Plant Systematics and Evolution

, Volume 300, Issue 5, pp 1199–1208 | Cite as

Low genetic diversity and high levels of inbreeding in the Sinai primrose (Primula boveana), a species on the brink of extinction

  • Ares JiménezEmail author
  • Hassan Mansour
  • Barbara Keller
  • Elena Conti
Original Article


The Sinai primrose (Primula boveana) is one of the most endangered plant species worldwide, with less than 200 wild individuals surviving in the Sinai mountains of Egypt. There has been a decline in both the number and size of its populations in recent times, possibly caused by threats that include habitat aridification and the impact of human activities. Studying the standing genetic variation and extent of inbreeding of P. boveana is necessary for the design of appropriate conservation strategies for this species. In the present work, we used a set of seven, recently developed, polymorphic microsatellite markers to characterize the genetic variation and levels of inbreeding of the extant populations of P. boveana. We found low levels of genetic variation (H T = 0.470), high differentiation between populations (F ST = 0.737, R ST = 0.935), and very elevated levels of inbreeding (F = 0.862) due to recurrent selfing. These results may be the reflection of low levels of genetic variation and high levels of inbreeding over a long evolutionary period, suggesting that the current genetic pool of the species may enable P. boveana to persist in a habitat where water availability and pollinator services are restricted. Nevertheless, in sight of its rapidly dwindling abundance, it seems prudent to adopt swift measures, including habitat restoration and ex-situ conservation, to prevent the impending extinction of this emblematic species.


Aridification Genetic variation Inbreeding Mount St. Catherine Sinai primrose Human-driven environmental change 



We thank S. Hussein for his help during field work and M. D. Nowak for his valuable comments in early drafts of this manuscript. We also thank G. Oostermeijer for the constructive comments and suggestions provided during the revision process. This work was supported by a Swiss National Science Foundation grant to HM (IZK0Z3_139418) for a short research stay in Zurich and by the Institute of Systematic Botany of the University of Zurich.

Supplementary material

606_2013_955_MOESM1_ESM.doc (52 kb)
Supplementary material 1 (DOC 51 kb)


