Abstract
The distribution of genetic diversity among natural populations is significantly shaped by geographical and environmental heterogeneity. The key objectives of this study were to outline the population genetic structure and to investigate the effects of historical and current factors in shaping the population structure of an endemic tropical tree, Hagenia abyssinica. We used 11 polymorphic microsatellites to estimate genetic variability and evaluate gene flow among natural populations of H. abyssinica. Further, we employed ecological niche modeling approaches, to analyze the demographic history and map potential distributions of H. abyssinica during the Last Glacial Maximum and the present. Significant levels of genetic diversity (H O = 0.477, H E = 0.439) were observed among the sampled locations. High coefficient of genetic differentiation (F ST = 0.32) and considerable genetic variation within the sampled locations (68.01%) were detected. Our results indicated the existence of three genetic groups with limited gene exchange and revealed positive correlations (r = 0.425, P < 0.05) between genetic diversity and geo-graphic distance. The ecological niche modeling (ENM) results support the existence of three distribution zones during the Last Glacial Maximum (LGM), with high probability of occurrence (0.8–1.0), and indicated slight distribution disturbances during and after the LGM. The fundamental patterns of genetic diversity and population structuring of H. abyssinica result from a combination of both environmental and geographical factors, including long-term isolation by distance and characteristic life history of this species. Our ENM results identified three zones that could have served as glacial refugia for this species and lay a foundation for further studies, outlining demographic histories and population structures of Afromontane species.
Similar content being viewed by others
References
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
Aguinagalde I, Hampe A, Mohanty A, MartínJP DJ, Petit RJ (2005) Effects of life‐history traits and species distribution on genetic structure at maternally inherited markers in European trees and shrubs. J Biogeogr 32:329–339
Allal F, Sanou H, Millet L, Vaillant A, Camus-Kulandaivelu L, Logossa Z, Lefevre F, Bouvet J (2011) Past climate changes explain the phylogeography of Vitellaria paradoxa over Africa. Heredity 107:174–186
Assefa A, Ehrich D, Taberlet P, Nemomissa S, Brochmann C (2007) Pleistocene colonization of afro-alpine ‘sky islands’ by the arctic-alpine Arabis alpina. Heredity 99:133–142
Ayele TB, Gailing O, Umer M, Finkeldey R (2009) Chloroplast DNA haplotype diversity and postglacial recolonization of Hagenia abyssinica (Bruce) J. F. Gmel. in Ethiopia. Plant Syst Evol 280:175–185
Ayele TB, Gailing O, Finkeldey R (2011) Assessment and integration of genetic, morphological and demographic variation in Hagenia abyssinica (Bruce) J. F. Gmel to guide its conservation. J Nat Conserv 19:8–17
Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345
Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773
Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326
Bonnefille R, Riollet G, Buchet G, Icole M, Lafont R, Arnold M, Jolly D (1995) Glacial anterglacial record from intertropical Africa, high resolution pollen and carbon data at Rusaka, Burundi. Quat Sci Rev 14:917–936
e Souza HAV, Collevatti RG, Lima-Ribeiro MS, De Lemos-Filho JP, Lovato MB (2016) A large historical refugium explains spatial patterns of genetic diversity in a Neotropical savanna tree species. Ann Bot, mcw096
Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Ehrich D, Gaudeul M, Assefa A, Koch MA, Mummenhoff K, Nemomissa S, Consortium I, Brochmann C (2007) Genetic consequences of Pleistocene range shifts: contrast between the Arctic, the Alps and the East African mountains. Mol Ecol 16:2542–2559
Elith J, Graham CH, Anderson RP, Dudı’k M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR et al (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151
Epperson BK, Li TQ (1996) Measurement of genetic structure within populations using Moran’s spatial autocorrelation statistics. Proc Natl Acad Sci USA 93:10528–10532
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
Excoffier L, Lischer HE (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
