Mammalian Biology

, Volume 99, Issue 1, pp 42–53 | Cite as

Genetic variation among different springbok (Antidorcas marsupialis) colour variants

  • Willem G. CoetzerEmail author
  • J. Paul Grobler
Original investigation


The linebreeding of southern African antelope species, involving selection for specific coat colour pheno-types, is a wide-spread practice in the South African game farming industry. Concerns have been voiced with regards to the genetic status of these line-bred colour variants, due to the high risk of inbreeding. The springbok (Antidorcas marsupialis) is one of the most well-known examples of such linebreeding. Numerous colour variants have been observed, with the most notable the black, copper and white colour phenotypes. To our knowledge, no research has been performed on the genetic basis of these springbok colour variants. In this study, we aimed to 1) assess the level of genetic variation within and among the common, black, copper and white colour variants of springbok, and 2) investigate the possible genetic mechanisms involved in the coat colour of these variants. Portions of the mtDNA control region ( CR) and two immune-linked Toll-like receptor (TLR4 and TLR7) genes were sequenced for the genetic diversity estimates. A 50 K Bovine SNP chip was also screened to assess the level of genetic diversity of a subset of samples. The complete melanocortin 1 receptor (MC1R) gene was targeted for the second aim. Comparable levels of diversity were identified across specimens. Pairwise genetic diversity analysis of the SNP data identified the white springbok as a unique group within springbok, with Bayesian clustering analysis supporting this observation. A possible reason for this clustering pattern was linked to the historical occurrence of white springbok in nature. The level of genetic diversity observed for each colour variant was associated with 1) the large historical and extant population sizes of springbok providing a deep genetic pool and/or 2) the management practices of the managers/farmers that are aimed at preventing or minimizing inbreeding and loss of genetic diversity. The MC1R assessment identified a nonsynony-mous SNP (c. G902A) unique to white springbok (homozygous AA). A 24 bp deletion was observed in black, copper and king springbok colour variants. This deletion was complete for ~21 % of black springbok. The heterozygous variant was observed in ~88 % of copper springbok and ~5 % of black springbok. This would suggest that additional genetic factors are involved in coat colour determination (due to the incomplete association of the 24 bp deletion). Further research is therefore needed to identify the other possible genetic factors involved.


Springbok Colour variant Colour gene MC1R TLR 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abitbol, M., Legrand, R., Tiret, L., 2014. A missense mutation in melanocortin 1 receptor is associated with the red coat colour in donkeys. Anim. Genet. 45, 878–880, Scholar
  2. Akira, S., 2009. Pathogen recognition by innate immunity and its signaling. Proc. Japan Acad. Ser. B Phys. Biol. Sci. 85, 143–156, Scholar
  3. Akira, S., Takeda, K., Kaisho, T., 2001. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2,675, Scholar
  4. Anderson, C., Schultze, E., Codron, D., Bissett, C., Gaylard, A., Child, M.F., 2016. A conservation assessment of Antidorcas marsupialis. In: Child, M.F., Roxburgh, L., Do Ling San, E., Raimondo, D., Davies-Mostert, H.T. (Eds.), The Red List of Mammals of South Africa, Swaziland and Lesotho. South African National Biodiversity Institute and Endangered Wildlife Trust, South Africa, South Africa.Google Scholar
