Conservation genetic assessment of four plant species in a small replica of a steppe ecosystem >30 years after establishment

  • Christina Magdalena Müller
  • Björn Huwe
  • Volker Wissemann
  • Jasmin Joshi
  • Birgit Gemeinholzer
Original Paper

Abstract

To counter species loss living ex situ collections in botanic gardens became important elements of robust conservation programs. Several limitations, problems, and risks associated with living ex situ collections have been reported such as appropriate cultivation management to maintain genetic diversity and stochastic effects in small isolated populations in artificial habitats. However, not all small and isolated populations exhibit these predicted genetic changes. In a multi-species in situ/ex situ comparison of sand dune steppe- and grassland vegetation >30 years after the ex situ population establishment, we compared four different species’ population genetic diversities (Alyssum montanum ssp. gmelinii, Gypsophila fastigiata, Helianthemum nummularium ssp. obscurum, Onosma arenaria) by means of ISSR. We observed different species-specific genetic responses to quite similar abiotic selective forces concerning different neutral genetic diversities of wild versus botanic garden populations. The genetic divergence was kept relatively low in two of the four investigated species between the model steppe plant community within the botanic garden where human interference was kept at a minimum and the wild population. However, the moderate genetic divergence of the two other species kept under the same conditions highlights the importance of species-specific intrinsic responses and stochastic effects to ecosystem changes and provides data on population genetic dynamics in small and isolated populations. This contributes to further improve recommendations on how to best conserve endangered plant species in ex situ environments (cultivation in near nature-like replicas of the original site with as little human inference as possible over only certain periods of time, >30 years).

Keywords

Ex situ/in situ population genetic comparison ISSR Conservation genetics Sand dune steppe- and grassland vegetation Botanic gardens 

References

  1. Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188. doi:10.1111/j.1365-294X.2008.03971.x CrossRefPubMedGoogle Scholar
  2. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA, Fay JC (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3:e3376. doi:10.1371/journal.pone.0003376 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Basey AC, Fant JB, Kramer AT (2015) Producing native plant materials for restoration: 10 rules to collect and maintain genetic diversity. Native Plants Journal 16:37–53. doi:10.3368/npj.16.1.37 CrossRefGoogle Scholar
  4. BNatSchG (2009) Bundesnaturschutzgesetz (Gesetz über Naturschutz und Landschaftspflege) Artikel 1 des Gesetzes vom 29.07.2009 (BGBl. I S. 2542), in Kraft getreten am 01.03.2010 zuletzt geändert durch Gesetz vom 13.10.2016 (BGBl. I S. 2258) m.W.v. 01.01.2017Google Scholar
  5. Boyce MS (1992) Population viability analysis. Annu Rev Ecol Syst 23:481–506CrossRefGoogle Scholar
  6. Brouwer W, Stählin A (1955) Handbuch der Samenkunde. DLG-Verlag, Frankfurt am MainGoogle Scholar
  7. Brütting C, Hensen I, Wesche K (2013) Ex situ cultivation affects genetic structure and diversity in arable plants. Plant Biol 15:505–513. doi:10.1111/j.1438-8677.2012.00655.x CrossRefPubMedGoogle Scholar
