Advertisement

Genetic variation among different springbok (Antidorcas marsupialis) colour variants

Abstract

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.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

References

  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, https://doi.org/10.1111/age.12207.

  2. Akira, S., 2009. Pathogen recognition by innate immunity and its signaling. Proc. Japan Acad. Ser. B Phys. Biol. Sci. 85, 143–156, https://doi.org/10.2183/pjab/85.143.

  3. Akira, S., Takeda, K., Kaisho, T., 2001. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2,675, https://doi.org/10.1038/90609.

  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.

  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, https://doi.org/10.1210/en.2008-1087.

  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.

  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, https://doi.org/10.1016/j.ympev.2009.03.008.

  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, https://doi.org/10.1046/j.1365-294X.2003.02063.x.

  9. Barsh, G.S., 1996. The genetics of pigmentation: from fancy genes to complex traits. Trends Genet. 12, 299–305, https://doi.org/10.1016/0168-9525(96)10031-7.

  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.

  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.

  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, https://doi.org/10.4098/AT.arch.93-45.

  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, https://doi.org/10.1080/00359190809519220.

  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, https://doi.org/10.1074/jbc.M505590200.

  15. Cloete, F., 2018. The Rise, Fall and Future of Colour Variants. Farmer’s Weekly, URL https://www.farmersweekly.co.za/animals/game-and-wildlife/rise-fall-future-colour-variants/ (Accessed 8.19.19).

  16. Coulon, A., 2010. GENHET: an easy-to-use R function to estimate individual heterozygosity. Mol. Ecol. Resour. 10, 167–169.

  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.

  18. Cronwright-Schreiner, S.C., 1925. The Migratory Springbucks of South Africa: the Trekbokke. T. Fisher Unwin, London.

  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, https://doi.org/10.4238/2015.March.13.16.

  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, https://doi.org/10.1073/pnas.0904691106.

  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.

  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.

  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, https://doi.org/10.1007/s12686-011-9548-7.

  24. East, R., 1999. African Antelope Database 1998. IUCN/SSC Antelope Specialist Group.

  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.

  26. Foll M., 2012. BayeScan v2.1 user manual. Ecolog. 20, 1450–1462.

  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.

  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, https://doi.org/10.1016/j.smallrumres.2012.02.008.

  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, https://doi.org/10.1186/1471-2148-13-194.

  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.

  31. Frost W., 2014. The Antelope of Africa. Jacana Media (Pty) Ltd., Sunnyside, Auckland Park, South Africa.

  32. Furstenburg, D., 2016. Springbok Antidorcas marsupialis management. In: Oberem, P., Oberem, P. (Eds.), The New Game Rancher. BRIZA Publisher, Pretoria, pp. 226–234.

  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, https://doi.org/10.1093/jhered/esn080.

  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, https://doi.org/10.1098/rspb.2006.3762.

  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), https://doi.org/10.4098/AT.arch.99-16.

  36. Guex, N., Peitsch, M.C., 1997. SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling. Electrophoresi. 18, 2714–2723.

  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.

  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, https://doi.org/10.1016/S2095-3119(14)60928-X.

  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, https://doi.org/10.4238/2015.February.6.22.

  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, https://doi.org/10.1111/mec.12975.

  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, https://doi.org/10.1371/journal.pone.0036536.

  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, https://doi.org/10.1016/j.cbpa.2008.11.011.

  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.

  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, https://doi.org/10.1074/jbc.M806688200.

  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, https://doi.org/10.1016/j.cell.2016.10.004,750-762.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.

  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, https://doi.org/10.1007/BF00713067.

  48. IBM Corp, 2017. IBM SPSS Statistics for Windows, Version 25.0.

  49. IUCN SSC Antelope Specialist Group, 2016. Antidorcas marsupialis (errata version published in 2017)., https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T1676A50181753.en.

  50. Janssens, S., Beyaert, R., 2003. Role of toll-like receptors in pathogen recognition. Clin. Microbiol. Rev. 16, 637–646, https://doi.org/10.1128/CMR.16.4.637.

  51. Jones, S.V., 1923. Color variations in wild animals. J. Mammal. 1, 172–177.

  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, https://doi.org/10.1093/bioinformatics/bts199.

  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.

  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, https://doi.org/10.1111/1755-0998.12387.

  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.

  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.

  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.

  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.

  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.

  60. Leigh, J., Bryant, D., 2015. Popart: full-feature software forhaplotype network construction. Methods Ecol. Evol. 6, 1110–1116, https://doi.org/10.1111/2041-210X.12410.

