Biodiversity and Conservation

, Volume 27, Issue 9, pp 2275–2291 | Cite as

Population genetic analyses of the endangered alpine Sinadoxa corydalifolia (Adoxaceae) provide insights into future conservation

  • Yaling Wang
  • Qianlong Liang
  • Guoqian Hao
  • Chunlin Chen
  • Jianquan Liu
Original Paper


With increasing temperature and anthropogenic activity, endangered alpine species in the high altitudes of the Qinghai-Tibet Plateau face high risk of extinction; however, they have received little attention in the past. In this study, we used 12 nuclear and nine chloroplast microsatellites (simple sequence repeats, SSR) to assess genetic diversity within and among the only two populations of the highly endangered alpine species Sinadoxa corydalifolia (Adoxaceae). We identified only one individual exhibiting clonal reproduction across all 160 extant plants. The levels of genetic variability were estimated to be very low, with the allele number Na = 3.2 and the expected heterozygosity He = 0.368. The genetic differentiation is extremely high between the two regional populations (FST = 0.214), with a limited rate of gene flow in the recent past. In addition, numerous endemic alleles were found for each subpopulation within each population. Our analyses suggest that it is critical not only to conserve all surviving individuals of the two populations in situ but also to mediate gene flow artificially between subpopulations within each population in this endangered species.


Sinadoxa corydalifolia Qinghai-Tibet Plateau Endangered species nSSR cpSSR Population structure Genetic diversity 



This work was supported by grants from National key research and development program (2017YFC0505203) and the National Natural Science Foundation of China (Grant Numbers 31590821). We thank Dr Quanjun Hu for conducting all estimations.

Supplementary material

10531_2018_1537_MOESM1_ESM.docx (42 kb)
Supplementary material 1 (DOCX 42 kb)


