bioinformatics 27, 1332–1334.

    Article  CAS  PubMed  Google Scholar 

  • Fu, J., and Wen, L. (2023). Impacts of Quaternary glaciation, geological history and geography on animal species history in continental East Asia: a phylogeographic review. Mol Ecol 32, 4497–4514.

    Article  PubMed  Google Scholar 

  • Harris, R.S. (2007). Improved pairwise alignment of genomic DNA. State College: The Pennsylvania State University.

    Google Scholar 

  • Hahn, C., Bachmann, L., and Chevreux, B. (2013). Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative map** approach. Nucleic Acids Res 41, e129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hijmans, R.J. (2015). Raster: Geographic data analysis and modeling. R Package Version 2.4-15.

  • Heinrich, S., Wittmann, T.A., Prowse, T.A.A., Ross, J.V., Delean, S., Shepherd, C.R., and Cassey, P. (2016). Where did all the pangolins go? International CITES trade in pangolin species. Glob Ecol Conserv 8, 241–253.

    Google Scholar 

  • Hohenlohe, P.A., Funk, W.C., and Rajora, O.P. (2021). Population genomics for wildlife conservation and management. Mol Ecol 30, 62–82.

    Article  PubMed  Google Scholar 

  • Hu, J.Y., Hao, Z.Q., Frantz, L., Wu, S.F., Chen, W., Jiang, Y.F., Wu, H., Kuang, W.M., Li, H., Zhang, Y.P., et al. (2020a). Genomic consequences of population decline in critically endangered pangolins and their demographic histories. Natl Sci Rev 7, 798–814.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu, Y., Thapa, A., Fan, H., Ma, T., Wu, Q., Ma, S., Zhang, D., Wang, B., Li, M., Yan, L., et al. (2020b). Genomic evidence for two phylogenetic species and long-term population bottlenecks in red pandas. Sci Adv 6, eaax5751.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu, Y., Wang, X., Xu, Y., Yang, H., Tong, Z., Tian, R., Xu, S., Yu, L., Guo, Y., Shi, P., et al. (2023). Molecular mechanisms of adaptive evolution in wild animals and plants. Sci China Life Sci 66, 453–495.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kardos, M., Åkesson, M., Fountain, T., Flagstad, Ø, Liberg, O., Olason, P., Sand, H., Wabakken, P., Wikenros, C., and Ellegren, H. (2018). Genomic consequences of intensive inbreeding in an isolated wolf population. Nat Ecol Evol 2, 124–131.

    Article  PubMed  Google Scholar 

  • Kirin, M., McQuillan, R., Franklin, C.S., Campbell, H., McKeigue, P.M., and Wilson, J. F. (2010). Genomic runs of homozygosity record population history and consanguinity. PLoS ONE 5, e13996.

    Article  PubMed  PubMed Central  Google Scholar 

  • Klein Goldewijk, K., Beusen, A., Doelman, J., and Stehfest, E. (2017). Anthropogenic land use estimates for the Holocene-HYDE 3.2. Earth Syst Sci Data 9, 927–953.

    Article  Google Scholar 

  • Knaus, B.J., and Grünwald, N.J. (2017). VCFR: a package to manipulate and visualize variant call format data in R. Mol Ecol Resources 17, 44–53.

    Article  CAS  Google Scholar 

  • Kondrashov, A.S., and Crow, J.F. (1993). A molecular approach to estimating the human deleterious mutation rate. Hum Mutat 2, 229–234.

    Article  CAS  PubMed  Google Scholar 

  • Kuang, W., Ming, C., Li, H., Wu, H., Frantz, L., Roos, C., Zhang, Y., Zhang, C., Jia, T., and Yang, J.Y. (2019). The origin and population history of the endangered golden snub-nosed monkey (Rhinopithecus roxellana). Mol Biol Evol 36, 487–499.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35, 1547.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kyriazis, C.C., Wayne, R.K., and Lohmueller, K.E. (2021). Strongly deleterious mutations are a primary determinant of extinction risk due to inbreeding depression. Evol Lett 5, 33–47.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., and Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079.

    Article  PubMed  PubMed Central  Google Scholar 

  • Librado, P., and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.

    Article  CAS  PubMed  Google Scholar 

  • Liu, X., and Fu, Y.X. (2015). Exploring population size changes using SNP frequency spectra. Nat Genet 47, 555–559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu, H.Y., Yi, S.W., Xu, Z.W., Zhou, Y.L., Zeng, L., Zhu, F.Y., Feng, H., Dong, L.N., Zhuo, H.X., Yu, K.F., et al. (2013). Chinese deserts and sand fields in Last Glacial Maximum and Holocene Optimum. Chin Sci Bull 58, 2775–2783.

    Article  CAS  Google Scholar 

  • McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al. (2010). The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res 20, 1297–1303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mills, L.S., and Allendorf, F.W. (1996). The one-migrant-per-generation rule in conservation and management. Conserv Biol 10, 1509–1518.

