Advertisement

Mammalian Biology

, Volume 77, Issue 1, pp 60–66 | Cite as

Genetic analysis of southern African gemsbok (Oryx gazella) reveals high variability, distinct lineages and strong divergence from the East African Oryx beisa

  • Bennie Osmers
  • Britt-Sabina Petersen
  • Günther B. Hartl
  • J. Paul Grobler
  • Antoinette Kotze
  • Elzet Van Aswegen
  • Frank E. ZachosEmail author
Original Investigation

Abstract

We carried out a population genetic analysis of five southern African gemsbok (Oryx gazella) populations based on 530 bp of the mitochondrial control region and ten microsatellites in 75 individuals. Both markers show the high variability often observed in African bovids. Three of the populations which can be traced back to very small founding or current sizes do not show any signs of reduced variability compared to the remaining populations. The mitochondrial haplotypes form three distinct lineages which most likely originated in the Pleistocene when climate fluctuations led to periodical reduction and spreading of gemsbok habitat and which, today, are found throughout the distribution range. Bayesian microsatellite analyses yielded two groups, suggesting a more recent geographical differentiation following the admixture of the mtDNA lineages. Combining our sequences with available published data of the remaining oryx species allowed for a direct molecular comparison of O. gazella and O. beisa which have sometimes been considered a single species. The average genetic divergence between haplotypes from the two taxa was very high (39.9%), supporting their classification into two different species.