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Feyissa T, Nybom H, Bartish IV, Welander M (2007) Analysis of genetic diversity in the endangered tropical tree species Hagenia abyssinica using ISSR markers. Genet Resour Crop Evol 54:947–958
Feyssa DH, Abdeta C, Berhan T, Sharma M (2015) Medicinal plants use and conservation practices in Jimma Zone, South West Ethiopia. Int J Biodivers Conserv 7:202–210
Gichira AW, Long ZC, Hu GW, Gituru RW, Wang QF, Chen JM (2016) Development of microsatellite markers in Hagenia abyssinica (Bruce) J. F. Gmel, an endangered tropical tree of eastern Africa, using next-generation sequencing. Genetics and molecular research: GMR, 15
Gizaw A, Kebede M, Nemomissa S, Ehrich D, Bekele B, Mirré V, Popp M, Brochmann C (2013) Phylogeography of the heathers Erica arborea and E. trimera in the afro-alpine ‘sky islands’ inferred from AFLPs and plastid DNA sequences. Flora-Morphology, Distribution, Functional Ecology of Plants 208:453–463
Gottelli D, Marino J, Sillero‐Zubiri C, Funk SM (2004) The effect of the last glacial age on speciation and population genetic structure of the endangered Ethiopian wolf (Canis simensis). Mol Ecol 13:2275–2286
Gugger PF, Ikegami M, Sork VL (2013) Influence of late Quaternary climate change on present patterns of genetic variation in valley oak, Quercus lobata Née. Mol Ecol 22:3598–3612
Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186
Hale ML, Burg TM, Steeves TE (2012) Sampling for microsatellite-based population genetic studies: 25–30 individuals per population is enough to accurately estimate allele frequencies. PLoS One 9:e45170
Hall JB (1973) Vegetational zones on the southern slopes of Mount Cameroon. Vegetation 27:49–69
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, MA, pp 43–63
Hamrick JL, Godt M (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond B 351:1291-1298
Hedberg O (1969) Evolution and speciation in a tropical high mountain flora. Biol J Linn Soc 1:135–148
Hedberg O (1970) Evolution of the afroalpine flora. Biotropica:16–23
Hewitt GM (1999) Post‐glacial re‐colonization of European biota. Biol J Linn Soc 68:87–112
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978
Iloh AC, Ogundipe OT (2016) Using ecological niche modelsto plan conservation in a changing environment: a case for the plant Chasmanthera dependens Hochst (Menispermaceae) in West Africa. J Ecol Nat Environ 8:1–8
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:1
Kabede M, Ehrich D, Taberlet P, Nemomissa S, Brochmann C (2007) Phylogeography and conservation genetics of a giant lobelia (Lobelia giberroa) in Ethiopian and tropical East African mountains. Mol Ecol 16:1233–1243
Kadu C, Schueler S, Konrad H, Muluvi G, Eyog‐Matig O, Muchugi A, Williams V, Ramamonjisoa L, Kapinga C, Foahom B (2011) Phylogeography of the Afromontane Prunus africana reveals a former migration corridor between East and West African highlands. Mol Ecol 20:165–178
Kadu CA, Konrad H, Schueler S, Muluvi GM, Eyog-Matig O, Muchugi A, Williams VL, Ramamonjisoa L, Kapinga C, Foahom B (2013) Divergent pattern of nuclear genetic diversity across the range of the Afromontane Prunus africana mirrors variable climate of African highlands. Ann Bot 111:47–60
Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189
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
Koch MA, Kiefer C, Ehrich D, Vogel J, Brochmann C, Mummenhoff K (2006) Three times out of Asia Minor: the phylogeography of Arabis alpina L.(Brassicaceae). Mol Ecol 15:825–839
Kumilign A (2005) Estimation of sex-related genetic diversity of Hagenia abyssinica (Bruce) J.F. Gmel using random amplified polymorphic DNA (RAPD) markers. aau
Lamb AL, Leng MJ, Mohammed MU, Lamb HF (2004) Holocene climate and vegetation change in the Main Ethiopian Rift Valley, inferred from the composition (C/N and δ 13 C) of lacustrine organic matter. Quat Sci Rev 23:881–891
Linder HP (2014) The evolution of African plant diversity. Front Ecol Evol 2:1–14
Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95
Mccarty JP (2001) Consecuencias Biológicas de Cambios Climáticos Recientes. Conserv Biol 15:320–331
Merrow C, Smith MJ, Silander JA (2013) A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36:1058–1069
Mihretie Z, Schueler S, Konrad H, Bekele E, Geburek T (2015) Patterns of genetic diversity of Prunus africana in Ethiopia: hot spot but not point of origin for range-wide diversity. Tree Genet Genomes 11:1–13
Negash L. (1995) Indigenous trees of Ethiopia: biology, uses and propagation techniques. Addis Ababa: Department of Biology, Addis Ababa University 285p