    Article  Google Scholar 

  • Muscarella, R., Galante, P.J., Soley-Guardia, M., Boria, R.A., Kass, J.M., Uriarte, M., and Anderson, R.P. (2014). ENM eval: an R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods Ecol Evol 5, 1198–1205.

    Article  Google Scholar 

  • Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B., and Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.

    Article  CAS  PubMed  Google Scholar 

  • Nigenda-Morales, S.F., Lin, M., Nuñez-Valencia, P.G., Kyriazis, C.C., Beichman, A.C., Robinson, J.A., Ragsdale, A.P., Urbán R., J., Archer, F.I., Viloria-Gómora, L., et al. (2023). The genomic footprint of whaling and isolation in fin whale populations. Nat Commun 14, 5465.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patterson, N., Moorjani, P., Luo, Y., Mallick, S., Rohland, N., Zhan, Y., Genschoreck, T., Webster, T., and Reich, D. (2012). Ancient admixture in human history. Genetics 192, 1065–1093.

    Article  PubMed  PubMed Central  Google Scholar 

  • Phillips, S.J., Anderson, R.P., and Schapire, R.E. (2006). Maximum entropy modeling of species geographic distributions. Ecol Model 190, 231–259.

    Article  Google Scholar 

  • Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A.R., Bender, D., Maller, J., Sklar, P., de Bakker, P.I.W., Daly, M.J., et al. (2007). PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81, 559–575.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ralls, K., Ballou, J.D., Dudash, M.R., Eldridge, M.D.B., Fenster, C.B., Lacy, R.C., Sunnucks, P., and Frankham, R. (2018). Call for a paradigm shift in the genetic management of fragmented populations. Conserv Lett 11, e12412.

    Article  Google Scholar 

  • Robinson, J., Kyriazis, C.C., Yuan, S.C., and Lohmueller, K.E. (2023). Deleterious variation in natural populations and implications for conservation genetics. Annu Rev Anim Biosci 11, 93–114.

    Article  PubMed  Google Scholar 

  • Santiago, E., Novo, I., Pardiñas, A.F., Saura, M., Wang, J., and Caballero, A. (2020). Recent demographic history inferred by high-resolution analysis of linkage disequilibrium. Mol Biol Evol 37, 3642–3653.

    Article  CAS  PubMed  Google Scholar 

  • Sharma, H.P., Rimal, B., Zhang, M., Sharma, S., Poudyal, L.P., Maharjan, S., Kunwar, R., Kaspal, P., Bhandari, N., Baral, L., et al. (2020). Potential distribution of the critically endangered Chinese Pangolin (Manis pentadactyla) in different land covers of Nepal: implications for conservation. Sustainability 12, 1282.

    Article  Google Scholar 

  • Sun, X., Liu, Y.C., Tiunov, M.P., Gimranov, D.O., Zhuang, Y., Han, Y., Driscoll, C.A., Pang, Y., Li, C., Pan, Y., et al. (2023). Ancient DNA reveals genetic admixture in China during tiger evolution. Nat Ecol Evol 7, 1914–1929.

    Article  PubMed  Google Scholar 

  • Vaser, R., Adusumalli, S., Leng, S.N., Sikic, M., and Ng, P.C. (2016). SIFT missense predictions for genomes. Nat Protoc 11, 1–9.

    Article  CAS  PubMed  Google Scholar 

  • von Seth, J., Dussex, N., Diez-del-Molino, D., van der Valk, T., Kutschera, V.E., Kierczak, M., Steiner, C.C., Liu, S., Gilbert, M.T.P., Sinding, M.H.S., et al. (2021). Genomic insights into the conservation status of the world’s last remaining Sumatran rhinoceros populations. Nat Commun 12, 2393.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Q., Lan, T., Li, H., Sahu, S.K., Shi, M., Zhu, Y., Han, L., Yang, S., Li, Q., Zhang, L., et al. (2022). Whole-genome resequencing of Chinese pangolins reveals a population structure and provides insights into their conservation. Commun Biol 5, 821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei, S., Li, Z., Momigliano, P., Fu, C., Wu, H., and Merilä, J. (2020). The roles of climate, geography and natural selection as drivers of genetic and phenotypic differentiation in a widespread amphibian Hyla annectans (Anura: Hylidae). Mol Ecol 29, 3667–3683.

    Article  PubMed  Google Scholar 

  • Wei, F., Huang, G., Guan, D., Fan, H., Zhou, W., Wang, D., and Hu, Y. (2022a). Digital Noah’s Ark: last chance to save the endangered species. Sci China Life Sci 65, 2325–2327.

    Article  PubMed  Google Scholar 

  • Wei, S., Sun, S., Dou, H., An, F., Gao, H., Guo, C., and Hua, Y. (2022b). Influence of Pleistocene climate fluctuations on the demographic history and distribution of the critically endangered Chinese pangolin (Manis pentadactyla). BMC Zool 7, 1.