  5. Aqeilan, R.I., Hagan, J.P., de Bruin, A., Rawahneh, M., Salah, Z., Gaudio, E., Siddiqui, H., Volinia, S., Alder, H., Lian, J.B., Stein, G.S., Croce, C.M., 2009. Targeted ablation of the WW domain-containing oxidoreductase tumor suppressor leads to impaired steroidogenesis. Endocrinology 150, 1530–1535, Scholar
  6. Aqeilan, R.I., Palamarchuk, A., Weigel, R.J., Herrero, J.J., Pekarsky, Y., Croce, C.M., 2004. Physical and functional interactions between the Wwox tumor suppressor protein and the AP-2γ transcription factor. Cancer Res. 64, 8256 LP- 8261.PubMedCrossRefPubMedCentralGoogle Scholar
  7. Ayoub, N.A., McGowen, M.R., Clark, C., Springer, M.S., Gatesy, J., 2009. Evolution and phylogenetic utility of the melanocortin-1 receptor gene (MC1R) in Cetartiodactyla. Mol. Phylogenet. Evol. 52,550–557, Scholar
  8. Ballard, J.W.O., Whitlock, M.C., City, I., Ballard, J.W.O., Whitlock, M.C., 2004. The incomplete natural history of mitochondria. Mol. Ecol. 13, 729–744, Scholar
  9. Barsh, G.S., 1996. The genetics of pigmentation: from fancy genes to complex traits. Trends Genet. 12, 299–305, Scholar
  10. Bednarek, A.K., Keck-Waggoner, C.L., Daniel, R.L., Laflin, K.J., Bergsagel, P.L., Kiguchi, K., Brenner, A.J., Aldaz, C.M., 2001. WWOX, the FRA16D gene, behaves as a suppressor of tumor growth. CancerRes. 61, 8068 LP- 8073.Google Scholar
  11. Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T.G., Bertoni, M., Bordoli, L., Schwede, T., 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42, W252–W258.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bigalke R.C., Hartl, G.B., Berry, M.P.S., Van Hensbergen, H.J., 1993. Population genetics of the springbok Antidorcas marsupialis - a preliminary study. Acta Theriol. (Warsz)38, 103–111, Scholar
  13. Carruthers, J., Frssaf, J.C., 2008. Wilding the farm or farming the wild? The evolution of scientific game ranching in South Africa from the 1960s to the present. Trans. R. Soc. South Africa 63,160–181, Scholar
  14. Chang, N.S., Doherty, J., Ensign, A., Schultz, L., Hsu, L.J., Hong, Q., 2005. WOX1 is essential for tumor necrosis factor-, UV light-, staurosporine-, and p53-mediated cell death, and its tyrosine 33-phosphorylated form binds and stabilizes serine 46-phosphorylated p53. J. Biol. Chem. 280, 43100–43108, Scholar
  15. Cloete, F., 2018. The Rise, Fall and Future of Colour Variants. Farmer’s Weekly, URL (Accessed 8.19.19).Google Scholar
  16. Coulon, A., 2010. GENHET: an easy-to-use R function to estimate individual heterozygosity. Mol. Ecol. Resour. 10, 167–169.PubMedCrossRefPubMedCentralGoogle Scholar
  17. Cousins, J.A., Sadler, J.P., Evans, J., 2008. Exploring the role of private wildlife ranching as a conservation tool in South Africa. Ecol. Soc, 13.Google Scholar
  18. Cronwright-Schreiner, S.C., 1925. The Migratory Springbucks of South Africa: the Trekbokke. T. Fisher Unwin, London.Google Scholar
  19. Dai, Q.X., Yao, Y.F., Qi, Z.C., Huang, Y., Ni, Q.Y., Zhang, M.W., Xu, H.L., 2015. Sequence characterization and phylogenetic analysis of toll-like receptor (TLR) 4 gene in the Tibetan macaque (Macaca thibetana). Genet. Mol. Res. 14, 1875–1886, Scholar
