Advertisement

Plant Systematics and Evolution

, Volume 300, Issue 3, pp 415–430 | Cite as

Crossing barriers in an extremely fragmented system: two case studies in the afro-alpine sky island flora

  • Tigist Wondimu
  • Abel Gizaw
  • Felly M. Tusiime
  • Catherine A. Masao
  • Ahmed A. Abdi
  • Galina Gussarova
  • Magnus Popp
  • Sileshi Nemomissa
  • Christian Brochmann
Original Article

Abstract

The flora on the afro-alpine sky islands is renowned for extreme fragmentation, representing a unique natural experiment in biogeography. Here we address the roles of isolation and gene flow, in particular across the narrow Rift Valley (the RV barrier) that cuts through the Ethiopian Highlands (EH), and across the vast low-lying landscape that separates EH from the East African mountains (the EH–EA barrier). We inferred the history of two species with different dispersal mechanisms, but with similar geographic ranges and habitats based on Amplified fragment length polymorphisms (AFLPs). Contrary to our predictions, we found that the populations from opposite sides of the RV barrier were less similar than those from opposite sides of the EH–EA barrier, and that only the supposedly short distance-dispersed species (Trifolium cryptopodium) showed a strong signal of secondary gene flow across the RV barrier. In the wind-dispersed Carduus schimperi, we rather found an evidence for the gene flow between differentiated populations inhabiting different EA mountains. Both species harbored little genetic diversity but considerable genetic rarity in several individual mountains, suggesting long-term isolation and bottlenecks during climatically unfavorable periods. Our genetic data corroborate a division of C. schimperi into three subspecies, but with new delimitation of their ranges, and of T. cryptopodium into two intraspecific taxa. Our findings support the idea that stochasticity may play a major role in shaping extremely fragmented ecosystems such as the afro-alpine. After initial colonization of different mountains, periods of isolation may alternate with unpredictable episodes of intermountain gene flow.

Keywords

Afro-alpine flora AFLP Biogeographic stochasticity Carduus schimperi Fragmentation Phylogeography Trifolium cryptopodium 

Notes

Acknowledgments

This study is part of the project ‘AFROALP-II—Afro-alpine ‘sky islands’: genetic versus taxonomic biodiversity, climate change, and conservation’ funded by The Norwegian Programme for Development, Research and Higher Education (NUFU; project no 2007/1058) to S. Nemomissa and C. Brochmann. We thank the other members of the AFROALP-II team for discussions and help during the fieldwork. Sincere thanks are due to Mats Thulin and Manuel Pimentel who determined/verified the identity of our Trifolium and Carduus collections, respectively, and to Desalegn Chala for producing the base map.

