Conservation Genetics

, Volume 14, Issue 2, pp 427–438 | Cite as

Population genetic structure and connectivity in the endangered Ethiopian mountain Nyala (Tragelaphus buxtoni): recommending dispersal corridors for future conservation

  • Anagaw Atickem
  • Eli K. Rueness
  • Leif E. Loe
  • Dimitar Serbezov
  • Afework Bekele
  • Nils Chr Stenseth
Research Article

Abstract

Habitat fragmentation is an increasing threat to wildlife species across the globe and it has been predicted that future biodiversity will decrease rapidly without the intervention of scientifically-based management. In this study we have applied a landscape genetics approach to suggest a network design that will maintain connectivity among populations of the endangered mountain Nyala (Tragelaphus buxtoni) in the fragmented highlands of Ethiopia. DNA was obtained non-invasively from 328 individuals and genetic population structure and gene flow were estimated using 12 microsatellite markers. In addition, a 475-bp segment of the mitochondrial control region was sequenced for 132 individuals. Potential dispersal corridors were determined from least-cost path analysis based on a habitat suitability map. The genetic data indicated limited gene flow between the sampled mountain Nyala populations of the Bale Massif and the Arsi Massif. The genetic differentiation observed among five sampling areas of the Bale Massif followed a pattern of isolation by distance. We detected no impact of habitat resistance on the gene flow. In the future, however, the current expanding human population in the highlands of Ethiopia may reduce the current mountain Nyala habitat and further limit migration. Hence, maintaining habitat connectivity and facilitating survival of stepping-stone populations will be important for the future conservation of the species. The approach used here may also be useful for the study and conservation of other wildlife species inhabiting areas of increasing human encroachment.

Keywords

Mountain Nyala Landscape genetics Isolation by distance Dispersal corridors Gene flow Least-cost path 

Supplementary material

10592_2013_450_MOESM1_ESM.docx (555 kb)
Supplementary material 1 (DOCX 556 kb)