  20. Decker, J.E., Pires, J.C., Conant, G.C., McKay, S.D., Heaton, M.P., Chen, K., Cooper, A., Vilkki, J., Seabury, C.M., Caetano, A.R., Johnson, G.S., Brenneman, R.A., Hanotte, O., Eggert, L.S., Wiener, P., Kim,J.-J., Kim, K.S., Sonstegard, T.S., VanTassell, C.P., Neibergs, H.L., McEwan, J.C., Brauning, R., Coutinho, L.L., Babar, M.E., Wilson, G.A., McClure, M.C., Rolf, M.M., Kim, J., Schnabel, R.D., Taylor, J.F., 2009. Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics. Proc. Natl. Acad. Sci. 106, 18644–18649, Scholar
  21. Diebold, S.S., Kaisho, T., Hemmi, H., Akira, S., Reise Sousa, C.R., 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science (80-.) 303,1529–1531.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Doney, J.M., Ryder, M.L., Gunn, R.G., Grubb, P., 1974. Coulour, conformation, affinities, fleece and patterns of inheritance of the soay sheep. In: Jewell, P.A., Milner, C., Boyd, J.M. (Eds.), Island Survivors: The Ecology of the Soay Sheep of St Kilda. Athlone Press, London, UK, pp. 88–125.Google Scholar
  23. Earl D.A., vonHoldt, B.M., 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361, Scholar
  24. East, R., 1999. African Antelope Database 1998. IUCN/SSC Antelope Specialist Group.Google Scholar
  25. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Foll M., 2012. BayeScan v2.1 user manual. Ecolog. 20, 1450–1462.Google Scholar
  27. Foll M., Gaggiotti, O., 2008. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetic. 180, 977–993.CrossRefGoogle Scholar
  28. Fontanesi L., Rustempasić, A., Brka, M., Russo, V., 2012. Analysis of polymorphisms in the agouti signalling protein (ASIP) and melanocortin 1 receptor (MC1R) genes and association with coat colours in two Pramenka sheep types. Small Rumin. Res. 105, 89–96, Scholar
  29. Fornůsková, A., Vinkler, M., Pagès, M., Galan, M., Jousselin, E., Cerqueira, F., Morand, S., Charbonnel, N., Bryja, J., Cosson, J.F., 2013. Contrasted evolutionary histories of two Toll-like receptors (Tlr4 and Tlr7) in wild rodents (Murinae). BMC Evol. Biol. 13, 194, Scholar
  30. Fredriksson, R., Lagerström, M.C., Lundin, L.G., Schiöth, H.B., 2003. The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol. 63, 1256–1272.PubMedPubMedCentralGoogle Scholar
  31. Frost W., 2014. The Antelope of Africa. Jacana Media (Pty) Ltd., Sunnyside, Auckland Park, South Africa.Google Scholar
  32. Furstenburg, D., 2016. Springbok Antidorcas marsupialis management. In: Oberem, P., Oberem, P. (Eds.), The New Game Rancher. BRIZA Publisher, Pretoria, pp. 226–234.Google Scholar
  33. Ginja C., Telo da Gama, L., Penedo, M.C.T., 2009. Y Chromosome haplotype analysis in Portuguese cattle breeds using SNPs and STRs. J. Hered. 100, 148–157, Scholar
  34. Gratten, J., Beraldi, D., Lowder, B., McRae, A., Visscher, P., Pemberton, J., Slate, J., 2007. Compelling evidence that a single nucleotide substitution in TYRP1 is responsible for coat-colour polymorphism in a free-living population of Soay sheep. Proc. R. Soc. B Biol. Sci. 274, 619–626, Scholar
  35. Grobler, P.J., Taylor, P.J., Pretorius, M.D., Anderson, C.P., 1999. Fluctuating asymmetry and allozyme variability in an isolated springbok Antidorcas marsupialis population from the Chelmsford Nature Reserve. Acta Theriol. (Warsz), Scholar
  36. Guex, N., Peitsch, M.C., 1997. SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling. Electrophoresi. 18, 2714–2723.CrossRefGoogle Scholar
  37. Hamman, K., Vrahimis, S., Blom, H., 2003. Can current trends in the game industry be reconciled with nature conservation? African Indaba Yearb. 1, 3–16.Google Scholar
  38. Han, J.L., Yang, M., Guo, T.T., Yue, Y.J., Liu, J.B., Niu, C.E., Wang, C.F., Yang, B.H., 2015a. Molecular characterization of two candidate genes associated with coat color in Tibetan sheep (Ovis arise). J. Integr. Agric. 14, 1390–1397, Scholar