  1. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709. CrossRefPubMedGoogle Scholar
  2. Amos W, Hoffman JI, Frodsham A, Zhang L, Best S, Avs H (2007) Automated binning of microsatellite alleles: problems and solutions. Mol Ecol Notes 7:10–14. CrossRefGoogle Scholar
  3. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37. CrossRefPubMedGoogle Scholar
  4. Beaumont MA, Bruford MW (1999) Microsatellites in conservation genetics. In: Goldstein DB, Schlotterer C (eds) Microsatellites: evolution and applications. Oxford University Press, Oxford, pp 165–182Google Scholar
  5. Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345. CrossRefPubMedGoogle Scholar
  6. Boufford DE (2014) Biodiversity hotspot: China’s Hengduan Mountains. Arnoldia 72:24–35Google Scholar
  7. Brinkmann B, Klintschar M, Neuhuber F, Hühne J, Rolf B (1998) Mutation rate in human microsatellites: influence of the structure and length of the tandem repeat. Am J Hum Genet 62:1408–1415. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Casas-Marce M, Soriano L, López-Bao JV, Godoy JA (2013) Genetics at the verge of extinction: insights from the Iberian lynx. Mol Ecol 22:5503–5515. CrossRefPubMedGoogle Scholar
  9. Charlebois D, Byers PL, Finn CE, Thomas AL (2010) Elderberry: botany, horticulture, potential. Horticult Rev 37:213–280Google Scholar
  10. Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504. CrossRefPubMedGoogle Scholar
  11. Dean D (2014) Assessing the genetic diversity of the genus Viburnum using simple sequence repeats. Dissertation, University of TennesseeGoogle Scholar
  12. Diffenbaugh NS, Giorgi F (2012) Climate change hotspots in the CMIP5 global climate model ensemble. Clim Chang 114:813–822. CrossRefGoogle Scholar
  13. Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B (2014) Defaunation in the Anthropocene. Science 345:401–406. CrossRefPubMedGoogle Scholar
  14. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  15. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. CrossRefGoogle Scholar
  16. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611. CrossRefPubMedGoogle Scholar
  17. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50. CrossRefGoogle Scholar
  18. Falush D, Stephens M, Pritchard J (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedPubMedCentralGoogle Scholar
  19. Frankham R, Ballou JD, Briscoe DA (2002) Introduction of conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  20. Garner BA et al (2016) Genomics in conservation: case studies and bridging the gap between data and application. Trends Ecol Evol 31:81–83. CrossRefPubMedGoogle Scholar
  21. Ge XJ, Zhang LB, Yuan YM, Hao G, Chiang TY (2005) Strong genetic differentiation of the East-Himalayan Megacodon stylophorus (Gentianaceae) detected by inter-simple sequence repeats (ISSR). Biodivers Conserv 14:849–861. CrossRefGoogle Scholar
  22. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486. CrossRefGoogle Scholar
  23. Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hamrick JL, Godt MJW (1996) Conservation genetics of endemic plant species. In: Avise JC, Hamrick JL (eds) Conservation genetics. Chapman and Hall, New York, pp 281–304CrossRefGoogle Scholar
  25. Harrisson KA, Pavlova A, Telonis-Scott M, Sunnucks P (2014) Using genomics to characterize evolutionary potential for conservation of wild populations. Evol Appl 7:1008–1025. CrossRefPubMedPubMedCentralGoogle Scholar
  26. He YJ, Cui GF, Feng ZW, Zheng J, Dong JS, Li YB (2004) Conservation priorities for plant species of forest-meadow ecotone in Sanjiangyuan Nature Reserve. J Appl Ecol 15:1307–1312Google Scholar
  27. He YQ, Lu AG, Zhang ZL, Pang HX, Zhao JD (2005) Seasonal variation in the regional structure of warming across China in the past half century. Clim Res 28:213–219. CrossRefGoogle Scholar
  28. Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162. CrossRefGoogle Scholar
  29. Holmes DS (2005) Sexual reproduction in British populations of Adoxa moschatellina L. Watsonia 25:265–273Google Scholar
  30. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106. CrossRefPubMedGoogle Scholar
  31. Kullan ARK, Kulkarni AV, Kumar RS, Rajkumar R (2016) Development of microsatellite markers and their use in genetic diversity and population structure analysis in Casuarina. Tree Genet Genomes 12:49. CrossRefGoogle Scholar
  32. Li XL, Li SC, Chu HJ, Li ZZ, Chen YY (2013) Genetic diversity and population structure of the endangered alpine quillwort Isoetes hypsophila (Isoetaceae) revealed by SSR analysis. Biochem Syst Ecol 47:11–20. CrossRefGoogle Scholar
  33. Liang HX, Wu CY (1995) On the taxonomic system, phylogeny and distrbution in Adoxaceae. Acta Botanica Yunnanica 17:380–390Google Scholar
  34. Liu JQ, Ho TN, Zhou GY, Lu AM (1999) Karyomorphology of Sinadoxa (Adoxaceae) and its systematic significance. Caryologia 52:159–164CrossRefGoogle Scholar
  35. Liu JQ, Chen ZD, Lu AM (2000) The phylogenetic relationships of Sinadoxa, revealed by the ITS data. Acta Bot Sin 42:656–658Google Scholar
  36. Liu JM, Wang L, Geng YP, Wang QB, Luo LJ, Zhong Y (2006) Genetic diversity and population structure of Lamiophlomis rotata (Lamiaceae), an endemic species of Qinghai-Tibet Plateau. Genetica 128:385–394. CrossRefPubMedGoogle Scholar
  37. Liu JQ, Duan YW, Hao G, Ge XJ, Sun H (2014) Evolutionary history and underlying adaptation of alpine plants on the Qinghai-Tibet Plateau. J Syst Evol 52:241–249CrossRefGoogle Scholar
  38. López-Pujol J, Zhang FM, Sun HQ, Ying TS, Ge S (2011) Centres of plant endemism in China: places for survival or for speciation? J Biogeogr 38:1267–1280. CrossRefGoogle Scholar
  39. Mao KS, Yao XL, Huang ZH (2005) Molecular phylogeny and species speciation of Adoxaceae.s.s. Acta Botanica Yunnanica 27:620–628Google Scholar
