Genetic Diversity and Differentiation Among Species and Populations of Boswellia

  • Ahmed Al-Harrasi
  • Abdul Latif Khan
  • Sajjad Asaf
  • Ahmed Al-Rawahi


The results of this study revealed a high level of genetic differentiation within populations and a low level of genetic diversity among populations of B. sacra. AFLP and SSR markers revealed more variations compared to RAPD and SDS-PAGE markers. Overall, a reasonable level of genetic diversity is observed in all the populations, but some populations showed high levels of genetic variations and high genetic and geographic distances (Thumrait, Dowkha and Mughsil). Our findings may be useful for further molecular study of and conservation strategies for this endemic species.


Populations RAPD SSR AFLP SDS-PAGE Markers Conservation 


  1. Addisalem, A., Bongers, F., Kassahun, T., & Smulders, M. (2016). Genetic diversity and differentiation of the frankincense tree (Boswellia papyrifera (Del.) Hochst) across Ethiopia and implications for its conservation. Forest Ecology and Management, 360, 253–260.CrossRefGoogle Scholar
  2. Addisalem, A., Duminil, J., Wouters, D., Bongers, F., & Smulders, M. (2016). Fine-scale spatial genetic structure in the frankincense tree Boswellia papyrifera (Del.) Hochst. and implications for conservation. Tree Genetics & Genomes, 12, 86–96.CrossRefGoogle Scholar
  3. Addisalem, A., Esselink, G. D., Bongers, F., & Smulders, M. (2015). Genomic sequencing and microsatellite marker development for Boswellia papyrifera, an economically important but threatened tree native to dry tropical forests. Aob Plants, 7.Google Scholar
  4. Alemu, B., Garedew, E., Eshetu, Z., & Kassa, H. (2015). Land use and land cover changes and associated driving forces in north western lowlands of Ethiopia. International Research Journal of Agricultural Science and Soil Science, 5, 28–44.CrossRefGoogle Scholar
  5. Assefa, M., Dekebo, H., Kassa, H., Habtu, A., Fitwi, G., & Redi-Abshiro, M. (2012). Biophysical and chemical investigations of frankincense of Boswellia papyrifera from North and Northwestern Ethiopia. Journal of Chemical and Pharmaceutical Research, 4.Google Scholar
  6. Banks, S. C., Cary, G. J., Smith, A. L., Davies, I. D., Driscoll, D. A., Gill, A. M., & Peakall, R. (2013). How does ecological disturbance influence genetic diversity?. Trends in ecology & evolution, 28(11), 670–679.Google Scholar
  7. Barnes, M. A., & Turner, C. R. (2016). The ecology of environmental DNA and implications for conservation genetics. Conservation Genetics, 17, 1–17. Scholar
  8. Basar, S. (2005). Phytochemical investigations on Boswellia species. University of Hamburg, Germany.Google Scholar
  9. Bekana, D., Kebede, T., Assefa, M., & Kassa, H. (2014). Comparative phytochemical analyses of resins of Boswellia species (B. papyrifera (Del.) Hochst., B. neglecta S. Moore, and B. rivae Engl.) from Northwestern, Southern, and Southeastern Ethiopia. ISRN Analytical Chemistry, 2014, 1–9.CrossRefGoogle Scholar
  10. Bell, G., & Collins, S. (2008). Adaptation, extinction and global change. Evolutionary Applications, 1, 3–16. Scholar
  11. Blows, M. W., & Hoffmann, A. A. (2005). A reassessment of genetic limits to evolutionary change. Ecology, 86, 1371–1384. Scholar
  12. Booy, G., Hendriks, R., Smulders, M., Van Groenendael, J., & Vosman, B. (2000). Genetic diversity and the survival of populations. Plant Biology, 2, 379–395.CrossRefGoogle Scholar
  13. Bornet, B., & Branchard, M. (2001). Nonanchored inter simple sequence repeat (ISSR) markers: Reproducible and specific tools for genome fingerprinting. Plant Molecular Biology Reporter, 19, 209–215. Scholar
  14. Carter, M. C., & Sytsma, M. D. (2001). Comparison of the genetic structure of North and South American populations of a clonal aquatic plant. Biological Invasions, 3, 113–118.CrossRefGoogle Scholar