  39. Han, J.L., Yang, M., Yue, Y.J., Guo, T.T., Liu, J.B., Niu, C.E., Yang, B.H., 2015b. Analysis of agouti signaling protein (ASIP)gene polymorphisms and association with coat color in Tibetan sheep (Ovis arties). Genet. Mol. Res. 14, 1200–1209, Scholar
  40. Hartmann, S.A., Schaefer, H.M., Segelbacher, G., 2014. Genetic depletion at adaptive but not neutral loci in an endangered bird species. Mol. Ecol. 23, 5712–5725, Scholar
  41. Haynes, G.D., Latch, E.K., 2012. Identification of novel single nucleotide polymorphisms (SNPs) in deer (Odocoileus spp.) using the BovineSNP50 BeadChip. PLoS One 7, e36536, Scholar
  42. Hetem, R.S., de Witt, B.A., Fick, L.G., Fuller, A., Kerley, G.I.H., Meyer, L.R., Mitchell, D., Maloney, S.K., 2009. Body temperature, thermoregulatory behaviour and pelt characteristics of three colour morphs of springbok (Antidorcas marsupialis). Comp. Biochem. Physiol. - A Mol. Integr. Physiol. 152, 379–388, Scholar
  43. Hoffman, J.I., Thorne, M.S., McEwing, R., Forcada, J., Ogden, R., 2013. Cross-amplification and validation of SNPs conserved over 44 million years between seals and dogs. PLoS One 8, e68365.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hsu, L.J., Schultz, L., Hong, Q., Van Moer, K., Heath, J., Li, M.Y., Lai, F.J., Lin, S.R., Lee, M.H., Lo, C.P., Lin, Y.S., Chen, S.T., Chang, N.S., 2009. Transforming growth factor beta1 signaling via interaction with cell surface Hyal-2 and recruitment ofWWOX/WOX1. J. Biol. Chem. 284, 16049–16059, Scholar
  45. Hua, T., Vemuri, K., Pu, M., Qu, L., Han, G.W., Wu, Y., Zhao, S., Shui, W., Li, S., Korde, A., Laprairie, R.B., Stahl, E.L., Ho, J.H., Zvonok, N., Zhou, H., Kufareva, I., Wu, B., Zhao, Q., Hanson, M., Bohn, L.M., Makriyannis, A., Stevens, R.C., Liu, Z.J., 2016. Crystal structure of the human cannabinoid receptor CB1. Cell 167,,750-762.e14.
  46. Hughes, K.L., Bildfell, R.J., Alcantar, B., 2017. Pigmented tumors in fallow deer (Dama dama): 11 cases. J. Vet. Diagn. Invest. 29, 483–488.PubMedCrossRefPubMedCentralGoogle Scholar
  47. Iannuzzi, L., Di Meo, G.P., 1995. Chromosomal evolution in bovids: a comparison of cattle, sheep and goat G- and R-banded chromosomes and cytogenetic divergences among cattle, goat and river buffalo sex chromosomes. Chromosome Res. 3, 291–299, Scholar
  48. IBM Corp, 2017. IBM SPSS Statistics for Windows, Version 25.0.Google Scholar
  49. IUCN SSC Antelope Specialist Group, 2016. Antidorcas marsupialis (errata version published in 2017)., Scholar
  50. Janssens, S., Beyaert, R., 2003. Role of toll-like receptors in pathogen recognition. Clin. Microbiol. Rev. 16, 637–646, Scholar
  51. Jones, S.V., 1923. Color variations in wild animals. J. Mammal. 1, 172–177.CrossRefGoogle Scholar
  52. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649, Scholar
  53. Kijas, J.M.H., Wales, R., Törnsten, A., Chardon, P., Moller, M., Andersson, L., 1998. Melanocortin receptor 1 (MC1R) mutations and coat color in pigs. Genetics 150, 1177–1185.PubMedPubMedCentralGoogle Scholar
  54. Kopelman, N.M., Mayzel, J., Jakobsson, M., Rosenberg, N., Mayrose, I., 2015. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol. Ecol. Resour. 15, 1179–1191, Scholar
  55. Kruger, J.H., 1976. An Investigation of Certain Dermatological, Morphological and Genetic Aspects of the Black Springbok and the White Springbok (Antidorcas marsupialis). University of Pretoria.Google Scholar
  56. Kruger, J.H., Skinner, J.D., Robinson, T.J., 1979. On the taxonomic status of the black and white springbok, Antidorcas marsupialis. S. Afr. J. Sci. 75, 411–412.Google Scholar