Keywords

Oryx gazella Bovidae Microsatellites Mitochondrial DNA Southern Africa 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alpers, D.L., van Vuuren, B.J., Arctander, P., Robinson, T.J., 2004. Population genetics of the roan antelope (Hippotragus equinus) with suggestions for conservation. Mol. Ecol. 13, 1771–1784.PubMedCrossRefPubMedCentralGoogle Scholar
  2. Amersham Biosciences, 2002. MegaBACE Genetic Profiler Version 2.0, www.amershambiosciences.com.Google Scholar
  3. Arctander, P., Kat, P.W., Aman, R.A., Siegismund, H.R., 1996. Extreme genetic differences among populations of Gazella granti, grant’s gazelle, in Kenya. Heredity 76, 465–475.CrossRefGoogle Scholar
  4. Arnason, U., Gullberg, A., Widegren, B., 1993. Cetacean mitochondrial DNA control region: sequences of all baleen whales and two sperm whale species. Mol. Biol. Evol. 10, 960–970.PubMedPubMedCentralGoogle Scholar
  5. Bandelt, H.-J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48.PubMedCrossRefPubMedCentralGoogle Scholar
  6. Birungi, J., Arctander, P., 2000. Large sequence divergence of mitochondrial DNA genotypes of the control region within populations of the African antelope, kob (Kobus kob). Mol. Ecol. 9, 1997–2008.PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bishop, M.D., Kappes, S.M., Keele, J.W., Stone, R.T., Sunden, S.L.F., Hawkins, G.A., Solinas Toldo, S., Fries, R., Grosz, M.D., Yoo, J., Beattie, C.W., 1994. A genetic linkage map for cattle. Genetics 136, 619–639.PubMedPubMedCentralGoogle Scholar
  8. Bothma, J. du P., Van Rooyen, N., Du Toit, J.G., 2002. Antelope and other smaller herbivores. In: Bothma, J., du, P. (Eds.), Game Ranch Management. , 4th ed. Van Schaik, Pretoria, pp. 149–150.Google Scholar
  9. Buchanan, F.C., Crawford, A.M., 1993. Ovine Microsatellites at the OarFCB11, Oar-FCB128, OarFCB193, OarFCB266, OarFCB304 loci. Anim. Genet. 24, 145.CrossRefGoogle Scholar
  10. Cerling, T.E., Harris, J.M., MacFadden, B.J., Leakey, M.G., Quade, J., Eisenmann, V., Ehleringer, J.R., 1997. Global vegetation change through the Miocene/Pliocene boundary. Nature 389, 153–158.CrossRefGoogle Scholar
  11. DeMenocal, P.B., 1995. Plio-Pleistocene African climate. Science 270, 53–59.CrossRefGoogle Scholar
  12. Eckert, I., Suchentrunk, F., Markov, G., Hartl, G.B., 2010. Genetic diversity and integrity of German wildcat (Felis silvestris) populations as revealed by microsatellites, allozymes, and mitochondrial DNA sequences. Mamm. Biol. 75, 160–174.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin, version 3.11. An integrated software package for population genetics data analysis. Evol. Bioinform. Online 1, 47–50.Google Scholar
  15. Felsenstein, J., 2005. PHYLIP (Phylogeny Inference Package) Version 3.6. Distributed by the Author. Department of Genome Sciences, University of Washington, Seattle.Google Scholar
  16. Forster, P., Torroni, A., Renfrew, C., Röhl, A., 2001. Phylogenetic star contraction applied to Asian and Papuan mtDNA evolution. Mol. Biol. Evol. 18, 1864–1881.PubMedCrossRefPubMedCentralGoogle Scholar
  17. Goudet, J., 1995. FSTAT, version 2.9.3.2. A computer program to calculate F-statistics. J. Hered. 86, 485–486.CrossRefGoogle Scholar
  18. Grobler, J.P., Pretorius, D.M., Botha, K., Kotze, A., Hallerman, E.M., Jansen van Vuuren, B., 2005. An exploratory analysis of geographic genetic variation in Southern African nyala (Tragelaphus angasii). Mamm. Biol. 70, 291–299.CrossRefGoogle Scholar
  19. Grubb, P., 2005. Order Artiodactyla. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World. A Taxonomic and Geographic Reference., 3rd ed. The Johns Hopkins University Press, Baltimore, pp. 637–722.Google Scholar
  20. Hajji, G.M., Zachos, F.E., Charfi-Cheikrouha, F., Hartl, G.B., 2007. Conservation genetics of the imperilled Barbary red deer in Tunisia. Anim. Conserv. 10, 229–235.CrossRefGoogle Scholar
  21. Hall, T.A., 1999. BioEdit version 7.0.4.1: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98.Google Scholar
  22. Haring, E., Sheremetyeva, I.N., Kryukov, A.P., 2011. Phylogeny of Palearctiv vole species (genus Microtus, Rodentia) based on mitochondrial sequences. Mamm. Biol. 76, 258–267.CrossRefGoogle Scholar
  23. Henry, H.M., Penty, J.M., Pierson, C.A., Crawford, A.M., 1993. Ovine microsatellites at the OarHH35, OarHH41, OarHH44, OarHH47 and OarHH64 loci. Anim. Genet. 24, 222.PubMedCrossRefPubMedCentralGoogle Scholar