  8. Cardle L, Ramsay L, Milbourne D, Macaulay M, Marshall D, Waugh R (2000) Computational and experimental characterization of physically clustered simple sequence repeats in plants. Genetics 156:847–854. http://www.genetics.org/content/genetics/156/2/847.full.pdf
  9. Cibrian-Jaramillo A, Hird A, Oleas N, Ma H, Meerow AW, Francisco-Ortega J, Griffith MP (2013) What is the conservation value of a plant in a botanic garden?: using indicators to improve management of ex situ collections. Bot Rev 79:559–577. doi:10.1007/s12229-013-9120-0 CrossRefGoogle Scholar
  10. Cieślak E, Kaźmierczakowa R, Ronikier M (2010) Cochlearia polonica Fröhl. (Brassicaceae), a narrow endemic species of southern Poland: History of conservation efforts, overview of current population resources and genetic structure of populations. Acta Soc Bot Pol 79:255–261. https://pbsociety.org.pl/journals/index.php/asbp/article/download/asbp.2010.033/179
  11. Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843. doi:10.1111/j.1365-294X.2006.02994.x CrossRefPubMedGoogle Scholar
  12. Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374PubMedPubMedCentralGoogle Scholar
  13. Crane PR, Hopper SD, Raven PH, Stevenson DW (2009) Plant science research in botanic gardens. Trends Plant Sci 14:575–577. doi:10.1016/j.tplants.2009.09.007 CrossRefPubMedGoogle Scholar
  14. Cruzan MB (2001) Population size and fragmentation tresholds for the maintenance of genetic diversity in the herbaceous endemic Scutellaria montana (Lamiaceae). Evol 55:1569CrossRefGoogle Scholar
  15. Darimont CT, Carlson SM, Kinnison MT, Paquet PC, Reimchen TE, Wilmers CC (2009) Human predators outpace other agents of trait change in the wild. Proc Natl Acad Sci USA 106:952–954. doi:10.1073/pnas.0809235106 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Davey JW, Blaxter ML (2011) RADSeq: next-generation population genetics. Brief Funct Genom 10:108. doi:10.1093/bfgp/elr007 CrossRefGoogle Scholar
  17. Dogan B, Duran A, Bagci Y, Dinc M, Martin E, Cetin O, Ozturk M (2010) Phylogenetic relationships among the taxa of the genus Johrenia DC. (Apiaceae) from Turkey based on molecular method. Bangladesh J Plant Taxon. doi:10.3329/bjpt.v17i2.6693 Google Scholar
  18. Dosmann MS (2006) Research in the garden: averting the collections crisis. Bot Rev 72:207–234CrossRefGoogle Scholar
  19. Duminil J, Hardy OJ, Petit RJ (2009) Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure. BMC Evol Biol 9:177. doi:10.1186/1471-2148-9-177 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7 CrossRefGoogle Scholar
  21. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242. doi:10.1146/annurev.es.24.110193.001245 CrossRefGoogle Scholar
  22. ENSCONET (2009) Seed collecting manual for wild speciesGoogle Scholar
  23. Enßlin A, Sandner TM, Matthies D (2011) Consequences of ex situ cultivation of plants: genetic diversity, fitness and adaptation of the monocarpic Cynoglossum officinale L. in botanic gardens. Biol Cons 144:272–278. doi:10.1016/j.biocon.2010.09.001 CrossRefGoogle Scholar
  24. Ensslin A, Tschöpe O, Burkart M, Joshi J (2015) Fitness decline and adaptation to novel environments in ex situ plant collections: current knowledge and future perspectives. Biol Conserv 192:394–401. doi:10.1016/j.biocon.2015.10.012 CrossRefGoogle Scholar
  25. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x CrossRefPubMedGoogle Scholar
  26. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x CrossRefPubMedGoogle Scholar
  27. Falk DA, Holsinger KE (1991) Genetics and conservation of rare plants. Oxford University Press, New YorkGoogle Scholar