  57. Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874.CrossRefGoogle Scholar
  58. Kurt-Jones, E.A., Popova, L., Kwinn, L., Haynes, L.M., Jones, L.P., Tripp, R.A., Walsh, E.E., Freeman, M.W., Golenbock, D.T., Anderson, L.J., 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1, 398–402.PubMedCrossRefPubMedCentralGoogle Scholar
  59. le, J.C., 2015. The springbok migrations of yesteryear: the most spectacucar and grandiose historical mammal events in the world. In: Wildlife Ranching South Africa Conference, Sun City, South Africa.Google Scholar
  60. Leigh, J., Bryant, D., 2015. Popart: full-feature software forhaplotype network construction. Methods Ecol. Evol. 6, 1110–1116, Scholar
  61. Li, B., He, X., Zhao, Y., Zhao, Q., Bai, D., Manglai, D., 2014. Tyrosinase-related protein 1 (TYRP1) gene polymorphism and skin differential expression related to coat color in Mongolian horse. Livest. Sci. 167, 58–64.CrossRefGoogle Scholar
  62. Librado P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452, Scholar
  63. Lund, J.M., Alexopoulou, L., Sato, A., Karow, M., Adams, N.C., Gale, N.W., Iwasaki, a, Flavell, R., 2004. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. U. S. A. 101, 5598–5603, Scholar
  64. Makina, S.O., Muchadeyi, F.C., van Marle-Köster, E., MacNeil, M.D., Maiwashe, A., 2014. Genetic diversity and population structure among six cattle breeds in South Africa using a whole genome SNP panel. Front. Genet. 5, 333, Scholar
  65. Manceau, M., Domingues, V.S., Linnen, C.R., Rosenblum, E.B., Hoekstra, H.E., 2010. Convergence in pigmentation at multiple levels: mutations, genes and function. Philos. Trans. R. Soc. B Biol. Sci. 365, 2439–2450.CrossRefGoogle Scholar
  66. Mancuso G., Gambuzza, M., Midiri, A., Biondo, C., Papasergi, S., Akira, S., Teti, G., Beninati, C., 2009. Bacterial recognition by TLR7 in the lysosomes of conventional dendritic cells. Nat. Immunol. 10, 587–594, Scholar
  67. McRobie, H., Thomas, A., Kelly, J., 2009. The genetic basis of melanism in the gray squirrel (Sciurus carolinensis). J. Hered. 100, 709–714.PubMedCrossRefPubMedCentralGoogle Scholar
  68. Medzhitov R., 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135–145, Scholar
  69. Miller, J.M., Kijas, J.W., Heaton, M.P., McEwan, J.C., Coltman, D.W., 2012. Consistent divergence times and allele sharing measured from cross-species application of SNP chips developed forthree domestic species. Mol. Ecol. Resour. 12, 1145–1150, Scholar
  70. Miller, S.M., Guthrie, A.J., Harper, C.K., 2016. Single base-pair deletion in ASIP exon 3 associated with recessive black phenotype in impala (Aepyceros melampus). Anim. Genet. 47,511–512, Scholar
  71. Nel, L., 2016. 2nd National Stakeholder Engagement Workshop on the Intensive and Selctive Breeding, SA Hunters. URL conservation-bewaring/item/230-2nd-national-stakeholderengagement-workshop-on-the-intensive-and-selective-breeding (Accessed 7.6.16).Google Scholar
  72. Nogueira, D.M., Alves, M.S., 2011. A case of leucism in the burrowing owl Athene cunicularia (Aves: Strigiformes) with confirmation of species identity using cytogenetic analysis. Zoología 28,53–57, Scholar
  73. Oberem, P., URL (accessed 10.16.17) 2015. Wildlife Rancing in South Africa. African Geogr.Google Scholar
  74. Oberem, Pamela, Oberem, Pieter, 2016. The New Game Rancher. Briza Publications.Google Scholar