  15. Charlesworth, B. (2009). Effective population size and patterns of molecular evolution and variation. Nature Reviews Genetics, 10, 195.CrossRefPubMedGoogle Scholar
  16. Collins, D., Mill, R. R., & Möller, M. (2003). Species separation of Taxus baccata, T. canadensis, and T. cuspidata (Taxaceae) and origins of their reputed hybrids inferred from RAPD and cpDNA data. American Journal of Botany, 90, 175–182.CrossRefPubMedGoogle Scholar
  17. Coppi, A., Cecchi, L., Selvi, F., & Raffaelli, M. (2010). The Frankincense tree (Boswellia sacra, Burseraceae) from Oman: ITS and ISSR analyses of genetic diversity and implications for conservation. Genetic Resources and Crop Evolution, 57, 1041–1052.CrossRefGoogle Scholar
  18. de Mendonça, P. C., Bertoni, B. W., Amui, S. F., Giuliatti, S., Corrêa, V. S. C., de Castro, F. S., & Pereira, A. M. S. (2012). Genetic diversity of Stryphnodendron adstringens (Mart.) Coville determined by AFLP molecular markers. Biochemical Systematics and Ecology, 41, 16–20.CrossRefGoogle Scholar
  19. Duminil, J., Brown, R. P., Ewédjè, E.-E. B., Mardulyn, P., Doucet, J.-L., & Hardy, O. J. (2013). Large-scale pattern of genetic differentiation within African rainforest trees: insights on the roles of ecological gradients and past climate changes on the evolution of Erythrophleum spp (Fabaceae). BMC Evolutionary Biology, 13, 195.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Duminil, J., Hardy, O. J., & Petit, R. J. (2009). Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure. BMC Evolutionary Biology, 9, 177.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Edwards, C. E., Parchman, T. L., & Weekley, C. W. (2011). Assembly, gene annotation and marker development using 454 floral transcriptome sequences in Ziziphus celata (Rhamnaceae), a highly endangered, Florida endemic plant. DNA Research, 19, 1–9.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Eshete, A., Sterck, F., & Bongers, F. (2011). Diversity and production of Ethiopian dry woodlands explained by climate-and soil-stress gradients. Forest Ecology and Management, 261, 1499–1509.CrossRefGoogle Scholar
  23. Eslamieh, J. (2017). The genus Boswellia: preservation through horticulture (p. 80527). Fort Collins, CO: A Book’s Mind.Google Scholar
  24. Fleishman, E., Launer, A. E., Switky, K. R., Yandell, U., Heywood, J., & Murphy, D. D. (2001). Rules and exceptions in conservation genetics: genetic assessment of the endangered plant Cordylanthus palmatus and its implications for management planning. Biological Conservation, 98(1), 45–53.Google Scholar
  25. Frankham, R. (1995). Conservation genetics. Annual Review of Genetics, 29, 305–327. Scholar
  26. González-Martínez, S. C., Krutovsky, K. V., & Neale, D. B. (2006). Forest-tree population genomics and adaptive evolution. New Phytologist, 170, 227–238.CrossRefPubMedGoogle Scholar
  27. Govindaraj, M., Vetriventhan, M., & Srinivasan, M. (2015). Importance of genetic diversity assessment in crop plants and its recent advances: an overview of its analytical perspectives. Genetics Research International, 2015, 431487.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Haile, G., Gebrehiwot, K., Lemenih, M., & Bongers, F. (2011). Time of collection and cutting sizes affect vegetative propagation of Boswellia papyrifera (Del.) Hochst through leafless branch cuttings. Journal of Arid Environments, 75, 873–877.CrossRefGoogle Scholar
  29. Hameed, A., Shah, T. M., Atta, B. M., Iqbal, N., Haq, M. A., & Ali, H. (2009). Comparative seed storage protein profiling of Kabuli chickpea genotypes. Pakistan Journal of Botany, 41, 703–710.Google Scholar
