Skip to main content

Advertisement

SpringerLink
Log in

Landscape genetic structure of Olea europaea subsp. cuspidata in Ethiopian highland forest fragments

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Understanding patterns of genetic diversity at the landscape scale will enhance conservation and management of natural populations. Here we analyzed the genetic diversity, population connectivity, and spatial genetic structure among subpopulations and age groups of Olea europaea subsp. cuspidata, a cornerstone species of the Afromontane highlands. The study was conducted at the landscape level within a radius of approximately 4 km, as well as on a fine scale (intensive study plot) of less than 300 m radius. In total 542 samples from four natural subpopulations in northwestern Ethiopia were analyzed using ten nuclear microsatellite markers. Inbreeding was higher in smaller populations. No genetic difference was detected among cohorts of different tree sizes in the intensive studied plot. Average population differentiation was low but significant (F ST  = 0.016). Landscape genetic analysis inferred two groups: the most distant subpopulation WE located less than 4 kms from the other three subpopulations formed a separate group. Sixty-four percent of the total migrants were shared among the three latter subpopulations, which are spatially clustered. Immigrants were non-randomly distributed inside of the intensive study plot. Significant spatial genetic structure (SGS) was found both at the landscape scale and in the intensive study plot, and adults showed stronger SGS than young trees. An indirect estimate of 220 m as mean gene dispersal distance was obtained. We conclude that even under fragmentation migration is not disrupted in wild olive trees and that large protected populations at church forests are very important to conserve genetic resources. However, the higher level of inbreeding and evidence for population bottlenecks in the small populations, as well as the persisting heavy pressure on most remaining populations, warrants quick action to maintain genetic diversity of wild olive in the Ethiopian highlands.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abiyu HA (2012) The role of seed dispersal, exclosures, nurse shrubs and trees around churches and farms for restoration of ecosystem diversity and productivity in the Ethiopian highlands. Dissertation, University of Natural Resources and Life sciences, Vienna

  • Abiyu A, Teketay D, Glatzel G, Gratzer G (2015) Tree seed dispersal by African civets in the Afromontane highlands: too long a latrine to be effective for tree population dynamics. Afr J Ecol 53:588–591

    Article  Google Scholar 

  • Aerts R, Van Overtveld K, November E, Wassie A, Abiyu A, Demissew S, Daye DD, Giday K, Haile M, TewoldeBerhan S, Teketay D, Teklehaimanot Z, Binggeli P, Deckers J, Friis I, Gratzer G, Hermy M, Heyn M, Honnay O, Paris M, Sterck FJ, Muys B, Bongers F, Healey JR (2016) Conservation of the Ethiopian church forests: threats, opportunities and implications for their management. Sci Total Environ. doi:10.1016/j.scitotenv.2016.02.034

    PubMed  Google Scholar 

  • Anderson CD, Epperson BK, Fortin MJ, Holderegger R, James PMA, Rosenberg MS, Scribner KT, Spear S (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575

    Article  PubMed  Google Scholar 

  • Baali-Cherif D, Besnard G (2005) High genetic diversity and clonal growth in relict populations of Olea europaea subsp. laperrinei (Oleaceae) from Hoggar, Algeria. Ann Bot 96:823–830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balkenhol N, Cushman S, Storfer A, Waits L (2016) Landscape genetics: concepts, methods, applications, 1st edn. Wiley Blackwell, London

    Google Scholar 

  • Bekele T (2005) Recruitment, survival and growth of Olea europeaea subsp. cuspidata seedlings and juveniles in dry Afromontane forests of northern Ethiopia. Trop Ecol 46:113–126

    Google Scholar 

  • Besag J (1977) Contribution to the discussion of Dr. Replay’s paper. J Roy Stat Soc B 39:193–195

    Google Scholar 

  • Besnard G, Khadari B, Villemur P, Bervillé A (2000) Cytoplasmic male sterility in the olive (Olea europaea L.). Theor Appl Genet 100:1018–1024

    Article  Google Scholar 

  • Besnard G, Christin PA, Baali-Cherif D, Bouguedoura N, Anthelme F (2007) Spatial genetic structure in the Laperrinei’s olive (Olea europaea subsp. laperrinei), a long living tree from the central Saharan mountains. Heredity 99:649–657