  40. Mccauley DE (1995) The use of chloroplast DNA polymorphism in studies of gene flow in plants. Trends Ecol Evol 10:198–202. CrossRefPubMedGoogle Scholar
  41. Miraldo A et al (2016) An Anthropocene map of genetic diversity. Science 353:1532–1535. CrossRefPubMedGoogle Scholar
  42. Ouborg NJ, Vergeer P, Mix C (2006) The rough edges of the conservation genetics paradigm for plants. J Ecol 94:1233–1248. CrossRefGoogle Scholar
  43. Paetkau D, Strobeck C (1995) The molecular basis and evolutionary history of a microsatellite null allele in bears. Mol Ecol 4:519–520. CrossRefPubMedGoogle Scholar
  44. Palmer JD, Jansen RK, Michaels HJ, Chase MW, Manhart JR (1988) Chloroplast DNA variation and plant phylogeny. Ann Mo Bot Gard 75:1180–1206. CrossRefGoogle Scholar
  45. Pauwels M, Vekemans X, Godé C, Frérot H, Castric V, Saumitou-Laprade P (2012) Nuclear and chloroplast DNA phylogeography reveals vicariance among European populations of the model species for the study of metal tolerance, Arabidopsis halleri (Brassicaceae). New Phytol 193:916–928. CrossRefPubMedGoogle Scholar
  46. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Report 15:8–15. CrossRefGoogle Scholar
  48. Powell W et al (1995) Hypervariable microsatellites provide a general source of polymorphic DNA markers for the chloroplast genome. Curr Biol 5:1023–1029. CrossRefPubMedGoogle Scholar
  49. Powell W, Machray GC, Provan J (1996) Polymorphism revealed by simple sequence repeats. Trends Plant Sci 1:215–222. CrossRefGoogle Scholar
  50. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  51. Prohens J, Anderson GJ, Herraiz FJ, Bernardello G, Santos-Guerra A, Crawford D, Nuez F (2007) Genetic diversity and conservation of two endangered eggplant relatives (Solanum vespertilio Aiton and Solanum lidii Sunding) endemic to the Canary Islands. Genet Resour Crop Evol 54:451–464. CrossRefGoogle Scholar
  52. Provan J, Corbett G, Mcnicol JW, Powell W (1997) Chloroplast DNA variability in wild and cultivated rice (Oryza spp.) revealed by polymorphic chloroplast simple sequence repeats. Genome 40:104. CrossRefPubMedGoogle Scholar
  53. Provan J, Powell W, Hollingsworth PM (2001) Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol Evol 16:142–147. CrossRefPubMedGoogle Scholar
  54. Qi WC, Lin F, Liu YH, Huang BQ, Cheng JH, Zhang W, Zhao H (2016) High-throughput development of simple sequence repeat markers for genetic diversity research in Crambe abyssinica. BMC Plant Biol 16:139. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Segelbacher G et al (2010) Applications of landscape genetics in conservation biology: concepts and challenges. Conserv Genet 11:375–385. CrossRefGoogle Scholar
  56. Silva LCR, Sun G, Zhu-Barker X, Liang QL, Wu N, Horwath WR (2016) Tree growth acceleration and expansion of alpine forests: the synergistic effect of atmospheric and edaphic change. Sci Adv 2:8. CrossRefGoogle Scholar
  57. Sosa PA, González-Pérez MA, Moreno C, Clarke JB (2010) Conservation genetics of the endangered endemic Sambucus palmensis Link (Sambucaceae) from the Canary Islands. Conserv Genet 11:2357–2368. CrossRefGoogle Scholar
  58. Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87:173–180. CrossRefGoogle Scholar
  59. Sun XD, Yu XH, Zhou SM, Liu SQ (2016) De novo assembly and characterization of the Welsh onion (Allium fistulosum L.) transcriptome using Illumina technology. Mol Genet Genomics 291:647–659. CrossRefPubMedGoogle Scholar
  60. Tian H, Kang M, Li L, Yao XH, Huang HW (2009) Genetic diversity in natural populations of Castanea mollissima inferred from nuclear SSR markers. Biodivers Sci 17:296–302. CrossRefGoogle Scholar
  61. Turnpenny P, Ellard S (2012) Emery’s elements of medical genetics, 14th edn. Churchill Livingstone, LondonGoogle Scholar
  62. Wang H, Pan G, Ma QG, Zhang JP, Pei D (2015) The genetic diversity and introgression of Juglans regia and Juglans sigillata in Tibet as revealed by SSR markers. Tree Genet Genome 11:804. Google Scholar
  63. Wang YL, Guo XY, Hao GQ, Wang TJ, Wang K (2016) The complete chloroplast genome of Sinadoxa corydalifolia (Adoxaceae). Conserv Genet Resour 8:303–305. CrossRefGoogle Scholar
  64. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. PubMedGoogle Scholar
  65. Wu CY (1987) Flora of Tibet, vol 5. Science Press, BeijingGoogle Scholar
  66. Wu CY (1988) Hengduan Mountain flora and her significance. Journal of Japanese Botany 63:297–311Google Scholar
  67. Wu CY, Wu ZL, Huang RF (1981) Sinadoxa C.Y.Wu, Z.L.Wu et R.F.Huang, genus novum familiae Adoxacearum. Acta Phytotaxon Sin 19:203–210Google Scholar
  68. Wu SG, Yang YP, Fei Y (1995) On the flora of the alpine region in the Qinghai-Xizang (Tibet) Plateau. Acta Botanica Yunnanica 17:233–250Google Scholar
  69. Zhang GL, Zhang YJ, Dong JW, Xiao XM (2013) Green-up dates in the Tibetan Plateau have continuously advanced from 1982 to 2011. Proc Natl Acad Sci USA 110:4309–4314. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Zheng W, Wang LY, Meng LH, Liu JQ (2008) Genetic variation in the endangered Anisodus tanguticus (Solanaceae), an alpine perennial endemic to the Qinghai-Tibetan Plateau. Genetica 132:123–129. CrossRefPubMedGoogle Scholar
  71. Zhu ZC et al (2016) Greening of the Earth and its drivers. Nat Clim Chang 6:791–795. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Yaling Wang
    • 1
    • 2
  • Qianlong Liang
    • 1
  • Guoqian Hao
    • 3
  • Chunlin Chen
    • 1
  • Jianquan Liu
    • 1
  1. 1.Key Laboratory of Bio-resource and Eco-environment of Ministry of Education, College of Life SciencesSichuan UniversityChengduChina
  2. 2.College of Life Science and EngineeringNorthwest Minzu UniversityLanzhouChina
  3. 3.Biodiversity Institute of Mount Emei, Mount Emei Scenic Area Management CommitteeLeshanChina

Personalised recommendations