  30. Hamrick, J. L. (2004). Response of forest trees to global environmental changes. Forest Ecology and Management, 197, 323–335. Scholar
  31. Hoffmann, A. A., & Sgrò, C. M. (2011). Climate change and evolutionary adaptation. Nature, 470, 479. Scholar
  32. Huenneke, L. F. (1991). Ecological implications of genetic variation in plant populations. Genetics and conservation of rare plants, 31–44.Google Scholar
  33. Kaiser, R., Mageney, V., Schwefel, K., Vollmers, D., Krüger, A., & Horn, R. (2016). Genotyping of red and white fruited strawberry (Fragaria L.) accessions and hybrids based on microsatellite markers and on the genetic diversity in the allergen genes fra a 1 and fra a 3. Genetic Resources and Crop Evolution, 63, 1203–1217.CrossRefGoogle Scholar
  34. Khan, A. L., Al-Harrasi, A., Al-Rawahi, A., Al-Farsi, Z., Al-Mamari, A., Waqas, M., … Lee, I.-J. (2016). Endophytic Fungi from Frankincense Tree Improves Host Growth and Produces Extracellular Enzymes and Indole Acetic Acid. PLoS One, 11, e0158207. Scholar
  35. Khan, A. L., Al-Harrasi, A., Asaf, S., Park, C. E., Park, G.-S., Khan, A. R., … Shin, J.-H. (2017). The First Chloroplast Genome Sequence of Boswellia sacra, a Resin-Producing Plant in Oman. PLoS One, 12, e0169794.CrossRefPubMedPubMedCentralGoogle Scholar
  36. King, R., & Zalucki, J. M. (2012). Potential inbreeding in a small population of a mass flowering species, Xanthorrhoea johnsonii (Xanthorrhoeaceae): is your mother my father? American Journal of Plant Sciences, 3, 303–312.CrossRefGoogle Scholar
  37. Kjølner, S., Såstad, S., Taberlet, P., & Brochmann, C. (2004). Amplified fragment length polymorphism versus random amplified polymorphic DNA markers: clonal diversity in Saxifraga cernua. Molecular Ecology, 13, 81–86.CrossRefPubMedGoogle Scholar
  38. Koch, P., Platzer, M., & Downie, B. R. (2014). RepARK—de novo creation of repeat libraries from whole-genome NGS reads. Nucleic Acids Research, 42, e80–e80.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kramer, A. T., Ison, J. L., Ashley, M. V., & Howe, H. F. (2008). The paradox of forest fragmentation genetics. Conservation Biology, 22, 878–885.CrossRefPubMedGoogle Scholar
  40. Lacombe, T., & Thomas, M. R. (2006). Historical origins and genetic diversity of wine grapes. Trends in Genetics, 22(9), 511–519.Google Scholar
  41. Laikre, L., Schwartz, M. K., Waples, R. S., & Ryman, N. (2010). Compromising genetic diversity in the wild: unmonitored large-scale release of plants and animals. Trends in Ecology & Evolution, 25, 520–529. Scholar
  42. Lamy, T., Laroche, F., David, P., Massol, F., & Jarne, P. (2017). The contribution of species–genetic diversity correlations to the understanding of community assembly rules. Oikos, 126, 759–771.CrossRefGoogle Scholar
  43. Lanfear, R., Calcott, B., Kainer, D., Mayer, C., & Stamatakis, A. (2014). Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evolutionary Biology, 14, 82. Scholar
  44. Lawton-Rauh, A. (2008). Demographic processes shaping genetic variation. Current Opinion in Plant Biology, 11, 103–109.CrossRefPubMedGoogle Scholar
  45. Ledig, F. T., & Fryer, J. H. (1972). A pocket of variability in Pinus rigida. Evolution, 26, 259–266.CrossRefPubMedGoogle Scholar
  46. Lemenih, M., Feleke, S., & Tadesse, W. (2007). Constraints to smallholders production of frankincense in Metema district, North-western Ethiopia. Journal of Arid Environments, 71, 393–403.CrossRefGoogle Scholar
  47. Maki, M. (1999). RAPD markers revealed less genetic variation in the endangered plant Cerastium fisherianum var. molle than in its widespread congener C. fisherianum var. fisherianum (Caryophyllaceae). Molecular Ecology, 8, 145–150.CrossRefGoogle Scholar