    Article  CAS  PubMed  Google Scholar 

  • Besnard G, García-Verdugo C, Rubio De Casas R, Treier UA, Galland N, Vargas P (2008) Polyploidy in the olive complex (Olea europaea): evidence from flow cytometry and nuclear microsatellite analyses. Ann Bot 101:25–30

    Article  CAS  PubMed  Google Scholar 

  • Besnard G, Baali-Cherif D, Bettinelli-Riccardi S, Bouguedoura N (2009) Pollen-mediated gene flow in a highly fragmented landscape: consequences for defining a conservation strategy of the relict Laperrine’s olive. CR Biol 332:662–672

    Article  Google Scholar 

  • Besnard G, El Bakkali A, Haouane H, Baali-Cherif D, Moukhli A, Khadari B (2013) Population genetics of Mediterranean and Saharan olives: geographic patterns of differentiation and evidence for early generation of admixture. Ann Bot 112:1293–1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breton C, Bervillé A (2013) From the olive flower to the drupe: flower types, pollination, self and inter-compatibility and fruit set. In: Barbara S (ed) The Mediterranean genetic code—grapevine and olive, In Tech, pp 291–213

  • Breton C, Tersac M, Bervillé A (2006) Genetic diversity and gene flow between the wild olive (oleaster, Olea europaea L.) and the olive: several Plio-Pleistocene refuge zones in the Mediterranean basin suggested by simple sequence repeats analysis. J Biogeogr 33:1916–1928

    Article  Google Scholar 

  • Breton, CM, Farinelli D, Shafiq S, Heslop-Harrison JS, Sedgley M, Bervillé AJ (2014) The self-incompatibility mating system of the olive (Olea europaea L.) functions with dominance between S- alleles. Tree Genet Genom 10:1055–1067

    Article  Google Scholar 

  • Carriero F, Fontanazza G, Cellini F, Giorio G (2002) Identification of simple sequence repeats (microsatellites) in olive (Olea europaea L.). Theor Appl Genet 104:301–307

    Article  CAS  PubMed  Google Scholar 

  • Chybicki IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. J Hered 100:106–113

    Article  CAS  PubMed  Google Scholar 

  • Cipriani G, Marrazzo MT, Marconi R, Cimato A, Testolin R (2002) Microsatellite markers isolated in olive (Olea europaea L.) are suitable for individual fingerprinting and reveal polymorphism within ancient cultivars. Theor Appl Genet 104:223–228

    Article  CAS  PubMed  Google Scholar 

  • Collevatti RG, Estolano R, Rebeiro ML, Rabelo SG, Lima EJ, Munhoz CBR (2014) High genetic diversity and contrasting fine-scale spatial genetic structure in four seasonally dry tropical forest tree species. Plant Syst Evol 300:1671–1681

    Article  Google Scholar 

  • Cruse-Sanders JM, Hamrick JL (2004) Spatial and genetic structure within populations of wild American ginseng (Panax quinquefolius L., Araliaceae). J Hered 95:309–321

    Article  CAS  PubMed  Google Scholar 

  • Cuneo P, Leishman MR (2006) African olive (Olea europeaea subsp. cuspidata) as an environmental weed in Eastern Australia: a review. Cunninghamia 9:545–577

    Google Scholar 

  • Darbyshire I, Lamb H, Umer M (2003) Forest clearance and regrowth in northern Ethiopia during the last 3000 years. Holocene 13:537–546

    Article  Google Scholar 

  • De La Rosa R, James CM, Tobutt KR (2002) Isolation and characterization of polymorphic microsatellites in olive (Olea europaea L.) and their transferability to other genera in the Oleaceae. Mol Ecol Notes 2:265–267

    Article  Google Scholar 

  • Desalegn G, Tadesse W (2010) Major characteristics and potential uses of Eucalyptus timber species grown in Ethiopia. In: Gil L, Tadesse W, Tolosana E, López R (eds) Eucalyptus species management, history, status and trends in Ethiopia. Proceedings of the congress, Ethiopian institute of agricultural research, Addis Ababa, pp 29–52