  1. Al Wadi H (1993) Primula boveana and Jebel Katarina. Bull Alp Gar Soc 61:68–70Google Scholar
  2. Al Wadi H, Richards AJ (1993) Primary homostyly in Primula L. subgenus Sphondylia (Duby) Rupr. and the evolution of distyly in Primula. New Phytol 124:329–338CrossRefGoogle Scholar
  3. Alpert P, Krichak SO, Shafir H, Haim D, Osetinsky I (2008) Climatic trends to extremes employing regional modeling and statistical interpretation over the E. Mediterranean. Global Planet Change 63:163–170CrossRefGoogle Scholar
  4. Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165PubMedCrossRefGoogle Scholar
  5. Barrett SCH (1992) Evolution and function of heterostyly. Springer-Verlag, BerlinCrossRefGoogle Scholar
  6. Barton NH, Slatkin M (1986) A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 56:409–415PubMedCrossRefGoogle Scholar
  7. Blacket MJ, Robin C, Good RT, Lee SF, Miller AD (2012) Universal primers for fluorescent labelling of PCR fragments–an efficient and cost-effective approach to genotyping by fluorescence. Mol Ecol Resour 12:456–463PubMedCrossRefGoogle Scholar
  8. Booy G, Hendriks RJJ, Smulders MJM, Van Groenendael JM, Vosman B (2000) Genetic diversity and the survival of populations. Plant Biol 2:379–395CrossRefGoogle Scholar
  9. Busch JW (2005) Inbreeding depression in self-incompatible and self-compatible populations of Leavenworthia alabamica. Heredity 94:156–165CrossRefGoogle Scholar
  10. Charlesworth D, Charlesworth B (1979) A model for the evolution of distyly. Am Nat 114:467–498CrossRefGoogle Scholar
  11. Crema S, Cristofolini G, Rossi M, Conte L (2009) High genetic diversity detected in the endemic Primula apennina Widmer (Primulaceae) using ISSR fingerprinting. Plant Syst Evol 280:29–36CrossRefGoogle Scholar
  12. Crnokrak P, Barrett SCH (2002) Purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358PubMedCrossRefGoogle Scholar
  13. Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270PubMedCrossRefGoogle Scholar
  14. Darwin C (1862) On the two forms or dimorphic conditions in the species of Primula, and on their remarkable sexual relations. J Proc Linn Soc Bot 6:77–96Google Scholar
  15. Darwin C (1877) The different forms of flowers on plants of the same species. John Murray, LondonCrossRefGoogle Scholar
  16. de Vos JM, Keller B, Isham ST, Kelso S, Conti E (2012) Reproductive implications of herkogamy in homostylous primroses: variation during anthesis and reproductive assurance in alpine environments. Funct Ecol 26:854–865CrossRefGoogle Scholar
  17. Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Natl Rev Genet 5:435–445CrossRefGoogle Scholar
  18. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Ann Rev Ecol Syst 24:217–242CrossRefGoogle Scholar
  19. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedCentralPubMedGoogle Scholar
  20. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  21. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge university Press, CambridgeCrossRefGoogle Scholar
  22. García N, Cuttelod A, Abdul Malak D (2010) The status and distribution of freshwater biodiversity in northern Africa. IUCN, Gland, Switzerland, Cambridge, UK, and Malaga, SpainGoogle Scholar
  23. Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Global Planet Change 63:90–104CrossRefGoogle Scholar
  24. Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792PubMedCrossRefGoogle Scholar
  25. Glover BJ, Abbott RJ (1995) Low genetic diversity in the Scottish endemic Primula scotica Hook. New Phytol 129:147–153CrossRefGoogle Scholar
  26. González-Tejero MR, Casares-Porcel M, Sánchez-Rojas CP, Ramiro-Gutiérrez JM, Molero-Mesa J, Pieroni A, Giusti ME, Censorii E, de Pascale C, Della A, Paraskeva-Hadijchambi D, Hadjichambis A, Houmani Z, El-Demerdash M, El-Zayat M, Hmamouchi M, ElJohring S (2008) Medicinal plants in the Mediterranean area: synthesis of the results of the project Rubia. J Ethnopharmacol 116:341–357PubMedCrossRefGoogle Scholar
  27. Grainger J (2003) ‘People are living in the park’. Linking biodiversity conservation to community development in the Middle East region: a case study from the Saint Katherine Protectorate, Southern Sinai. J Arid Environ 54:29–38CrossRefGoogle Scholar
  28. Hamrick JL, Godt MJW (1989) Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding and genetic resources. Sinauer Associates, Sunderland, pp 42–46Google Scholar
  29. Hedrick PH (1999) Highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318CrossRefGoogle Scholar
  30. Heller NE, Zavaleta ES (2009) Biodiversity management in the face of climate change: a review of 22 years of recommendations. Biol Conserv 142:14–32CrossRefGoogle Scholar