  48. Moran, E. V., & Clark, J. S. (2011). Estimating seed and pollen movement in a monoecious plant: a hierarchical Bayesian approach integrating genetic and ecological data. Molecular Ecology, 20, 1248–1262.CrossRefPubMedGoogle Scholar
  49. Moran, E. V., & Clark, J. S. (2012). Between-site differences in the scale of dispersal and gene flow in red oak. PLoS One, 7, e36492.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Moran, P. (2002). Current conservation genetics: building an ecological approach to the synthesis of molecular and quantitative genetic methods. Ecology of Freshwater Fish, 11, 30–55.CrossRefGoogle Scholar
  51. Nisar, M., Ghafoor, A., Khan, M. R., Ahmad, H., Qureshi, A. S., & Ali, H. (2007). Genetic diversity and geographic relationship among local and exotic chickpea germplasm. Pakistan Journal of Botany, 39, 1575–1581.Google Scholar
  52. Novaes, R., Rodrigues, J., & Lovato, M. (2009). An efficient protocol for tissue sampling and DNA isolation from the stem bark of Leguminosae trees. Genetics and Molecular Research, 8, 86–96.CrossRefPubMedGoogle Scholar
  53. Nybom, H. (2004). Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Molecular Ecology, 13, 1143–1155.CrossRefPubMedGoogle Scholar
  54. Ouborg, N. J., Angeloni, F., & Vergeer, P. (2010). An essay on the necessity and feasibility of conservation genomics. Conservation Genetics, 11, 643–653.CrossRefGoogle Scholar
  55. Parmentier, I., Duminil, J., Kuzmina, M., Philippe, M., Thomas, D. W., Kenfack, D., … Hardy, O. J. (2013). How Effective Are DNA Barcodes in the Identification of African Rainforest Trees? PLoS One, 8, e54921. Scholar
  56. Peakall, R., Ruibal, M., & Lindenmayer, D. B. (2003). Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution, 57, 1182–1195.CrossRefPubMedGoogle Scholar
  57. PÉRez-Collazos, E., & CatalÁN, P. (2007). Genetic diversity analysis and conservation implications for the Iberian threatened populations of the irano-turanian relict Krascheninnikovia ceratoides (Chenopodiaceae). Biological Journal of the Linnean Society, 92, 419–429. Scholar
  58. Pinares, A., González-Astorga, J., Vovides, A. P., Lazcano, J., & Vendrame, W. A. (2009). Genetic diversity of the endangered endemic Microcycas calocoma (Miq.) A. DC (Zamiaceae, Cycadales): Implications for conservation. Biochemical Systematics and Ecology, 37, 385–394. Scholar
  59. Ponce-Reyes, R., Nicholson, E., Baxter, P. W. J., Fuller, R. A., & Possingham, H. (2013). Extinction risk in cloud forest fragments under climate change and habitat loss. Diversity and Distributions, 19, 518–529. Scholar
  60. Powell, W., Machray, G. C., & Provan, J. (1996). Polymorphism revealed by simple sequence repeats. Trends in Plant Science, 1, 215–222.CrossRefGoogle Scholar
  61. Pradeep Reddy, M., Sarla, N., & Siddiq, E. A. (2002). Inter simple sequence repeat (ISSR) polymorphism and its application in plant breeding. Euphytica, 128, 9–17. Scholar
  62. Quazi, M., Al-Riyami, W., Al-Jadeedi, S., Ambu-Saidi, H., Ali, A., Al-busaidi, H., … Hakkim, F. (2014). Conservation of omani frankincense (boswellia sacra, burseraceae) through plant tissue culture approach. Journal of Science, 4, 632–636.Google Scholar
  63. Raffaelli, M., Mosti, S., & Tardelli, M. (2003). The Frankincense Tree (Boswellia sacra Flueck., Burseraceae) in Dhofar, southern Oman: field-investigations on the natural populations. Webbia, 58, 133–149. Scholar
  64. Raffaelli, M., Mosti, S., & Tardelli, M. (2006). Boswellia sacra Flueck. (Burseraceae) in the Hasik area (Eastern Dhofar, Oman) and a list of the surrounding flora. Webbia, 61, 245–251. Scholar
  65. Raffaelli, M., Tardelli, M., & Mosti, S. (2008). Preserving and restoring the frankincense tree (Boswellia sacra) at Wadi Doka: a work in progress. A port in Arabia between Rome and the Indian Ocean (3rd C BC–5th C. AD). Khor Rori Report, 2, 715–723.Google Scholar