  • Dias PC (1996) Sources and sinks in population biology. Trends Ecol Evol 11:326–330

    Article  CAS  PubMed  Google Scholar 

  • Doligez A, Baril C, Joly HI (1998) Fine-scale spatial genetic structure with nonuniform distribution of individuals. Genetics 148:905–919

    CAS  PubMed  PubMed Central  Google Scholar 

  • Escobar-Páramo P (2000) Microsatellite primers for the wild brown capuchin monkey Cebus apella. Mol Ecol 9:107–118

    Article  PubMed  Google Scholar 

  • Fuchs EJ, Hamrick JL (2010) Spatial genetic structure within size classes of the endangered tropical tree Guaiacum sanctum (Zygophyllaceae). Am J Bot 97:1200–1207

    Article  PubMed  Google Scholar 

  • García-Verdugo C, Fay MF, Granado-Yela C, Rubio de Casas RR, Balaguer L, Besnard G, Vargas P (2009) Genetic diversity and differentiation processes in the ploidy series of Olea europaea L.: a multiscale approach from subspecies to insular populations. Mol Ecol 18:454–467

    Article  PubMed  Google Scholar 

  • García-Verdugo C, Forrest AD, Balaguer L, Fay MF, Vargas P (2010) The relevance of gene flow in metapopulation dynamics of an oceanic island endemic, Olea europaea subsp. guanchica. Evolution 64:3525–3536

    Article  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, version 2.9.3. University of Lausanne. http://www.unil.ch/izea/softwares/fstat.html. Accessed 26 June 2016

  • Green PS (2002) A revision of Olea L. (Oleaceae). Kew Bull 57:91–140

    Article  Google Scholar 

  • Guillot G, Mortier F, Estoup A (2005) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715

    Article  CAS  Google Scholar 

  • Hanski I (1998) Metapopulation dynamics. Nature 396:41–49

    Article  CAS  Google Scholar 

  • Harata T, Nanami S, Yamakura T, Matsuyama S, Chong L, Diway BM, Tan S, Itoh A (2012) Fine-scale spatial genetic structure of ten dipterocarp tree species in a Bornean rain forest. Biotropica 44:586–594

    Article  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hardy OJ, Maggia L, Bandou E, Breyne P, Caron H, Chevallier M, Doligez A, Dutech C, Kremer A, Latouch-Hallê C, Troispoux V, Veron V, Degen D (2006) Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Mol Ecol 15:559–571

    Article  CAS  PubMed  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    Article  CAS  PubMed  Google Scholar 

  • Henze PB (2000) Layers of time: a history of Ethiopia. Hurst and Company, London

    Book  Google Scholar 

  • Holderegger R, Buehler D, Gugerli F, Manel S (2010) Landscape genetics of plants. Trends Plant Sci 15:675–683

    Article  CAS  PubMed  Google Scholar 

  • Jones FA, Hubbell SP (2006) Demographic spatial genetic structure of the Neotropical tree, Jacaranda capaia. Mol Ecol 15:3205–3217

    Article  CAS  PubMed  Google Scholar 

  • Jordano P, Garcia C, Godoy JA, Garcia-Castano JL (2007) Differential contribution of frugivores to complex seed dispersal patterns. Proc Natl Acad Sci 104:3278–3282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaniewski D, Boiy T, Terral JF, Khadari B, Besnard G (2012) Primary domestication and early uses of the emblematic olive tree: palaeobotanical, historical and molecular evidence from the Middle East. Biol Rev 87:885–899

    Article  PubMed  Google Scholar 

  • Keller D, Holderegger R, Van Strien MJ, Bolliger J (2015) How to make landscape genetics beneficial for conservation management? Conserv Genet 16:503–512

    Article  Google Scholar 

  • Latouche-Hallê C, Ramboer A, Bandou E, Caron H, Kremer A (2003) Nuclear and chloroplast genetic structure indicate fine-scale spatial dynamics in a Neotropical tree population. Heredity 91:181–190

    Article  PubMed  Google Scholar 

  • Loiselle BE, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518

    Article  Google Scholar 

  • Nathan R, Schurr FM, Spiegel O, Steinitz O, Trakhtenbrot A, Tsoar A (2008) Mechanisms of long-distance seed dispersal. Trends Ecol Evol 23:638–647