References

  1. Adriaensen F, Chardon JP, De Blust G, Swinnen E, Villalba S, Gulinck H, Matthysen E (2003) The application of ‘least-cost’ modelling as a functional landscape model. Landscape Urban Plan 64:233–247CrossRefGoogle Scholar
  2. Apio A, Kabasa JD, Ketmaier V, Schroder C, Plath M, Tiedemann R (2010) Female philopatry and male dispersal in a cryptic, bush-dwelling antelope: a combined molecular and behavioural approach. J Zool 280:213–220CrossRefGoogle Scholar
  3. Arnason U, Gullberg A, Johnsson E, Ledje C (1993) The nucleotide sequence of the mitochondrial DNA molecule of the grey seal Halichoerus grypus and a comparison with mitochondrial sequences of other true seals. Mol Ecol 37:323–330Google Scholar
  4. Atickem A, Loe LE, Langangen Ø, Rueness EK, Bekele A, Stenseth NC (2011) Estimating population size and habitat suitability for mountain Nyala in areas with different protection status. Anim Conser 14:409–418CrossRefGoogle Scholar
  5. Beier P, Noss RF (1998) Do habitat corridors provide connectivity? Conserv Biol 12:1241–1252CrossRefGoogle Scholar
  6. Bellemain E, Taberlet P (2004) Improved noninvasive genotyping method: application to brown bear (Ursus arctos) faeces. Mol Ecol Notes 4:519–522CrossRefGoogle Scholar
  7. Bennet AF (2003) Linkages in the landscape: the role of corridors and connectivity in wildlife conservation. IUCN forest conservation programme. Conserving Forest Ecosystems Series No.1Google Scholar
  8. Berger J (2004) The last mile how to sustain long-distance migration in mammals. Cons Biol 18:320–331CrossRefGoogle Scholar
  9. Bonenfant C, Gaillard JM, Klein F, Loison A (2002) Sex- and age-dependent effects of population density on life history traits of red deer Cervus elaphus in a temperate forest. Ecography 25:446–458CrossRefGoogle Scholar
  10. Bonnot N, Gaillard JM, Coulon A, Galan M, Cosson JF, Delorme D, Klein F, Hewison AJM (2009) No difference between the sexes in fine-scale spatial Genetic structure of Roe deer. PLoS One 5:e14436CrossRefGoogle Scholar
  11. Brown L (1969) Observations on the status, habitat, and behavior of the mountain Nyala Tragelaphus buxoni in Ethiopia. Mammalia 33:545–597CrossRefGoogle Scholar
  12. Burkey TV (1995) Faunal collapse in East African game reserves revisited. Biol Conser 71:107–110CrossRefGoogle Scholar
  13. Carlsson J (2008) Effects of microsatellite null alleles on assignment testing. J Heredity 99:616–623CrossRefGoogle Scholar
  14. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Molec Biol Evol 24:621–631PubMedCrossRefGoogle Scholar
  15. Chetkiewicz CLB, Boyce MS (2009) Use of resource selection functions to identify conservation corridors. J Appl Ecol 46:1036–1047CrossRefGoogle Scholar
  16. Chetkiewicz CLB, St Clair CC, Boyce MS (2006) Corridors for conservation: integrating pattern and process. Annu Rev Ecol Evol Syst 37:317–342CrossRefGoogle Scholar
  17. Cushman SA, Landguth EL (2010) Spurious correlations and inference in landscape genetics. Mol Ecol 19:3592–3602PubMedCrossRefGoogle Scholar
  18. Eblate EM, Lughano KJ, Sebastian CD, Peter ML, Knut RH (2011) Polymorphic microsatellite markers for genetic studies of African antelope species. Afr J Biotechnol 10:11817–11820Google Scholar
  19. Evangelista P (2006) Population estimates of Mountain Nyala on the Rise. African Indaba eNewsletter 4Google Scholar
  20. Evangelista P, Swartzinski P, Waltermire R (2007) A profile of the Mountain Nyala (Tragelaphus buxtoni). African Indaba Newsletter 5Google Scholar
  21. Evangelista P, Norman J, Berhanu L, Kumar S, Alley N (2008) Predicting habitat suitability for the endemic mountain Nyala (Tragelaphus buxtoni) in Ethiopia. Wildl Res 35:409–416CrossRefGoogle Scholar
  22. 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
  23. Excoffier L, Lischer HEL (2010) Arlequin suite ver 35: a new series of programs to perform population genetics analyses under Linux Windows. Mol Ecol Resour 10:564–567PubMedCrossRefGoogle Scholar
  24. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515CrossRefGoogle Scholar
  25. Frankham R (2001) Inbreeding and extinction in isolated populations: reply to Elgar and Clode. Cons Biol 15:287–289Google Scholar
  26. Gagneux P, Boesch C, Woodruff DS (1997) Microsatellite scoring errors associated with noninvasive genotyping based on nuclear DNA amplified from shed hair. Mol Ecol 6:861–868PubMedCrossRefGoogle Scholar
  27. Goudet J (2002) FSTAT: a program to estimate and test gene diversities and fixation indices. Version 2932Google Scholar