  31. Holsinger KE, Gottlieb LD (1991) Conservation of rare and endangered plants: principles and prospects. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press, New York, pp 195–208Google Scholar
  32. Honnay O, Jacquemyn H (2007) Susceptibility of rare and common plant species to the genetic consequences of habitat fragmentation. Conserv Biol 21:824–831CrossRefGoogle Scholar
  33. Hoyle M, James M (2005) Global warming, human population pressure, and viability of the world’s smallest butterfly. Conserv Biol 19:1113–1124CrossRefGoogle Scholar
  34. Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70CrossRefGoogle Scholar
  35. Issar AS (2008) The impact of global warming on the water resources of the Middle East: past, present and future. In: Zereini F, Hötzl H (eds) Climate changes and water resources in the Middle East and North Africa. Springer, Heidelberg, pp 145–164CrossRefGoogle Scholar
  36. Jump AS, Marchant R, Peñuelas J (2009) Environmental change and the option value of genetic diversity. Trends Plant Sci 14:51–58PubMedCrossRefGoogle Scholar
  37. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241CrossRefGoogle Scholar
  38. Lande R, Schemske DW (1985) The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24–40CrossRefGoogle Scholar
  39. Li YC, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions, and mutational mechanisms: a review. Mol Ecol 11:2453–2465PubMedCrossRefGoogle Scholar
  40. López-Pujol J, Martinell MC, Massó S, Blanché C, Sáez L (2013) “The paradigm of extremes”: extremely low genetic diversity in an extremely narrow endemic species, Coristospermum huteri (Umbelliferae). Plant Syst Evol 299:439–446CrossRefGoogle Scholar
  41. Luijten SH, Dierick A, Gerard J, Oostermeijer B, Raijmann LEJ, Den Nijs HCM (2000) Population size, genetic variation, and reproductive success in a rapidly declining, self-incompatible perennial (Arinica montana) in the Netherlands. Conserv Biol 14:1776–1787CrossRefGoogle Scholar
  42. Mansour H, Jiménez A, Keller B, Nowak M, Conti E (2013) Development of thirteen microsatellite markers in the endangered Sinai primrose (Primula boveana, Primulaceae). Appl Plant Sci 1:1200515Google Scholar
  43. Mast AR, Kelso S, Conti E (2006) Are any primroses (Primula) primitively monomorphic? New Phytol 171:605–616PubMedCrossRefGoogle Scholar
  44. Matsumura C, Washitani I (2000) Effects of population size and pollinator limitation on seed-set of Primula sieboldii populations in a fragmented landscape. Ecol Res 15:307–322CrossRefGoogle Scholar
  45. McCain CM, Colwell RK (2011) Assessing the threat to montane biodiversity from discordant shifts in temperature and precipitation in a changing climate. Ecol Lett 14:1236–1245PubMedCrossRefGoogle Scholar
  46. Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064PubMedCentralPubMedGoogle Scholar
  47. Milberg P (1994) Germination ecology of the polycarpic grassland perennials Primula veris and Trollius europaeus. Ecography 17:3–8CrossRefGoogle Scholar
  48. Minuto L, Guerrina M, Roccotiello E, Roccatagliata N, Mariotti M, Casazza G (2013) Pollination ecology in the narrow endemic winter-flowering Primula allionii (Primulaceae). J Plant Res. doi: 10.1007/s10265-013-0588-9 PubMedGoogle Scholar
  49. Moustafa AA, Ramadan AA, Zaghloul MS, Helmy MA (2001) Characteristics of two endemic and endangered species (Primula boveana and Kickxia macilenta) growing in South Sinai. Egypt J Bot 41:17–39Google Scholar
  50. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323PubMedCentralPubMedCrossRefGoogle Scholar
  51. Nogués-Bravo D, Araújo MB, Errea MP, Martínez-Rica JP (2007) Exposure of global systems to climate warming during the 21st Century. Global Environ Chang 17:420–428CrossRefGoogle Scholar
  52. Nybom H (2004) Comparison of different DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155PubMedCrossRefGoogle Scholar
  53. Oostermeijer JGB, Van Eijck MW, Den Nijs JCM (1994) Offspring fitness in relation to population size and genetic variation in the rare perennial plant species Gentiana pneumonanthe (Gentianaceae). Oecologia 97:289–296Google Scholar
  54. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  55. Radford EA, Catullo G, de Montmollin B (2011) Important plant areas of the south and east Mediterranean region: priority sites for conservation. IUCN, Gland, Switzerland and Malaga, SpainGoogle Scholar
  56. Richards AJ (2003) Primula, 2nd edn. Timber Press, OregonGoogle Scholar