    Article  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nielsen R, Tarpy DR, Reeve HK (2003) Estimating effective paternity number in social insects and the effective number of alleles in a population. Mol Ecol 12:3157–3164

    Article  PubMed  Google Scholar 

  • Oddou-Muratorio S, Demesure-Musch B, Pélissier R, Gouyon PH (2004) Impact of gene flow and logging history on the local genetic structure of a scattered tree species, Sorbus torminalis L. Crantz. Mol Ecol 13:3689–3702

    Article  PubMed  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  CAS  PubMed  Google Scholar 

  • Paetkau D, Slade R, Burdens M, Estoup A (2004) Genetic assignment methods for the direct real-time estimation of migration rate: a simulation based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenALEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-un updatae. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Pinillos V, Cuevas J (2009) Open-pollination provides sufficient level of cross-pollen in Spanish monovarietal olive orchards. Hortscience 44:499–502

    Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Raf A, Eva N, Ives VB, Mintesinot B, Martin H, Bart M (2006) Effects of pioneer shrubs on the recruitment of the fleshy-fruited tree Olea europaea ssp. cuspidata in Afromontane savanna. Appl Veg Sci 9:117–126

    Article  Google Scholar 

  • Rangel TF, Diniz-Filho JAF, Bini LM (2010) SAM: a comprehensive application for spatial analysis in macroecology. Ecography 33:46–50

    Article  Google Scholar 

  • Sefc KM, Lopes MS, Mendonça D, Dos santos MR, Da Cámara Machado ML, Da Cámara Machado A (2000) Identification microsatellite loci in olive (Olea europaea) and their characterization in Italian and Iberian olive trees. Mol Ecol 9:1171–1193

    Article  CAS  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practices of statistics in biological research, 3rd edn. WH Freeman and Company, New York

    Google Scholar 

  • Unger GM, Konrad H, Geburek T (2011) Does spatial genetic structure increase with altitude? An answer from Picea abies in Tyrol, Austria. Plant Syst Evol 292:133–141

    Article  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Compton SG, Chen XY (2011) Fragmentation can increase spatial genetic structure without decreasing pollen-mediated gene flow in a wind-pollinated tree. Mol Ecol 20:4421–4432

    Article  PubMed  Google Scholar 

  • Wassie A, Sterck FJ, Bongers F (2010) Species and structural diversity of church forests in a fragmented Ethiopian highland landscape. J Veg Sci 21:938–948

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  • Yazdani R, Muona O, Rudin D, Szmidt AE (1985) Genetic structure of a Pinus sylvestris L. seed-tree stand and naturally regenerated understory. Forest Sci 7:430–436

    Google Scholar 

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  CAS  PubMed  Google Scholar 

  • Zegeye H, Teketay D, Kelbessa E (2011) Diversity and regeneration status of woody species in Tara Gedam and Abebaye forests, northwestern Ethiopia. J Forest Res 22:315–328

    Article  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge the project “Carbon storage and soil biodiversity in forest landscapes in Ethiopia: Knowledge base and participatory management (Carbo part)” for supporting this work. We also thank C. Dobeš and J.P. George for commenting on the manuscript, T. Thalmayr for help with figures, and D. Fentie for assisting in sample collection.

Author information

Authors and Affiliations

  1. Department of Forest Genetics, Austrian Research Centre for Forests (BFW), Seckendorff-Gudent-Weg 8, 1131, Vienna, Austria

    Alemayehu Kassa, Heino Konrad & Thomas Geburek

  2. Gondar Agricultural Research Center, 1337, Gondar, Ethiopia

    Alemayehu Kassa

Authors
  1. Alemayehu Kassa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heino Konrad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas Geburek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Geburek.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kassa, A., Konrad, H. & Geburek, T. Landscape genetic structure of Olea europaea subsp. cuspidata in Ethiopian highland forest fragments. Conserv Genet 18, 1463–1474 (2017). https://doi.org/10.1007/s10592-017-0993-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-017-0993-z

Keywords

Search

Navigation