  28. Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333. doi:10.1111/j.1365-294X.2007.03399.x CrossRefPubMedGoogle Scholar
  29. Gavrilets S (2003) Perspective: models of speciation: what have we learned in 40 years? Evol 57:2197–2215. doi:10.1111/j.0014-3820.2003.tb00233.x CrossRefGoogle Scholar
  30. Glowka L, Burhenne-Guilmin F, Synge H (1994) A guide to the convention on biological diversity. IUCN–the World Conservation Union, Gland, SwitzerlandGoogle Scholar
  31. Griffith P, Husby C (2010) The price of conservation: measuring the mission and its cost. BGJournal 7:12–14Google Scholar
  32. Grover A, Sharma PC (2016) Development and use of molecular markers: past and present. Crit Rev Biotechnol 36:290–302. doi:10.3109/07388551.2014.959891 CrossRefPubMedGoogle Scholar
  33. Guerrant EO, Havens K, Maunder M (eds) (2004) Ex situ plant conservation: Supporting species survival in the wild. Island Press, WashingtonGoogle Scholar
  34. Haeupler H, Muer T (2000) Bildatlas der Farn- und Blütenpflanzen Deutschlands. Eugen Ulmer, StuttgartGoogle Scholar
  35. Havens K, Guerrant EO, Maunder M, Vitt P (2004) Guidelines for ex situ conservation collection management: minimizing risks. In: Guerrant EO, Havens K, Maunder M (eds) Ex situ plant conservation: supporting species survival in the wild. Island Press, Washington, pp 454–473Google Scholar
  36. Hecker U (1987) Die Farn- und Blütenpflanzen des Mainzer Sandes. Mainzer Naturw Arch 25:85–133Google Scholar
  37. Hegi G (2009) Illustrierte flora von Mitteleuropa. Weissdorn-Verlag, JenaGoogle Scholar
  38. Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates of phenotypic change in wild animal populations. Mol Ecol 17:20–29. doi:10.1111/j.1365-294X.2007.03428.x CrossRefPubMedGoogle Scholar
  39. Hodvina S, Cezanne R (2007) Das Dünen-Steinkraut (Alyssum montanum subsp. gmelinii) in Hessen. Botanik und Naturschutz in Hessen 20:25–51Google Scholar
  40. Hohenlohe PA, Amish SJ, Catchen JM, Allendorf FW, Luikart G (2011) Next-generation RAD sequencing identifies thousands of SNPs for assessing hybridization between rainbow and westslope cutthroat trout. Mol Ecol Resour 11(Suppl 1):117–122. doi:10.1111/j.1755-0998.2010.02967.x CrossRefPubMedGoogle Scholar
  41. Honjo M, Ueno S, Tsumura Y, Handa T, Washitani I, Ohsawa R (2008) Tracing the origins of stocks of the endangered species Primula sieboldii using nuclear microsatellites and chloroplast DNA. Conserv Genet 9:1139–1147. doi:10.1007/s10592-007-9427-7 CrossRefGoogle Scholar
  42. Jännicke W (1892) Die Sandflora von Mainz, ein Relict aus der Steppenzeit. Gbr. Knauer, Frankfurt am MainGoogle Scholar
  43. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics (Oxford, England) 24:1403–1405. doi: 10.1093/bioinformatics/btn129
  44. Jorgensen C, Enberg K, Dunlop ES, Arlinghaus R, Boukal DS, Brander K, Ernande B, Gardmark A, Johnston F, Matsumura S, Pardoe H, Raab K, Silva A, Vainikka A, Dieckmann U, Heino M, Rijnsdorp AD (2007) Ecology: managing evolving fish stocks. Science (New York, N.Y.) 318:1247–1248. doi:10.1126/science.1148089 CrossRefGoogle Scholar
  45. Kalinowski ST (2011) The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure. Heredity 106:625–632. doi:10.1038/hdy.2010.95 CrossRefPubMedGoogle Scholar
  46. Kasso M, Balakrishnan M (2013) Ex situ conservation of biodiversity with particular emphasis to ethiopia. ISRN Biodiversity 2013:1–11. doi:10.1155/2013/985037 Google Scholar