  24. Hewitt, G., 2000. The genetic legacy of the quaternary ice ages. Nature 405, 907–913.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Hewitt, G., 2004. Genetic consequences of climatic oscillations in the quaternary. Philos. T. Roy. Soc. B 359, 183–195.CrossRefGoogle Scholar
  26. HIV sequence database, 2008. Find Model, A Tool to Find the Best Fitting Evolutionary Model for your Sequences, www.hiv.lanl.gov.Google Scholar
  27. Honnen, A.-C., Petersen, B., Kaßler, L., Elmeros, M., Roos, A., Sommer, R.S., Zachos, F.E., 2011. Genetic structure of Eurasian otter (Lutra lutra, Carnivora: Mustelidae) populations from the western Baltic sea region and its implications for the recolonization of north-western Germany. J. Zool. Syst. Evol. Res. 49, 169–175.CrossRefGoogle Scholar
  28. Huebinger, R.M., de Maar, T.W.J., Woodruff, L.H., Pomp, D., Louis Jr., E.E., 2006. Characterization of eight microsatellite loci in Grant’s gazelle (Gazella granti). Mol. Ecol. 6, 1150–1151.CrossRefGoogle Scholar
  29. Iyengar, A., Gilbert, T., Woodfine, T., Knowles, J.M., Diniz, F.M., Brenneman, R.A., Louis Jr., E.E., MacLean, N., 2007. Remnantsofancient genetic diversity preserved within captive groups of scimitar-horned oryx (Oryx dammah). Mol. Ecol. 16, 2436–2449.PubMedCrossRefPubMedCentralGoogle Scholar
  30. Knight, M., 1999. Oryx gazella (Südafrikanische Oryxantilope). In: Mills, G., Hes, L. (Eds.), Säugetiere des südlichen Afrikas, eine illustrierte Enzyklopädie. Struik Publishers, Pty Ltd., Kapstadt, p. 278f.Google Scholar
  31. Lancaster, I.N., 1979. Evidence for a widespread late Pleistocene humid period in the Kalahari. Nature 279, 145–146.CrossRefGoogle Scholar
  32. Lanszki, J., Hidas, A., Szentes, K., Révay, T., Lehoczky, I., Jeney, Z., Weiss, S., 2010. Genetic structure of otter (Lutra lutra) populations from two fishpond systems in Hungary. Mamm. Biol. 75, 447–450.CrossRefGoogle Scholar
  33. Loftus, R.T., Ertugrul, O., Harba, A.H., EL-Barody, M.A.A., MacHugh, D.E., Park, S.D.E., Bradley, D.G., 1999. A microsatellite survey of cattle from a centre of origin: the Near East. Mol. Ecol. 8, 2015–2022.PubMedCrossRefPubMedCentralGoogle Scholar
  34. Lorenzen, E.D., Arctander, P., Siegismund, H.R., 2008. Three reciprocally monophyletic mtDNA lineages elucidate the taxonomic status of Grant’s gazelles. Conserv. Genet. 9, 593–601.CrossRefGoogle Scholar
  35. Lorenzen, E.D., Masembe, C., Arctander, P., Siegismund, H.R., 2010. A long-standing Pleistocene refugium in southern Africa and a mosaic of refugia in East Africa: insights from mtDNA and the common eland antelope. J. Biogeogr. 37, 571–581.CrossRefGoogle Scholar
  36. Lorenzen, E.D., de Neergard, R., Arctander, P., Siegismund, H.R., 2007. Phylogeography, hybridization and Pleistocene refugia of the kob antelope (Kobus kob). Mol. Ecol. 16, 3241–3252.PubMedCrossRefGoogle Scholar
  37. Lorenzen, E.D., Siegismund, H.R., 2004. No suggestion of hybridization between the vulnerable black-faced impala (Aepyceros melampus petersi) and the common impala (A. m. melampus) in Etosha National Park, Namibia. Mol. Ecol. 13, 3007–3019.PubMedCrossRefGoogle Scholar
  38. MacHugh, D.E., Shriver, M.D., Loftus, R.T., Cunningham, P., Bradley, D.G., 1997. Microsatellite DNA variation and the evolution, domestication and phylogeography of taurine and zebu cattle (Bos taurus and Bos indicus). Genetics 146, 1071–1086.PubMedPubMedCentralGoogle Scholar
  39. Masembe, C., Muwanika, V.B., Nyakaana, S., Arctander, P., 2006. Three genetically divergent lineages of the Oryx in eastern Africa: evidence for an ancient introgressive hybridization. Conserv. Genet. 7, 551–562.CrossRefGoogle Scholar
  40. Nersting, L.G., Arctander, P., 2001. Phylogeography and conservation of impala and greater kudu. Mol. Ecol. 10, 711–719.PubMedCrossRefPubMedCentralGoogle Scholar
  41. Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure from multilocus genotype data. Genetics 155, 945–959.PubMedPubMedCentralGoogle Scholar
  42. Raymond, M., Rousset, F., 1995. GENEPOP, version 3.4. Population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249.Google Scholar
  43. Rozas, J., Sánchez-Delbarrio, J.C., Messeguer, X., Rozas, R., 2003. DnaSP version 4.00, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Scandura, M., Iacolina, L., Apollonio, M., 2011. Genetic diversity in the European wild boar Sus scrofa: phylogeography, population structure and wild × domestic hybridization. Mammal Rev. 41, 125–137.CrossRefGoogle Scholar
  45. Simonsen, B.T., Siegismund, H.R., Arctander, P., 1998. Population structure of African buffalo inferred from mtDNA sequences and microsatellite loci: high variation but low differentiation. Mol. Ecol. 7, 225–237.PubMedCrossRefPubMedCentralGoogle Scholar