    Article  CAS  Google Scholar 

  • Willi, Y., Kristensen, T.N., Sgrò, C.M., Weeks, A.R., Ørsted, M., and Hoffmann, A.A. (2022). Conservation genetics as a management tool: the five best-supported paradigms to assist the management of threatened species. Proc Natl Acad Sci USA 119, e2105076119.

    Article  CAS  PubMed  Google Scholar 

  • Wu, S.B. (2004). Assessment of threatened status of Chinese Pangolin (Manis pentadactyla). Chin J Appl Environ Biol 10, 456–461.

    Google Scholar 

  • **ng, Y., and Ree, R.H. (2017). Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proc Natl Acad Sci USA 114, E3444–E3451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, J., Lee, S.H., Goddard, M.E., and Visscher, P.M. (2011). GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet 88, 76–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, L., Chen, M., Challender, D.W.S., Waterman, C., Zhang, C., Huo, Z., Liu, H., and Luan, X. (2018). Historical data for conservation: reconstructing range changes of Chinese pangolin (Manispentadactyla) in eastern China (1970–2016). Proc R Soc B 285, 20181084.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, L., Wei, F., Zhan, X., Fan, H., Zhao, P., Huang, G., Chang, J., Lei, Y., and Hu, Y. (2022). Evolutionary conservation genomics reveals recent speciation and local adaptation in threatened takins. Mol Biol Evol 39, msac111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, S., Lan, T., Zhang, Y., Wang, Q., Li, H., Dussex, N., Sahu, S.K., Shi, M., Hu, M., Zhu, Y., et al. (2023). Genomic investigation of the Chinese alligator reveals wild-extinct genetic diversity and genomic consequences of their continuous decline. Mol Ecol Resour 23, 294–311.

    Article  PubMed  Google Scholar 

  • Zhang, C., Dong, S., Xu, J., He, W., and Yang, T. (2019). PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics 35, 1786–1788.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, F., Wu, S., Zou, C., Wang, Q., Li, S., and Sun, R. (2016). A note on captive breeding and reproductive parameters of the Chinese pangolin, Manis pentadactyla Linnaeus, 1758. ZooKeys 618, 129–144.

    Article  Google Scholar 

  • Zhang, H., Miller, M.P., Yang, F., Chan, H.K., Gaubert, P., Ades, G., and Fischer, G.A. (2015). Molecular tracing of confiscated pangolin scales for conservation and illegal trade monitoring in Southeast Asia. Glob Ecol Conserv 4, 414–422.

    Google Scholar 

  • Zhang, M., Cao, P., Dai, Q.Y., Wang, Y.Q., Feng, X.T., Wang, H.R., Wu, H., Min-Shan Ko, A., Mao, X.W., Liu, Y.C., et al. (2021). Comparative analysis of DNA extraction protocols for ancient soft tissue museum samples. Zoological Res 42, 280–286.

    Article  Google Scholar 

  • Zhao, S., Zheng, P., Dong, S., Zhan, X., Wu, Q., Guo, X., Hu, Y., He, W., Zhang, S., Fan, W., et al. (2013). Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nat Genet 45, 67–71.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, B., Xu, Q., and Shen, Y. (2002). The relationship between climate change and Quaternary glacial cycles on the Qinghai-Tibetan Plateau: review and speculation. Quat Int 97–98, 93–101.

    Article  Google Scholar 

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Acknowledgement

This work was supported by the Major Program of the Natural Science Foundation of Jiangxi Province of China (20233ACB209001), Guangdong Basic and Applied Basic Research Foundation (2022A1515111016), Science and Technology Department of Guangdong Province (2021QN02H103), Natural Resources Affairs Management-Ecological Forestry Construction Special Project of Forestry Administration of Guangdong Province (SLYJ2023B4002, SLYJ2023B4003, SLYJ2023B4005). We express sincere thanks to the Department of Wildlife Conservation of Forestry Administration of Guangdong Province for their support during the project implementation. We are also grateful to ** Huang & Fuwen Wei

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    Correspondence to Fuwen Wei.

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    The author(s) declare that they have no conflict of interest. F.Wei. conceived and supervised the project. S.Wei., H.Fan., W.Zhou., G.Huang., Y.Hua., S.Wu., X.Wei. and Y.Chen. collected the samples. X.Tan. carried out the DNA extraction and library construction. S.Wei. performed the bioinformatics analysis. S.Wei. wrote the manuscript. F.Wei., H.Fan., W.Zhou., S.Wei. revised the manuscript. All authors contributed to interpreting the data and approved the final manuscript.

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    Wei, S., Fan, H., Zhou, W. et al. Conservation genomics of the critically endangered Chinese pangolin. Sci. China Life Sci. (2024). https://doi.org/10.1007/s11427-023-2540-y

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