  47. Kinnison MT, Hendry AP (2001) The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112(113):145–164. doi:10.1023/A:1013375419520 CrossRefPubMedGoogle Scholar
  48. Knuth P (1898) Handbuch der Blütenbiologie, LeipzigGoogle Scholar
  49. Köhlein F (1984) Primeln und die verwandten Gattungen Mannsschild, Heilglöckchen, Götterblume, Troddelblume. Goldprimel, Ulmer, StuttgartGoogle Scholar
  50. Korneck D (1974) Xerothermvegetation in Rheinland-Pfalz und Nachbargebieten. Schriftenreihe Vegetationskunde 7Google Scholar
  51. Kubitzki K (ed) (2003) Malvales, Capparales and non-betalain Caryophyllales. Springer, Berlin [u.a.]Google Scholar
  52. Kühn I, Klotz S (2002) Systematik, Taxonomie und Nomenklatur. In: Klotz S, Kühn I, Durka W (eds) BIOLFLOR: Eine Datenbank mit biologisch-ökologischen Merkmalen zur Flora von Deutschland. Bundesamt für Naturschutz, BonnGoogle Scholar
  53. Lauterbach D, Ristow M, Gemeinholzer B (2011) Genetic population structure, fitness variation and the importance of population history in remnant populations of the endangered plant Silene chlorantha (Willd.) Ehrh. (Caryophyllaceae). Plant Biol (Stuttg) 13:667–777. doi:10.1111/j.1438-8677.2010.00418.x CrossRefGoogle Scholar
  54. Lauterbach D, Burkart M, Gemeinholzer B (2012) Rapid genetic differentiation between ex situ and their in situ source populations: an example of the endangered Silene otites (Caryophyllaceae). Bot J Linn Soc 168:64–75. doi:10.1111/j.1095-8339.2011.01185.x CrossRefGoogle Scholar
  55. Leimu R, Mutikainen PI, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952. doi:10.1111/j.1365-2745.2006.01150.x CrossRefGoogle Scholar
  56. Li D-Z, Pritchard HW (2009) The science and economics of ex situ plant conservation. Trends Plant Sci 14:614–621. doi:10.1016/j.tplants.2009.09.005 CrossRefPubMedGoogle Scholar
  57. Lienert J (2004) Habitat fragmentation effects on fitness of plant populations—a review. J Nat Conserv 12:53–72. doi:10.1016/j.jnc.2003.07.002 CrossRefGoogle Scholar
  58. Lönn M, Prentice HC, Bengtsson K (1996) Genetic structure, allozyme-habitat associations and reproductive fitness in Gypsophila fastigiata (Caryophyllaceae). Oecologia 106:308–316. doi:10.1007/BF00334558 CrossRefPubMedGoogle Scholar
  59. Lynch M, Milligan B (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99CrossRefPubMedGoogle Scholar
  60. Maunder M, Higgens S, Culham A (2001) The effectiveness of botanic garden collections in supporting plant conservation: a European case study. Biodivers Conserv 10:383–401. doi:10.1023/A:1016666526878 CrossRefGoogle Scholar
  61. Maunder M, Hughes C, Hawkins JA, Culham A (2004) Hybridization in ex situ plant collections: conservation concerns, liabilities, and opportunities. In: Guerrant EO, Havens K, Maunder M (eds) Ex situ plant conservation: supporting species survival in the wild. Island Press, Washington, pp 325–364Google Scholar
  62. Melfi VA (2012) Ex situ gibbon conservation: status, management and birth sex ratios. Int Zoo Yb 46:241–251. doi:10.1111/j.1748-1090.2011.00150.x CrossRefGoogle Scholar
  63. Miller AJ, Schaal BA (2006) Domestication and the distribution of genetic variation in wild and cultivated populations of the Mesoamerican fruit tree Spondias purpurea L. (Anacardiaceae). Mol Ecol 15:1467–1480. doi:10.1111/j.1365-294X.2006.02834.x CrossRefPubMedGoogle Scholar
  64. Namoff S, Husby CE, Francisco-Ortega J, Noblick LR, Lewis CE, Griffith MP (2010) How well does a botanical garden collection of a rare palm capture the genetic variation in a wild population? Biol Conserv 143:1110–1117. doi:10.1016/j.biocon.2010.02.004 CrossRefGoogle Scholar