  46. Spear, D., Chown, S.L., 2009. The extent and impacts of ungulate translocations: South Africa in a global context. Biol. Conserv. 142, 353–363.CrossRefGoogle Scholar
  47. Steffen, P., Eggen, A., Dietz, A.B., Womack, J.E., Stranzinger, G., Fries, R., 1993. Isolation and mapping of polymorphic microsatellites in cattle. Anim. Genet. 24, 121.PubMedCrossRefPubMedCentralGoogle Scholar
  48. Stokes, S., Thomas, D.S.G., Washington, R., 1997. Multiple episodes of aridity in southern Africa since the last interglacial period. Nature 388, 154–158.CrossRefGoogle Scholar
  49. Stone, R.T., Pulido, J.C., Duyk, G.M., Kappes, S.M., Keele, J.W., Beattie, C.W., 1995. A small-insert bovine genomic library highly enriched for microsatellite repeat sequences. Mamm. Genome 6, 714–724.PubMedCrossRefPubMedCentralGoogle Scholar
  50. Swarbrick, P.A., Dietz, A.B., Womack, J.E., Crawford, A.M., 1992a. Ovine and bovine dinucleotide repeat polymorphism at the MAF46 locus. Anim. Genet. 23, 182.PubMedCrossRefPubMedCentralGoogle Scholar
  51. Swarbrick, P.A., Howes, J., Crawford, A., 1992b. Ovine dinucleotide repeat polymorphism at the MAF50 locus. Anim. Genet. 23, 187.PubMedCrossRefPubMedCentralGoogle Scholar
  52. Swenson, J.E., Taberlet, P., Bellemain, E., 2011. Genetics and conservation of European brown bears Ursus arctos. Mammal Rev. 41, 87–98.CrossRefGoogle Scholar
  53. Tamura, K., Nei, M., 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526.PubMedPubMedCentralGoogle Scholar
  54. Taylor, C.R., 1969. The eland and the oryx. Sci. Am. 20, 89–95.Google Scholar
  55. Van Hooft, W.F., Groen, A.F., Prins, H.H.T., 2002. Phylogeography of the African buffalo based on mitochondrial and Y-chromosomal loci: Pleistocene origin and population expansion of the Cape buffalo subspecies. Mol. Ecol. 11, 267–279.PubMedCrossRefPubMedCentralGoogle Scholar
  56. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. MICRO-CHECKER, version 2.2.3. Software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538.Google Scholar
  57. Vila, C., Amorim, I.R., Leonard, J.A., Posada, D., Castroviejo, J., Petrucci-Fonseca, F., Crandall, K.A., Ellegren, H., Wayne, R.K., 1999. Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus. Mol. Ecol. 8, 2089– 2103.PubMedCrossRefPubMedCentralGoogle Scholar
  58. Vrba, E.S., 1995. The fossil records of African antelopes (Mammalia, Bovidae) in relation to human evolution and palaeoclimate. In: Vrba, E.S., Denton, G.H., Partridge, T.C., Burckle, L.H. (Eds.), Palaeoclimate and Evolution, with Emphasis on Human Origins. NewHaven Conn., pp. 385–424.Google Scholar
  59. Zachos, F.E., 2009. Gene trees and species trees – mutual influences and interdependences of population genetics and systematics. J. Zool. Syst. Evol. Res. 47, 209–218.CrossRefGoogle Scholar
  60. Zachos, F.E., Hartl, G.B., 2011. Phylogeography, population genetics and conservation of the European red deer Cervus elaphus. Mammal Rev. 41, 138–150.CrossRefGoogle Scholar
  61. Zachos, F.E., Hartl, G.B., Apollonio, M., Reutershan, T., 2003. On the phylo-geographic origin of the Corsican red deer (Cervus elaphus corsicanus): evidence from microsatellite and mitochondrial DNA. Mamm. Biol. 68, 284– 298.CrossRefGoogle Scholar
  62. Zachos, F.E., Karami, M., Ibenouazi, Z., Hartl, G.B., Eckert, I., Kirschning, J., 2010. First genetic analysis of a free-living population of the threatened goitered gazelle (Gazella subgutturosa). Mamm. Biol. 75, 277–282.CrossRefGoogle Scholar
  63. Zachos, F.E., Otto, M., Unici, R., Lorenzini, R., Hartl, G.B., 2008. Evidence of a phylo-genetic break in the Romanian brown bear (Ursus arctos) population from the Carpathians. Mamm. Biol. 73, 93–101.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2011

Authors and Affiliations

  • Bennie Osmers
    • 1
  • Britt-Sabina Petersen
    • 2
  • Günther B. Hartl
    • 3
  • J. Paul Grobler
    • 4
  • Antoinette Kotze
    • 4
    • 5
  • Elzet Van Aswegen
    • 5
  • Frank E. Zachos
    • 3
    • 6
    Email author
  1. 1.Department of BiodiversityUniversity of LimpopoSovengaSouth Africa
  2. 2.Institute for Clinical Molecular Biology, Christian-Albrechts-Universität zu KielKielGermany
  3. 3.Zoological Institute, Christian-Albrechts-Universität zu KielKielGermany
  4. 4.Department of GeneticsUniversity of the Free StateBloemfonteinSouth Africa
  5. 5.National Zoological GardensPretoriaSouth Africa
  6. 6.Mammal Collection, Natural History Museum ViennaViennaAustria

Personalised recommendations