  66. Raju, A., Lakshmi, P. V., Ramana, K. V., & Chandra, P. H. (2012). Entomophily, ornithophily and anemochory in the self-incompatible Boswellia ovalifoliolata Bal. & Henry (Burseraceae), an endemic and endangered medicinally important tree species. Journal of Threatened Taxa, 4, 2673–2684.CrossRefGoogle Scholar
  67. Rakoczy-Trojanowska, M., & Bolibok, H. (2004). Characteristics and a comparison of three classes of microsatellite-based markers and their application in plants. Cellular & Molecular Biology Letters, 9, 221–238.Google Scholar
  68. Ratnam, W., Rajora, O. P., Finkeldey, R., Aravanopoulos, F., Bouvet, J.-M., Vaillancourt, R. E., … Vinson, C. (2014). Genetic effects of forest management practices: global synthesis and perspectives. Forest Ecology and Management, 333, 52–65.CrossRefGoogle Scholar
  69. Rijkers, T., Ogbazghi, W., Wessel, M., & Bongers, F. (2006). The effect of tapping for frankincense on sexual reproduction in Boswellia papyrifera. Journal of Applied Ecology, 43, 1188–1195. Scholar
  70. Schaal, B. A., Hayworth, D. A., Olsen, K. M., Rauscher, J. T., & Smith, W. A. (1998). Phylogeographic studies in plants: problems and prospects. Molecular Ecology, 7, 465–474. Scholar
  71. Segelbacher, G., Cushman, S. A., Epperson, B. K., Fortin, M.-J., Francois, O., Hardy, O. J., … Manel, S. (2010). Applications of landscape genetics in conservation biology: concepts and challenges. Conservation Genetics, 11, 375–385.CrossRefGoogle Scholar
  72. Slatkin, M. (1987). Gene flow and the geographic structure of natural populations. Science, 236, 787–792.CrossRefPubMedGoogle Scholar
  73. Smouse, P. E., Peakall, R., & Gonzales, E. (2008). A heterogeneity test for fine-scale genetic structure. Molecular Ecology, 17, 3389–3400.CrossRefPubMedGoogle Scholar
  74. Smulders, M., Cottrell, J., Lefèvre, F., Van der Schoot, J., Arens, P., Vosman, B., … Castiglione, S. (2008). Structure of the genetic diversity in black poplar (Populus nigra L.) populations across European river systems: consequences for conservation and restoration. Forest Ecology and Management, 255, 1388–1399.CrossRefGoogle Scholar
  75. Sreekumar, V., & Renuka, C. (2006). Assessment of genetic diversity in Calamus thwaitesii BECC.(Arecaceae) using RAPD markers. Biochemical Systematics and Ecology, 34, 397–405.CrossRefGoogle Scholar
  76. Sunnichan, V., Mohan Ram, H., & Shivanna, K. (2005). Reproductive biology of Boswellia serrata, the source of salai guggul, an important gum-resin. Botanical Journal of the Linnean Society, 147, 73–82.CrossRefGoogle Scholar
  77. Teshome, M. (2013). Structure and composition of woody plants in Boswellia dominated woodland of Western Ethiopia. MSc Thesis. Wageningen University: The Netherlands.Google Scholar
  78. Teshome, M., Eshete, A., & Bongers, F. (2017). Uniquely regenerating frankincense tree populations in western Ethiopia. Forest Ecology and Management, 389, 127–135. Scholar
  79. Tolera, M., Sass-Klaassen, U., Eshete, A., Bongers, F., & Sterck, F. J. (2013). Frankincense tree recruitment failed over the past half century. Forest Ecology and Management, 304, 65–72.CrossRefGoogle Scholar
  80. Vekemans, X., & Hardy, O. J. (2004). New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology, 13, 921–935.CrossRefPubMedGoogle Scholar
  81. Verde, I., Abbott, A. G., Scalabrin, S., Jung, S., Shu, S., Marroni, F., … Cattonaro, F. (2013). The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nature Genetics, 45, 487.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Ahmed Al-Harrasi
    • 1
  • Abdul Latif Khan
    • 1
  • Sajjad Asaf
    • 1
  • Ahmed Al-Rawahi
    • 1
  1. 1.University of NizwaNizwaOman

Personalised recommendations