  28. Graves TA, Farley S, Goldstein MI, Servheen C (2007) Identification of functional corridors with movement characteristics of brown bears on the Kenai Peninsula, Alaska. Landsc Ecol 22:765–772CrossRefGoogle Scholar
  29. Haanes H, Knut HR, Olav R (2011) Sex-biased dispersal in a northern ungulate population. Rangifer 31:139–153CrossRefGoogle Scholar
  30. Hardy O, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  31. Hillman JC (1986) Conservation in the Bale Mountains National Park, Ethiopia. Oryx 20:89–94CrossRefGoogle Scholar
  32. Hillman JC (1993) Ethiopia: Compendium of Wildlife Conservation Information. Report to Ethiopian Wildlife Conservation Organization, Addis AbabaGoogle Scholar
  33. Jenkins DG, Carey M, Czerniewska J et al (2010) A meta-analysis of isolation by distance: relic or reference standard for landscape genetics? Ecography 33:315–320Google Scholar
  34. Joppa L, Loarie S, Pimm S (2008) On the protection of “protected areas”. PNAS 105:66–73CrossRefGoogle Scholar
  35. Kingdon J (1997) The Kingdon Field Guide to African Mammals. Academic Press, Natural World, London and New YorkGoogle Scholar
  36. Li H, Li D, Li T, Qiao Q, Yang J, Zhang H (2010) Application of least-cost path model to identify a giant panda dispersal corridor network after the Wenchuan earthquake-case study of Wolong Nature Reserve in China. Ecol Model 221:944–952CrossRefGoogle Scholar
  37. Lydekker R (1910) New antelope Tragelaphus buxtoni. Nature 85:19Google Scholar
  38. Maehr DS, Land ED, Shindle DB, Bass OL, Hoctor TS (2002) Florida panther dispersal and conservation. Biol Conserv 106:187–197CrossRefGoogle Scholar
  39. Magliocca F, Querouil S, Gautier-Hion A (2002) Grouping patterns, reproduction, and dispersal in a population of sitatungas (Tragelaphus spekei gratus). Can J Zool 80:245–250CrossRefGoogle Scholar
  40. Mantel NA (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  41. Margules C, Pressey R (2000) Systematic conservation planning. Nature 405:243–253PubMedCrossRefGoogle Scholar
  42. Mekonnen A, Bekele A, Hemson G, Teshome E, Atickem A (2010) Population size and habitat preference of the Vulnerable Bale monkey Chlorocebus djamdjamensis in Odobullu forest and its distribution across the Bale Mountains Ethiopia. Oryx 44:558–563CrossRefGoogle Scholar
  43. Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518CrossRefGoogle Scholar
  44. Murphy MA, Evans JS, Storfer A (2010) Quantifying Bufo boreas connectivity in Yellowstone National Park with landscape genetics. Ecology 91:252–261PubMedCrossRefGoogle Scholar
  45. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  46. Nei M, Chesser RK (1983) Estimation of fixation indices and gene diversities. Ann Hum Genet 47:253–259PubMedCrossRefGoogle Scholar
  47. Newman D, Tallmon DA (2001) Experimental evidence for beneficial fitness effects of gene flow in recently isolated populations. Conserv Biol 15:1054–1063CrossRefGoogle Scholar
  48. Oksanen J, Kindt R, O’Hara RB (2005) Vegan Community Ecology Package. Version 16–10 http://ccoulufi/jarioksa/. Accessed 10 Sept 2011
  49. Owen-Smith N (1993) Comparative mortality rates of male and female kudus: the costs of sexual size dimorphism. J Anim Ecol 62:428–440CrossRefGoogle Scholar
  50. Paetkau D, Calvert W, Stirling I, Strobek C (1995) Variation in genetic diversity across the range of North American brown bears. Conser Biol 12:418–429Google Scholar
  51. Peréz-Espona S, Pérez-Barberia FJ, Jiggins CD, Gordon IJ, Pemberton JM (2010) Variable extent of sex-biased dispersal in a strongly polygynous mammal. Mol Ecol 19:3101–3113PubMedCrossRefGoogle Scholar
  52. Peréz-Gonzalez J, Carranza J (2009) Female-biased dispersal under conditions of low male mating competition in a polygynous mammal. Mol Ecol 18:4617–4630PubMedCrossRefGoogle Scholar
  53. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  54. Pritchard JK, Wen X, Falush D (2007) Documentation for structure software Version 22. http://pritchbsduchicagoedu/software/structure22/readmepdf. Accessed 4 Sept 2011
  55. Pullinger MG, Johnson CJ (2010) Maintaining or restoring connectivity of modified landscapes: evaluating the least-cost path model with multiple sources of ecological information. Landsc Ecol 25:1547–1560CrossRefGoogle Scholar
  56. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  57. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Cons Biol 17:230–237CrossRefGoogle Scholar