References

  1. Arctander P, Johansen C, Coutellec-Vreto MA (1999) Phylogeography of three closely related African bovids (tribe Alcelaphini). Mol Biol Evol 16:1724–1739PubMedCrossRefGoogle Scholar
  2. 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 99:133–142PubMedCrossRefGoogle Scholar
  3. 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 280:175–185CrossRefGoogle Scholar
  4. Barres L, Sanmartin I, Anderson C, Susanna A, Buerki S, Galbany-Casals M, Vilatersana R (2013) Reconstructiong the evolution and biogeographic history of Tribe Cardueae (Compositae). Am J Bot 100:867–882PubMedCrossRefGoogle Scholar
  5. Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273PubMedCrossRefGoogle Scholar
  6. Brühl C (1997) Flightless insects: a test case for historical relationships of African mountains. J Biogeogr 24:233–250CrossRefGoogle Scholar
  7. Chorowicz J (2005) The East African rift system. J Afr Earth Sci 43:379–410CrossRefGoogle Scholar
  8. Coetzee JA (1964) Evidence for a considerable depression of the vegetation belts during the upper Pleistocene on the East African Mountains. Nature 204:564–566CrossRefGoogle Scholar
  9. Désamoré A, Laenen B, Devos N, Popp M, González-Mancebo JM, Carine MA, Vanderpoorten A (2011) Out of Africa: north-westwards Pleistocene expansions of the heather Erica arborea. J Biogeogr 38:164–176CrossRefGoogle Scholar
  10. Ehrich D (2006) AFLPdat: a collection of R functions for convenient handling of AFLP data. Mol Ecol Notes 6:603–604CrossRefGoogle Scholar
  11. Ehrich D (2007) Structure-sum v. 2007: A series of R functions for summarizing the outputs of the program Structure ver. 2.2. Unpublished, available from the author upon requestGoogle Scholar
  12. Ehrich D, Gaudeul M, Assefa A, Koch MA, Mummenhoff K, Nemomissa S, Brochmann C (2007) Genetic consequences of Pleistocene range shifts: contrast between the Arctic, the Alps and the East African mountains. Mol Ecol 16:2542–2559PubMedCrossRefGoogle Scholar
  13. Ellison NW, Liston A, Steiner JJ, Williams WM, Taylor NL (2006) Molecular phylogenetics of the clover genus (Trifolium–Leguminosae). Mol Phylogen Evol 39:688–705CrossRefGoogle Scholar
  14. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  15. Excoffier LLG, Schneider S (2005) ARLEQUIN version 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedCentralGoogle Scholar
  16. Falush D, Stephens M, Pritchard J (2007) Inference of population structure using multilocus genotype data: dominant markers and null allele. Mol Ecol Notes 7:574–578PubMedCentralPubMedCrossRefGoogle Scholar
  17. Fries TCE (1923) Beiträge zur Kenntnis der Flora des Kenia, Mt. Aberdare und Mt. Elgon. Notizblatt des Königl Botanischen Gartens und Museums zu Berlin 8:389–423Google Scholar
  18. Gaudeul M, Taberlet P, Till-Bottraud I (2000) Genetic diversity in an endangered alpine plant, Eryngium alpinum L. (Apiaceae), inferred from amplified fragment length polymorphism markers. Mol Ecol 9:1625–1637Google Scholar
  19. Gillett JB (1952) The genus Trifolium in southern Arabia and in Africa south of the Sahara. Kew Bull 7:367–404CrossRefGoogle Scholar
  20. Gillett JB, Polhill RM, Verdcourt B (1971) Leguminosae IIII. In: Milne-Redhead EE, Polhill RM eds. Flora of Tropical East Africa. London: crown agents for overseas governments and Administrations, pp 1016–1036Google Scholar
  21. 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 13:2275–2286PubMedCrossRefGoogle Scholar
  22. Hedberg O (1957) Afroalpine vascular plants. a taxonomic revision. Symb Bot Ups 15:1–411Google Scholar
  23. Hedberg O (1969) Evolution and speciation in a tropical high mountain flora. Bot J Linn Soc 1:135–148CrossRefGoogle Scholar
  24. Hedberg O (1970) Evolution of the afroalpine flora. Biotropica 2:16–23CrossRefGoogle Scholar
  25. Hedberg O (1986) Origin of the afroalpine flora. In: Vuilleumier F, Monastero M (eds) High altitude tropical biogeography. Oxford University Press, New York, pp 443–468Google Scholar
  26. Hedberg I, Hedberg O (1977) Chromosome numbers of afroalpine and afromontane angiosperms. Bot Not 130:1–24Google Scholar
  27. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806PubMedCrossRefGoogle Scholar
  28. Jeffrey C (1968) Notes on Compositae: III. The cynareae in east tropical Africa. Kew Bull 22:107–140CrossRefGoogle Scholar