  65. Ng WL, Tan SG (2015) Inter-simple sequence repeat (ISSR) markers: are we doing it right? ASM Sci J 9:30–39Google Scholar
  66. Oldfield SF (2009) Botanic gardens and the conservation of tree species. Trends Plant Sci 14:581–583. doi:10.1016/j.tplants.2009.08.013 CrossRefPubMedGoogle Scholar
  67. Oldfield S (2010) Botanic gardens: modern-day arks. MIT Press, Cambridge, MassGoogle Scholar
  68. Ouborg NJ, Vergeer P, Mix C (2006) The rough edges of the conservation genetics paradigm for plants. J Ecol 94:1233–1248. doi:10.1111/j.1365-2745.2006.01167.x CrossRefGoogle Scholar
  69. Palumbi SR (2001) Humans as the world’s greatest evolutionary force. Science 293:1786–1790CrossRefPubMedGoogle Scholar
  70. Parejo-Farnés C, Albaladejo GR, Arroyo J, Aparicio A (2013) A phylogenetic hypothesis for Helianthemum (Cistaceae) in the Iberian Peninsula. Bot. Complut. 37: 83–92. http://revistas.ucm.es/index.php/BOCM/article/download/42272/40241
  71. Parzies HK, Spoor W, Ennos RA (2000) Genetic diversity of barley landrace accessions (Hordeum vulgare ssp. vulgare) conserved for different lengths of time in ex situ gene banks. Heredity 84:476. doi:10.1046/j.1365-2540.2000.00705.x CrossRefPubMedGoogle Scholar
  72. Poczai P, Varga I, Laos M, Cseh A, Bell N, Valkonen JP, Hyvonen J (2013) Advances in plant gene-targeted and functional markers: a review. Plant Methods 9:6. doi:10.1186/1746-4811-9-6 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Podolsky RH (2001) Genetic variation for morphological and allozyme variation in relation to population size in Clarkia dudleyana, an endemic annual. Conserv Biol 15:412–423. doi:10.1046/j.1523-1739.2001.015002412.x CrossRefGoogle Scholar
  74. Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE 7:1–8. doi:10.1371/journal.pone.0032253 CrossRefGoogle Scholar
  75. Porras-Hurtado L, Ruiz Y, Santos C, Phillips C, Carracedo A, Lareu MV (2013) An overview of STRUCTURE: applications, parameter settings, and supporting software. Front Genet 4:98. doi:10.3389/fgene.2013.00098 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Poschlod P, WallisDeVries MF (2002) The historical and socioeconomic perspective of calcareous grasslands—lessons from the distant and recent past. Biol Conserv 104:361–376. doi:10.1016/S0006-3207(01)00201-4 CrossRefGoogle Scholar
  77. Pritchard JK, Stephens M, Donnelly Peter (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  78. Provine WB (2004) Perspectives: ernst Mayr: genetics and speciation. Genetics 167:1041–1046PubMedPubMedCentralGoogle Scholar
  79. Rice KJ, Emery NC (2003) Managing microevolution: restoration in the Face of Global Change. Front Ecol Environ 1:469. doi:10.2307/3868114 CrossRefGoogle Scholar
  80. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. doi:10.1046/j.1471-8286.2003.00566.x CrossRefGoogle Scholar
  81. Rucińska A, Puchalski J (2011) Comparative molecular studies on the genetic diversity of an ex situ garden collection and its source population of the critically endangered polish endemic plant Cochlearia polonica E. Fröhlich. Biodivers Conserv 20:401–413. doi:10.1007/s10531-010-9965-z CrossRefGoogle Scholar
  82. Rusterholz H-P, Aydin D, Baur B (2012) Population structure and genetic diversity of relict populations of Alyssum montanum on limestone cliffs in the Northern Swiss Jura mountains. Alp Bot 122:109–117. doi:10.1007/s00035-012-0105-0 CrossRefGoogle Scholar