  58. Refera B, Bekele A (2004) Population status and structure of mountain Nyala in the Bale Mountains National Park, Ethiopia. Afr J Ecol 42:1–7CrossRefGoogle Scholar
  59. Reynolds AJ, Lawrence C, Cserhalmi-Friedman PB, Christiano AM, Jahoda CAB (1999) Restoration of an inbred adder population. Nature 402:34–35CrossRefGoogle Scholar
  60. Rouget M, Cowling RM, Lombard AT, Knight AT, Kerley GIH (2006) Designing large-scale conservation corridors for pattern and process. Cons Biol 20:549–561CrossRefGoogle Scholar
  61. Rousset F (1997) Genetic differentiation and estimation of gene flow from F- statistics under isolation by distance. Genetics 145:1219–1228PubMedGoogle Scholar
  62. Rousset F (2008) GENEPOP’ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106PubMedCrossRefGoogle Scholar
  63. Schemske DW, Husband BC, Ruckelshaus MH, Goodwillie C, Parker IM, Bishop JG (1994) Evaluating approaches to the conservation of rare and endangered plants. Ecology 75:586–606CrossRefGoogle Scholar
  64. Segelbacher G, Cushman S, Epperson B et al (2010) Landscape Genetics: concepts and Challenges in a Conservation Context. Conserv Genet 11:375–385CrossRefGoogle Scholar
  65. Sillero-Zubiri C (2008) Tragelaphus buxtoni In: IUCN 2011 IUCN Red List of Threatened Species. Version 20111 (www.iucnredlist.org) Downloaded on 26 July 2011
  66. Simonsen BT, Siegismund HR, Arctander P (1998) Population structure of African buffalo inferred from mtDNA sequences and microsatellite loci: high variation but low differentiation. Mol Ecol 7:225–237PubMedCrossRefGoogle Scholar
  67. Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632CrossRefGoogle Scholar
  68. Soulé ME, Wilcox BA, Holtby C (1979) Benign neglect: a model of faunal collapse in the Game Reserves of East Africa. Biol Conserv 15:259–272CrossRefGoogle Scholar
  69. Spear SF, Balkenhol N, Fortin MJ, Mcrae BH, Scribner K (2010) Use of resistance surfaces for landscape genetics studies: considerations for parameterization and analysis. Mol Ecol 19:3576–3591PubMedCrossRefGoogle Scholar
  70. Stephanie KS, Tobias SK, Karin F, Thorsten W (2011) Analyzing the effect of stepping stones on target patch colonisation in structured landscapes for Eurasian lynx. Landsc Ecol 26:501–513CrossRefGoogle Scholar
  71. Stephens PA, d’Sa CA, Sillero-Zubiri C, Leader-Williams N (2001) Impact of livestock and settlement on the large mammalian wildlife of Bale Mountains National Park southern Ethiopia. Biol Conser 100:307–322CrossRefGoogle Scholar
  72. Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP (2010) Landscape genetics: where are we now? Mol Ecol 19:3496–3514PubMedCrossRefGoogle Scholar
  73. Sutherland GD, Harestad AS, Price K, Lertzman KP (2000) Scaling of natal dispersal distances in terrestrial birds and mammals. Conserv Ecol 4:16Google Scholar
  74. Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189–3194PubMedCrossRefGoogle Scholar
  75. 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 4:535–538CrossRefGoogle Scholar
  76. Wagner HW, Sefc KM (1999) Identity 10 Software for the analysis of microsatellite data Centre for Applied Genetics. University of Agricultural Sciences, ViennaGoogle Scholar
  77. Waltermire R (1975) A national park in the Bale mountains. Walia 6:20–23Google Scholar
  78. Westemeier RL, Brawn JD, Simpson SA et al (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698PubMedCrossRefGoogle Scholar
  79. Wikramanayake E, McKnight M, Dinerstein E et al (2004) Designing a conservation landscape for tigers in human-dominated environments. Conserv Biol 18:839–844CrossRefGoogle Scholar
  80. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multi-locus genotypes. Genetics 163:1177–1191PubMedGoogle Scholar
  81. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedGoogle Scholar
  82. Wright S (1978) Evolution and the genetics of populations, Vol 4, Variability within and among natural populations. University of Chicago Press, ChicagoGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Anagaw Atickem
    • 1
  • Eli K. Rueness
    • 1
  • Leif E. Loe
    • 2
  • Dimitar Serbezov
    • 1
  • Afework Bekele
    • 3
  • Nils Chr Stenseth
    • 1
  1. 1.Department of BiologyCentre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of OsloOsloNorway
  2. 2.Department of Ecology and Natural Resource ManagementNorwegian University of Life SciencesÅsNorway
  3. 3.Department of BiologyAddis Ababa UniversityAddis AbabaEthiopia

Personalised recommendations