Abstract
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.
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Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709. https://doi.org/10.1038/nrg2844
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. https://doi.org/10.1111/j.1471-8286.2006.01560.x
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Beaumont MA, Bruford MW (1999) Microsatellites in conservation genetics. In: Goldstein DB, Schlotterer C (eds) Microsatellites: evolution and applications. Oxford University Press, Oxford, pp 165–182
Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345. https://doi.org/10.1093/bioinformatics/bti803
Boufford DE (2014) Biodiversity hotspot: China’s Hengduan Mountains. Arnoldia 72:24–35
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. https://doi.org/10.1086/301869
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. https://doi.org/10.1111/mec.12498
Charlebois D, Byers PL, Finn CE, Thomas AL (2010) Elderberry: botany, horticulture, potential. Horticult Rev 37:213–280
Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504. https://doi.org/10.1038/sj.hdy.6800545
Dean D (2014) Assessing the genetic diversity of the genus Viburnum using simple sequence repeats. Dissertation, University of Tennessee
Diffenbaugh NS, Giorgi F (2012) Climate change hotspots in the CMIP5 global climate model ensemble. Clim Chang 114:813–822. https://doi.org/10.1007/s10584-012-0570-x
Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B (2014) Defaunation in the Anthropocene. Science 345:401–406. https://doi.org/10.1126/science.1251817
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 19:11–15
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. https://doi.org/10.1007/s12686-011-9548-7
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
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. https://doi.org/10.1177/117693430500100003
Falush D, Stephens M, Pritchard J (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Frankham R, Ballou JD, Briscoe DA (2002) Introduction of conservation genetics. Cambridge University Press, Cambridge
Garner BA et al (2016) Genomics in conservation: case studies and bridging the gap between data and application. Trends Ecol Evol 31:81–83. https://doi.org/10.1016/j.tree.2015.10.009
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. https://doi.org/10.1007/s10531-004-0655-6
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486. https://doi.org/10.1093/oxfordjournals.jhered.a111627
Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883
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 281–304
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. https://doi.org/10.1111/eva.12149
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 15:1307–1312
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. https://doi.org/10.3354/cr028213
Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162. https://doi.org/10.1146/annurev.ecolsys.31.1.139
Holmes DS (2005) Sexual reproduction in British populations of Adoxa moschatellina L. Watsonia 25:265–273
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. https://doi.org/10.1111/j.1365-294X.2010.04544.x
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. https://doi.org/10.1007/s11295-016-1009-8
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. https://doi.org/10.1016/j.bse.2012.10.014
Liang HX, Wu CY (1995) On the taxonomic system, phylogeny and distrbution in Adoxaceae. Acta Botanica Yunnanica 17:380–390
Liu JQ, Ho TN, Zhou GY, Lu AM (1999) Karyomorphology of Sinadoxa (Adoxaceae) and its systematic significance. Caryologia 52:159–164
Liu JQ, Chen ZD, Lu AM (2000) The phylogenetic relationships of Sinadoxa, revealed by the ITS data. Acta Bot Sin 42:656–658
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. https://doi.org/10.1007/s10709-006-7517-y
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 52:241–249
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. https://doi.org/10.1111/j.1365-2699.2011.02504.x
Mao KS, Yao XL, Huang ZH (2005) Molecular phylogeny and species speciation of Adoxaceae.s.s. Acta Botanica Yunnanica 27:620–628
Mccauley DE (1995) The use of chloroplast DNA polymorphism in studies of gene flow in plants. Trends Ecol Evol 10:198–202. https://doi.org/10.1016/S0169-5347(00)89052-7
Miraldo A et al (2016) An Anthropocene map of genetic diversity. Science 353:1532–1535. https://doi.org/10.1126/science.aaf4381
Ouborg NJ, Vergeer P, Mix C (2006) The rough edges of the conservation genetics paradigm for plants. J Ecol 94:1233–1248. https://doi.org/10.1111/j.1365-2745.2006.01167.x
Paetkau D, Strobeck C (1995) The molecular basis and evolutionary history of a microsatellite null allele in bears. Mol Ecol 4:519–520. https://doi.org/10.1111/j.1365-294X.1995.tb00248.x
Palmer JD, Jansen RK, Michaels HJ, Chase MW, Manhart JR (1988) Chloroplast DNA variation and plant phylogeny. Ann Mo Bot Gard 75:1180–1206. https://doi.org/10.2307/2399279
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. https://doi.org/10.1111/j.1469-8137.2011.04003.x
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. https://doi.org/10.1093/bioinformatics/bts460
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. https://doi.org/10.1007/BF02772108
Powell W et al (1995) Hypervariable microsatellites provide a general source of polymorphic DNA markers for the chloroplast genome. Curr Biol 5:1023–1029. https://doi.org/10.1016/S0960-9822(95)00206-5
Powell W, Machray GC, Provan J (1996) Polymorphism revealed by simple sequence repeats. Trends Plant Sci 1:215–222. https://doi.org/10.1016/1360-1385(96)86898-1
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
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. https://doi.org/10.1007/s10722-006-9174-5
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. https://doi.org/10.1139/g97-014
Provan J, Powell W, Hollingsworth PM (2001) Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol Evol 16:142–147. https://doi.org/10.1016/S0169-5347(00)02097-8
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. https://doi.org/10.1186/s12870-016-0828-y
Segelbacher G et al (2010) Applications of landscape genetics in conservation biology: concepts and challenges. Conserv Genet 11:375–385. https://doi.org/10.1007/s10592-009-0044-5
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. https://doi.org/10.1126/sciadv.1501302
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. https://doi.org/10.1007/s10592-010-0122-8
Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87:173–180. https://doi.org/10.1016/S0006-3207(98)00066-4
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. https://doi.org/10.1007/s00438-015-1131-6
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. https://doi.org/10.3724/SP.J.1003.2009.09043
Turnpenny P, Ellard S (2012) Emery’s elements of medical genetics, 14th edn. Churchill Livingstone, London
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. https://doi.org/10.1007/s11295-014-0804-3
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. https://doi.org/10.1007/s12686-016-0559-2
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. https://doi.org/10.1111/j.1558-5646.1984.tb05657.x
Wu CY (1987) Flora of Tibet, vol 5. Science Press, Beijing
Wu CY (1988) Hengduan Mountain flora and her significance. Journal of Japanese Botany 63:297–311
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 19:203–210
Wu SG, Yang YP, Fei Y (1995) On the flora of the alpine region in the Qinghai-Xizang (Tibet) Plateau. Acta Botanica Yunnanica 17:233–250
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. https://doi.org/10.1073/pnas.1210423110
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. https://doi.org/10.1007/s10709-007-9154-5
Zhu ZC et al (2016) Greening of the Earth and its drivers. Nat Clim Chang 6:791–795. https://doi.org/10.1038/nclimate3004
Acknowledgements
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.
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Wang, Y., Liang, Q., Hao, G. et al. Population genetic analyses of the endangered alpine Sinadoxa corydalifolia (Adoxaceae) provide insights into future conservation. Biodivers Conserv 27, 2275–2291 (2018). https://doi.org/10.1007/s10531-018-1537-7
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DOI: https://doi.org/10.1007/s10531-018-1537-7