  29. Jeffrey C, Beentje HJ (2000) Compositae I. In: Beentje HJ (ed) Flora of tropical East Africa. Balkema, Rotterdam, pp 46–54Google Scholar
  30. Kadu CA, Schueler S, Konrad H, Muluvi GM, Eyog-Matig O, Muchugi A, Williams VL, Ramamonjisoa L, Kapinga C, Foahom B, Katsvanga C, Hafashimana D, Obama C, Geburek T (2011) Phylogeography of the Afromontane Prunus africana reveals a former migration corridor between East and West African highlands. Mol Ecol 20:165–178PubMedCrossRefGoogle Scholar
  31. Kadu CA, Konrad H, Schueler S, Muluvi GM, Eyog-Matig O, Muchugi A, Williams VL, Ramamonjisoa L, Kapinga C, Foahom B, Katsvanga C, Hafashimana D, Obama C, Geburek T (2013) Divergent pattern of nuclear genetic diversity across the range of the Afromontane Prunus africana mirrors variable climate of African highlands. Ann Bot 111:47–60PubMedCrossRefGoogle Scholar
  32. Kazmi SMA (1963) Revision der Gattung Carduus (Compositae), Teil I. Sonderdruck aus den Mitteilungen der Botanischen Staatssamlung München 5:139–198Google Scholar
  33. Kebede 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 16:1233–1243PubMedCrossRefGoogle Scholar
  34. 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 15:825–839PubMedCrossRefGoogle Scholar
  35. Kosman E (2003) Nei’s gene diversity and the index of average differences are identical measures of diversity within populations. Plant Pathol 52:533–535CrossRefGoogle Scholar
  36. Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273PubMedCrossRefGoogle Scholar
  37. Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155PubMedCrossRefGoogle Scholar
  38. Popp M, Gizaw A, Nemomissa S, Suda J, Brochmann C (2008) Colonization and diversification in the African ‘sky islands’ by Eurasian Lychnis L. (Caryophyllaceae). J Biogeogr 35:1016–1029CrossRefGoogle Scholar
  39. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  40. Rohlf F (2000) NTSYSpc: Numerical Taxonomy and Multivariate Analysis System. Version 2.11a. Setauket (NY): Exeter SoftwareGoogle Scholar
  41. Rosenberg NA (2004) DISTRUCT: a program for the graphical disply of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  42. Schönswetter P, Tribsch A (2005) Vicariance and dispersal in the alpine perennial Bupleurum stellatum L. (Apiaceae). Taxon 54:725–732CrossRefGoogle Scholar
  43. Tadesse M (2004) Asteraceae (Compositae). In: Hedberg I, Friss I, Edwards S (eds) Flora of Ethiopia and Eritrea. Addis Ababa University, The National Herbarium, Addis AbabaGoogle Scholar
  44. Thulin M (1989) Subfamily Papilionoideae (Faboideae). In: Edwards S, Hedberg I (eds) Flora of Ethiopia and Eriteria. The National Herbarium, Addis Ababa University/Department of Systematic Botany, Uppsala University, Uppsala, Addis AbabaGoogle Scholar
  45. Van de Peer Y, De Wachter R (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10:569–570PubMedGoogle Scholar
  46. Vos P, Hogers R, Bleekwe M, Reijians M, Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP a new techinique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCentralPubMedCrossRefGoogle Scholar
  47. 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. trimerain the afro-alpine ‘sky islands’ inferred from AFLP and plastid DNA sequences. FLORA 208:453–463Google Scholar
  48. Yalden DW (1983) The extent of high ground in Ethiopia compared to the rest of Africa. SINET 6:35–38Google Scholar

Copyright information

© Springer-Verlag Wien 2013

Authors and Affiliations

  • Tigist Wondimu
    • 1
    • 2
  • Abel Gizaw
    • 1
    • 2
  • Felly M. Tusiime
    • 2
    • 3
  • Catherine A. Masao
    • 2
    • 4
  • Ahmed A. Abdi
    • 2
    • 5
  • Galina Gussarova
    • 2
  • Magnus Popp
    • 2
  • Sileshi Nemomissa
    • 1
  • Christian Brochmann
    • 2
  1. 1.Department of Plant Biology and Biodiversity Management, College of Natural SciencesAddis Ababa UniversityAddis AbabaEthiopia
  2. 2.National Centre for Biosystematics, Natural History MuseumUniversity of OsloOsloNorway
  3. 3.Department of Forestry and Tourism, School of Forestry, Geographical and Environmental SciencesMakerere UniversityKampalaUganda
  4. 4.Institute of Resource Assessment, University of Dar es SalaamDar es SalaamTanzania
  5. 5.National Museums of KenyaNairobiKenya

Personalised recommendations