  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.

  62. Librado P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452, https://doi.org/10.1093/bioinformatics/btp187.

  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, https://doi.org/10.1073/pnas.0400937101.

  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, https://doi.org/10.3389/fgene.2014.00333.

  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.

  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, https://doi.org/10.1038/ni.1733.

  67. McRobie, H., Thomas, A., Kelly, J., 2009. The genetic basis of melanism in the gray squirrel (Sciurus carolinensis). J. Hered. 100, 709–714.

  68. Medzhitov R., 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135–145, https://doi.org/10.1038/35100529.

  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, https://doi.org/10.1111/1755-0998.12017.

  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, https://doi.org/10.1111/age.12430.

  71. Nel, L., 2016. 2nd National Stakeholder Engagement Workshop on the Intensive and Selctive Breeding, SA Hunters. URL http://www.sahunters.co.za/index.php/ conservation-bewaring/item/230-2nd-national-stakeholderengagement-workshop-on-the-intensive-and-selective-breeding (Accessed 7.6.16).

  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, https://doi.org/10.1590/S1984-46702011000100008.

  73. Oberem, P., URL https://www.africageographic.com/blog/wildlife-ranching-in-south-africa/ (accessed 10.16.17) 2015. Wildlife Rancing in South Africa. African Geogr.

  74. Oberem, Pamela, Oberem, Pieter, 2016. The New Game Rancher. Briza Publications.

  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, https://doi.org/10.1007/s12686-011-9577-2.

  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.

  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.

  78. RCore, URL 2015. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing http://www.r-project.org.

  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, https://doi.org/10.1073/pnas.0502272102.

  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.

  81. Roulin, A., 2004. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol. Rev. 79, 815–848.

  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.

  83. Ryder M.L., Land, R.B., Ditchburn, R., 1974. Coat colour inheritance in Soay, Orkney and Shetland sheep. J. Zool. 173, 477–485.

  84. Ryel, L., 1963. The occurence of certain anomalies in Michigan white-tailed deer. J. Mammal. 1, 79–98.

  85. Sakluda-Gorgul, A., Seta, K., Nowakowska, M., Bednarek, A.K., 2011. WWOX oxidoreductase-substrate and enzymatic characterization. Zeitschrift für Naturforsch.. 66, 73–82.

  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.

  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.

  88. Skinner, J.D., 1993. Springbok (Antidorcas marsupialis) treks. Trans. R. Soc. South Afric. 48, 291–305, https://doi.org/10.1080/00359199309520276.

  89. Skinner, J.D., Louw, G.N., 1996. The Springbok Antidorcas marsupialis (Zimmermann, 1780). Trasvaal Museum, Pretoria, South Africa.

  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.

  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, https://doi.org/10.1086/428594.

  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, https://doi.org/10.1086/319501.

  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.

  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, https://doi.org/10.13140/RG.2.1.1211.1128.

  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.

  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, https://doi.org/10.1111/j.1558-5646.2011.01473.x.

  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, https://doi.org/10.1016/j.mambio.2011.11.006.

  98. van der Westhuizen, J., 2014. A Systematic Approach to Breeding Programs for Game. South African Stud Book and Animal Imporvement Association.

  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.

  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.

  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, https://doi.org/10.1016/S1671-2927(08)60256-4.

  102. Wesson, J., Walkerville, Gauteng, South Africa 2015. NACSSA Position Paper on the Breeding of Colour Variants in the Wildlife Industry.

  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, https://doi.org/10.1111/j.1365-2052.2005.01383.x.

  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.

  105. Wildlife South Africa, URL www.wrsa.co.za (Accessed 8.19.19) 2019. Wildlife Ranching South Africa.

  106. Wlasiuk, G., Nachman, M.W., 2010. Adaptation and constraint at toll-like receptors in primates. Mol. Biol. Evol. 27, 2172–2186, https://doi.org/10.1093/molbev/msq104.

  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, https://doi.org/10.1508/cytologia.32.273.

  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.

  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, https://doi.org/10.1155/2013/675382.

  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, https://doi.org/10.1016/j.immuni.2016.09.011.

Download references

Author information

Correspondence to Willem G. Coetzer.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Coetzer, W.G., Grobler, J.P. Genetic variation among different springbok (Antidorcas marsupialis) colour variants. Mamm Biol 99, 42–53 (2019). https://doi.org/10.1016/j.mambio.2019.10.006

Download citation

Keywords

  • Springbok
  • Colour variant
  • Colour gene
  • MC1R
  • TLR