  75. Ogden, R., Baird, J., Senn, H., McEwing, R., 2012. The use of cross-species genome-wide arrays to discover SNP markers for conservation genetics: a case study from Arabian and scimitar-horned oryx. Conserv. Genet. Resour. 4, 471–473, Scholar
  76. Ohto, U., Yamakawa, N., Akashi-Takamura, S., Miyake, K., Shimizu, T., 2012. Structural analyses of human Toll-like receptor 4 polymorphisms D299G and T399I.J. Biol. Chem. 287, 40611–40617.CrossRefGoogle Scholar
  77. Purcell S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.R., Bender, D., Maller, J., Sklar, P., De Bakker, P.I.W., Daly, M.J., 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575.PubMedPubMedCentralCrossRefGoogle Scholar
  78. RCore, URL 2015. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing Scholar
  79. Roach, J.C., Glusman, G., Rowen, L., Kaur, A., Purcell, M.K., Smith, K.D., Hood, L.E., Aderem, A., 2005. The evolution of vertebrate Toll-like receptors. Proc. Natl. Acad. Sci. U. S. A. 102, 9577–9582, Scholar
  80. Roche, C., 2005. The Springbok... Drink the rain’s blood: indigenous knowledge and its use in environmental history—The case of the /Xam and an understanding of springbok treks. S. Afr. J. Econ. Hist. 53, 1–22.CrossRefGoogle Scholar
  81. Roulin, A., 2004. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol. Rev. 79, 815–848.PubMedCrossRefPubMedCentralGoogle Scholar
  82. Rozen S., Skaletsky, H., 1999. Primer3 on the WWW for general users and for biologist programmers. In: Misener, S., Krawetz, S.A. (Eds.), Bioinformatics Methods and Protocols. Humana Press, Totowa, USA., pp. 365–386.CrossRefGoogle Scholar
  83. Ryder M.L., Land, R.B., Ditchburn, R., 1974. Coat colour inheritance in Soay, Orkney and Shetland sheep. J. Zool. 173, 477–485.CrossRefGoogle Scholar
  84. Ryel, L., 1963. The occurence of certain anomalies in Michigan white-tailed deer. J. Mammal. 1, 79–98.CrossRefGoogle Scholar
  85. Sakluda-Gorgul, A., Seta, K., Nowakowska, M., Bednarek, A.K., 2011. WWOX oxidoreductase-substrate and enzymatic characterization. Zeitschrift für Naturforsch.. 66, 73–82.Google Scholar
  86. Skead C.J., 2011. Introduced (non-indigenous) species: a growing threat to biodiversity. In: Boshoff, A.F., Kerley, G.I.H., Lloyd, P.H. (Eds.), Historical Incidence of the Larger Land Mammals in the Broader Western and Northern Cape. Nelson Mandela Metropolitan University, Port Elizabeth, pp. 468–487.Google Scholar
  87. Skead C.J., 2007. Historical incidence of the larger land mammals in the broader Eastern Cape. In: Boshoff, A.F., Kerley, G.I.H., Lloyd, P.H. (Eds.), Centre for African Conservation Ecology. Nelson Mandela Metropolitan University, Port Elizabeth.Google Scholar
  88. Skinner, J.D., 1993. Springbok (Antidorcas marsupialis) treks. Trans. R. Soc. South Afric. 48, 291–305, Scholar
  89. Skinner, J.D., Louw, G.N., 1996. The Springbok Antidorcas marsupialis (Zimmermann, 1780). Trasvaal Museum, Pretoria, South Africa.Google Scholar
  90. Smith, N., Wilson, S.L., 2002. Changing land use trends in the thicket biome: pastoralism to game farming. Terr. Ecol. Res. Unit Rep. 38, 23.Google Scholar
  91. Stephens, M., Scheet, P., 2005. Accounting for decay of linkage disequilibrium in haplotype Inference and missing-data imputation. Am. J. Hum. Genet. 76, 449–462, Scholar
  92. Stephens, M., Smith, N.J., Donnelly, P., 2001. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68, 978–989, Scholar
  93. Sumreddee, P., Toghiani, S., Hay, E.H., Roberts, A., Agrrey, S.E., Rekaya, R., 2018. Inbreeding depression in line 1 Hereford cattle population using pedigree and genomic information. J. Anim. Sci.Google Scholar