Nei M (1972) Genetic distance between populations. Am Nat:283–292
Olago D, Street-Perrott F, Perrott R, Ivanovich M, Harkness D (1999) Late Quaternary glacial-interglacial cycle of climatic and environmental change on Mount Kenya, Kenya. J Afr Earth Sci 29:593–618
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
Peterson AT (2003a) Predicting the geography of species’ invasions via ecological niche modeling. Q Rev Biol 78:419–433
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rousset F (2008) genepop’007: a complete re‐implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106
Scantlebury CE, Peachey L, Hodgkinson J, Matthews JB, Trawford A, Mulugeta G, Tefera G, Pinchbeck GL (2013) Participatory study of medicinal plants used in the control of gastrointestinal parasites in donkeys in eastern Shewa and Arsi zones of Oromia region, Ethiopia. BMC Vet Res 9:1
Seburanga J, Nsanzurwimo A, Folega F (2014) Status of Hagenia forest in the Parc National des Volcans, Rwanda: a review of historical records. J Ecol Nat Environ 6:170–182
Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst:393–430
Stockwell D (2006) Niche modeling: predictions from statistical distributions, CRC Press
van Breugel P, Kindt R, Lillesø JPB, Bingham M, Demissew S, Dudley C, Friis I, Gachathi F, Kalema J, Mbago F, Moshi HN, Mulumba J, Namaganda M, Ndangalasi HJ, Ruffo CK, Védaste M, Jamnadass R, Graudal L (2015) Potential natural vegetation map of eastern Africa (Burundi, Ethiopia, Kenya, Malawi, Rwanda, Tanzania, Uganda and Zambia). Version 2.0. Forest & Landscape Denmark and World Agroforestry Centre (ICRAF). URL: http://vegetationmap4africa.org
Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO‐CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Vivero JL, Demissew S, Kelbessa E (2005) The red list of endemic trees et shrubs of Ethiopia and Eritrea. Fauna et Flora International
White F (1981) The history of the Afromontane archipelago and the scientific need for its conservation. Afr J Ecol 19:33–54
Wisz MS, Hijmans R, Li J, Peterson AT, Graham C, Guisan A (2008) Effects of sample size on the performance of species distribution models. Divers Distrib 14:763–773
Woldemariam TZ, Fell AF, Linley PA, Bibby MC, Phillips RM (1992) Evaluation of the anti-tumour action and acute toxicity of kosins from Hagenia abyssinica. J Pharm Biomed Anal 10:555–560
Wondimu T, Gizaw A, Tusiime FM, Masao CA, Abdi AA, Gussarova G, Popp M, Nemomissa S, Brochmann C (2014) Crossing barriers in an extremely fragmented system: two case studies in the afro-alpine sky island flora. Plant Syst Evol 300:415–430
Wu H, Guiot J, Brewer S, Guo Z (2007) Climatic changes in Eurasia and Africa at the Last Glacial Maximum and mid-Holocene: reconstruction from pollen data using inverse vegetation modelling. Clim Dyn 29:211–229
Young JAT, Hastenrath S (1987) Glaciers of the Middle East and Africa - Glaciers of Africa, In: Williams RG. Ferrigno JG (ed), Satellite image atlas of glaciers of the world, U.S Government Printing Office 1386-G-3; U.S. Geological Survey, G49-G70
Acknowledgments
The authors acknowledge Geoffrey Mwachala and Daniel Miyawa of the National Museums of Kenya for their support in fieldwork, Zhicheng Long for his assistance in data analysis, Cornelius Mulili for proofreading, and Paul Gugger for his valuable comments and suggestions that improved an earlier version of this manuscript. This research was funded by the Sino-Africa Joint Research Center (Nos. Y323771W07 and SAJC201322).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by V. Decroocq
Data archiving declaration: The dataset of microsatellite loci used in this study is given in the Online Resource 1
Electronic supplementary material
Additional Supporting Information may be found in the online version of this article:
Online Resource 1
Occurrence points of Hagenia abyssinica and microsatellite dataset used in this study. (XLSX 26.4 kb)
Online Resource 2
Supporting details of AMOVA, STRUCTURE and MIGRATE-n analyses. (DOCX 54.1 kb)
Rights and permissions
About this article
Cite this article
Gichira, A.W., Li, ZZ., Saina, J.K. et al. Demographic history and population genetic structure of Hagenia abyssinica (Rosaceae), a tropical tree endemic to the Ethiopian highlands and eastern African mountains. Tree Genetics & Genomes 13, 72 (2017). https://doi.org/10.1007/s11295-017-1156-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-017-1156-6