  57. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60PubMedCrossRefGoogle Scholar
  58. Schemske DW, Husband BC, Rukelshaus MH, Goodwillie C, Parker IM, Bishop J (1994) Evaluating approaches to the conservation of rare and endangered plants. Ecology 75:584–606CrossRefGoogle Scholar
  59. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234PubMedCrossRefGoogle Scholar
  60. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629PubMedCrossRefGoogle Scholar
  61. Shao J-W, Chen W-L, Peng Y-Q, Zhu G-P, Zhang X-P (2009) Genetic diversity within and among populations of the endangered and endemic species Primula merilliana in China. Biochem Syst Ecol 37:699–706CrossRefGoogle Scholar
  62. Shimono A, Ueno S, Tsumura Y, Washitani I (2006) Spatial genetic structure links between soil seed banks and above-ground populations of Primula modesta in subalpine grassland. J Ecol 94:77–86CrossRefGoogle Scholar
  63. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedCentralPubMedGoogle Scholar
  64. Smyser TJ, Duchamp JE, Johnson SA, Larkin JL, Rhodes OE Jr (2012) Consequences of metapopulation collapse: comparison of genetic attributes between two Allegheny woodrat metapopulations. Conserv Genet 13:849–858CrossRefGoogle Scholar
  65. Spieth PT (1974) Gene flow and genetic differentiation. Genetics 78:961–965PubMedCentralPubMedGoogle Scholar
  66. Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101CrossRefGoogle Scholar
  67. Sydes MA, Peakall R (1998) Extensive clonality in the endangered shrub Haloragodendron lucasii (Haloragaceae) revealed by allozymes and RAPDs. Mol Ecol 7:87–93CrossRefGoogle Scholar
  68. Valdés A, García D (2011) Direct and indirect effects of landscape change on the reproduction of a temperate perennial herb. J Appl Ecol 48:1422–1431CrossRefGoogle Scholar
  69. Van Geert A, Van Rossum F, Triest L (2008) Genetic diversity in adult and seedling populations of Primula vulgaris in a fragmented agricultural landscape. Conserv Genet 9:845–853CrossRefGoogle Scholar
  70. Van Rossum F, Triest L (2006) Fine-scale genetic structure of the common Primula elatior (Primulaceae) at an early stage of population fragmentation. Am J Bot 93:12811288Google Scholar
  71. Van Rossum F, Enchchgadda G, Szabadi I, Triest L (2002) Commonness and long-term survival in fragmented habitats: Primula elatior as a study case. Conserv Biol 16:1286–1295CrossRefGoogle Scholar
  72. Van Rossum F, Campos De Sousa S, Triest L (2004) Genetic consequences of habitat fragmentation in an agricultural landscape on the common Primula veris, and comparison with its rare congener, P. vulgaris. Conserv Genet 5:231–245CrossRefGoogle Scholar
  73. Van Rossum F, Stiers I, Van Geert A, Triest L, Hardy O (2011) Fluorescent dye particles as pollen analogues for measuring pollen dispersal in an insect-pollinated forest herb. Oecologia 165:663–674PubMedCrossRefGoogle Scholar
  74. Vilas C, San Miguel E, Amaro R, García C (2005) Relative contribution of inbreeding depression and eroded adaptive diversity to extinction risk in small populations of shore campion. Conserv Biol 20:229–238CrossRefGoogle Scholar
  75. Weeda EJ, Westra R, Westra C, Westra T (1985) Nederlandse oecologische flora. Wilde planten en hun relaties, 1st edn. IWN, Vara & Vewin, HilversumGoogle Scholar
  76. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  77. Wendelbo P (1961) Studies in Primulaceae. II. An account of Primula subgenus Sphondylia with review of the sections of the genus. Aarbok for Universitet I Bergen. Mat- Naturv Serie 11:1–49Google Scholar
  78. Wolff K, El-Akkad S, Abbot RJ (1997) Population substructure in Alkanna orientalis (Boraginaceae) in the Sinai Desert, in relation to its pollinator behaviour. Mol Ecol 6:365–372CrossRefGoogle Scholar
  79. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedCentralPubMedGoogle Scholar
  80. Xue D-W, X-J GE, Hao G, Zhang C-Q (2004) High genetic diversity in a rare, narrowly endemic primrose species: Primula interjacens by ISSR analysis. Acta Bot Sin 46:1163–1169Google Scholar
  81. Zaghloul MS (2008) Diversity in soil seed bank of Sinai and implications for conservation and restoration. Afr J Environ Sci Technol 2:172–184Google Scholar

Copyright information

© Springer-Verlag Wien 2013

Authors and Affiliations

  • Ares Jiménez
    • 1
    Email author
  • Hassan Mansour
    • 2
  • Barbara Keller
    • 1
  • Elena Conti
    • 1
  1. 1.Institute of Systematic BotanyUniversity of ZurichZurichSwitzerland
  2. 2.Botany Department, Faculty of ScienceSuez Canal UniversityIsmailiaEgypt

Personalised recommendations