  94. Taylor, W.A., Lindsey, P.A., Davies-Mostert, H., 2015. An Assessment of the Economic, Social and Conservation Value of the Wildlife Ranching Industry and Its Potential to Support the Green Economy in South Africa. The Endangered Wildlife Trust, Johannesburg, Scholar
  95. Thompson, J.D., Higgins, D.G., Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680.PubMedPubMedCentralCrossRefGoogle Scholar
  96. Tschirren B., Andersson, M., Scherman, K., Westerdahl, H., Råberg, L., 2012. Contrasting patterns of diversity and population differentiation at the innate immunity gene Toll-like Receptor 2 (TLR2) in two sympatric rodent species. Evolutio. 66, 720–731, Scholar
  97. Van Aswegen, E., Labuschagne, C., Grobler, J.P., 2012. Phenotypic differences, spatial distribution and diversity at the Cytb and BMP4 genes in springbok (Antidorcas marsupialis). Mamm. Biol. 77, 391–396, Scholar
  98. van der Westhuizen, J., 2014. A Systematic Approach to Breeding Programs for Game. South African Stud Book and Animal Imporvement Association.Google Scholar
  99. Vinkler, M., Albrecht, T., 2009. The question waiting to be asked: innate immunity receptors in the perspective of zoological research. Folia Zool. 58, 15–28.Google Scholar
  100. Visser, J., Jansen Van Vuuren, B., 2017. The Influence of Commercial Game Farming on Maintaining Genetic Diversity in the Sable Antelope and Roan Antelope. Southern African Wildlife Management Association, Rawsonville, South Africa.Google Scholar
  101. Wang, X., Luoreng, Z., Xu, S., Gao, X., Li, J., Ren, H., Chen, J., 2009. The structure and sequence analysis ofTLR4gene in cattle. Agric. Sci. China 8, 632–637, Scholar
  102. Wesson, J., Walkerville, Gauteng, South Africa 2015. NACSSA Position Paper on the Breeding of Colour Variants in the Wildlife Industry.Google Scholar
  103. White, S.N., Halbert, N.D., Taylor, K.H., Derr, J.N., Womack, J.E., 2005. TLR4 variation in Yellowstone bison. Anim. Genet. 36, 533–534, Scholar
  104. Whitlock, M.C., Lotterhos, K.E., 2015. Reliable detection of loci responsible for local adaptation: inference of a null model through trimming the distribution of F ST. Am. Nat. 186, S24–S36.PubMedCrossRefPubMedCentralGoogle Scholar
  105. Wildlife South Africa, URL (Accessed 8.19.19) 2019. Wildlife Ranching South Africa.Google Scholar
  106. Wlasiuk, G., Nachman, M.W., 2010. Adaptation and constraint at toll-like receptors in primates. Mol. Biol. Evol. 27, 2172–2186, Scholar
  107. Wurster, D.H., Benirschke, K., 1967. Chromosome studies in some deer, the springbok, and the pronghorn, with notes on placentation in deer. Cytologi. 32, 273–285, Scholar
  108. Xu, Y., Zhang, X.H., Pang, Y.Z., 2013. Association of tyrosinase (TYR) and tyrosinase-related protein 1 (TYRP1 ) with melanic plumage color in Korean Quails (Coturnix coturnix). Asian-Aust. J. Anim. Sci. 26, 1518.CrossRefGoogle Scholar
  109. Yang, G.L., Fu, D.L., Lang, X., Wang, Y.T., Cheng, S.R., Fang, S.L., Luo, Y.Z., 2013. Mutations in MC1R gene determine black coat color phenotype in Chinese sheep. Sci. World J. 2013, Scholar
  110. Zhang, Z., Ohto, U., Shibata, T., Krayukhina, E., Taoka, M., Yamauchi, Y., Tanji, H., Isobe, T., Uchiyama, S., Miyake, K., Shimizu, T., 2016. Structural analysis reveals that Toll-like Receptor 7 is a dual receptor forguanosine and single-stranded RNA. Immunit. 45, 737–748, Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2019

Authors and Affiliations

  1. 1.Department of GeneticsUniversity of the Free StateBloemfonteinSouth Africa

Personalised recommendations