  83. Schweingruber FH, Poschlod P (2005) Growth rings in herbs and shrubs: life span, age determination and stem anatomy. Swiss Federal Research Institute WSLGoogle Scholar
  84. Secretariat of the Convention on Biological Diversity (SCBD) (2010) 2010. Global strategy for plant conservation. Updated Strategy 2011–2020. https://www.cbd.int/gspc/about.shtml. Accessed 4 August 2016
  85. Španiel S, Marhold K, Filová B, Zozomová-Lihová J (2011) Genetic and morphological variation in the diploid–polyploid Alyssum montanum in Central Europe: taxonomic and evolutionary considerations. Plant Syst Evol 294:1–25. doi:10.1007/s00606-011-0438-y CrossRefGoogle Scholar
  86. Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101. doi:10.1016/S0169-5347(02)00044-7 CrossRefGoogle Scholar
  87. Tautz D (1989) Hypervariabflity of simple sequences as a general source for polymorphic DNA markers. Nucl Acids Res 17:6463–6471. doi:10.1093/nar/17.16.6463 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Tautz D, Renz M (1984) Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucl Acids Res 12:4127–4138. doi:10.1093/nar/12.10.4127 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Tutin TG, Ball PW (1972) Diapensiaceae to myoporaceae. Cambridge University Press, CambridgeGoogle Scholar
  90. Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) (1964) Lycopodiaceae to plantanaceae. Cambridge University Press, CambridgeGoogle Scholar
  91. Vekemans X (2002) AFLP-surv version 1.0. Distributed by the author. Laboratoire de Ge´ne´tique et Evolution des Populations Ve´ge´tales. Department of Biology, University of Lille 1, LilleGoogle Scholar
  92. Volis S, Blecher M (2010) Quasi in situ: a bridge between ex situ and in situ conservation of plants. Biodivers Conserv 19:2441–2454. doi:10.1007/s10531-010-9849-2 CrossRefGoogle Scholar
  93. Weising K (2005) DNA fingerprinting in plants: principles, methods, and applications, 2nd edn. Taylor & Francis Group, Boca Raton, FLCrossRefGoogle Scholar
  94. Whitlock R, Hipperson H, Thompson D, Butlin RK, Burke T (2016) Consequences of in situ strategies for the conservation of plant genetic diversity. Biol Conserv 203:134–142. doi:10.1016/j.biocon.2016.08.006 CrossRefGoogle Scholar
  95. Wiens JA, Hobbs RJ (2015) Integrating conservation and restoration in a changing world. Bioscience 65:302–312. doi:10.1093/biosci/biu235 CrossRefGoogle Scholar
  96. Wolf AT, Harrison SP, Hamrick JL (2000) Influence of habitat patchiness on genetic diversity and spatial structure of a serpentine endemic plant. Conserv Biol 14:454–463. doi:10.1046/j.1523-1739.2000.98499.x CrossRefGoogle Scholar
  97. Xu Q, Wen X, Deng X (2004) A simple protocol for isolating genomic DNA from chestnut rose (Rosa roxburghii Tratt) for RFLP and PCR analyses. Plant Mol Biol Rep 22:301–302. doi:10.1007/BF02773140 CrossRefGoogle Scholar
  98. Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418. doi:10.1016/0169-5347(96)10045-8 CrossRefPubMedGoogle Scholar
  99. Zohary D (2004) Unconscious selection and the evolution of domesticated plants. Econ Bot 58:5–10CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Christina Magdalena Müller
    • 1
  • Björn Huwe
    • 2
  • Volker Wissemann
    • 1
  • Jasmin Joshi
    • 2
    • 3
  • Birgit Gemeinholzer
    • 1
  1. 1.Systematic BotanyJustus-Liebig-University GiessenGiessenGermany
  2. 2.Biodiversity Research/Sytematic BotanyUniversity of PotsdamPotsdamGermany
  3. 3.Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB)BerlinGermany

Personalised recommendations