Advertisement

Conservation Genetics

, Volume 19, Issue 4, pp 981–993 | Cite as

Assessing introgressive hybridization between blue wildebeest (Connochaetes taurinus) and black wildebeest (Connochaetes gnou) from South Africa

  • Paul Grobler
  • Anna M. van Wyk
  • Desiré L. DaltonEmail author
  • Bettine Jansen van Vuuren
  • Antoinette Kotzé
Research Article

Abstract

Introgressive hybridization poses a threat to the genetic integrity of black wildebeest (Connochaetes gnou) and blue wildebeest (Connochaetes taurinus) populations in South Africa. Black wildebeest is endemic to South Africa and was driven to near extinction in the early 1900s due to habitat destruction, hunting pressure and disease outbreaks. Blue wildebeest on the other hand are widely distributed in southern and east Africa. In South Africa the natural distribution ranges of both species overlap, however, extensive translocation of black wildebeest outside of its normal distribution range in South Africa have led to potential hybridization between the two species. The molecular identification of pure and admixed populations is necessary to design viable and sustainable conservation strategies, since phenotypic evidence of hybridization is inconclusive after successive generations of backcrossing. The aim of this study was to assess levels of hybridization in wildebeest using both species-specific and cross-species microsatellite markers. Black wildebeest (157) and blue wildebeest (122) from provincial and national parks and private localities were included as reference material, with 180 putative hybrid animals also screened. A molecular marker panel consisting of 13 cross-species and 11 species-specific microsatellite markers was developed. We used a Bayesian clustering model to confirm the uniqueness of blue- and black wildebeest reference groups, assign individuals to each of the two clusters, and determine levels of admixture. Results indicated a clear partition between black wildebeest and blue wildebeest (the average proportions of membership to black wildebeest and blue wildebeest clusters were QI = 0.994 and QI = 0.955 respectively). From the putative hybrid samples, only five hybrid individuals were confirmed. However, high levels of linkage disequilibrium were observed in the putative hybrid populations which may indicate historical hybridization. Measures of genetic diversity in the black wildebeest populations were found to be lower than that of the blue wildebeest. The observed lower level of genetic diversity was expected due to the demographic history of the specie. This study will make a significant contribution to inform a national conservation strategy to conserve the genetic integrity of both species.

Keywords

Black wildebeest Blue wildebeest Hybridization STRUCTURE HYBRIDLAB Microsatellites 

Notes

Acknowledgements

The authors wish to express their sincere gratitude to the South African National Biodiversity Institute (SANBI) and International Foundation of Science (IFS), Grant Number B6411, for funding the analysis of pure and hybrid wildebeest populations. We also thank Ezemvelo KZN Wildlife, the Free State Department of Economic, Small Business Development, Tourism and Environmental Affairs (DESTEA) and South African National Parks (SANParks) for providing samples, and for prioritizing the wildebeest hybridization issue. The DST NRF Professional Development Programme through the NZG is thanked for supporting human capital.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Black wildebeest samples were sanctioned under TOPS permit 036006 (University of the Free State) and a standing permit 03309 (National Zoological Gardens of South Africa). Samples from the Free State Provinces were collected under permit no. 01/30307 issued by DESTEA. Ethical clearance from the respective Institutional Research Ethics Committees was also obtained; UFS-AED2015/0067 (University of the Free State) and P7/12 (National Zoological Gardens of South Africa).

References

  1. Ackermann RR, Brink JS, Vrahimis S, De Klerk B (2010) Hybrid wildebeest (Artiodactyla: Bovidae) provide further evidence for shared signatures of admixture in mammalian crania. S Afr J Sci.  https://doi.org/10.4102/sajs.v106i11/12.423 CrossRefGoogle Scholar
  2. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: Setting conservation guidelines. Trends Ecol Evol 16:613–622.  https://doi.org/10.1016/S0169-5347(01)02290-X CrossRefGoogle Scholar
  3. Allendorf FW, Luikart G, Aitken SN (2013) Conservation and the genetics of populations, 2nd edn. Wiley, HobokenGoogle Scholar
  4. Attwell CA. (1977) Reproduction and population ecology of the blue wildebeest (Connochaetes taurinus taurinus) in Zululand. University of Natal, NatalGoogle Scholar
  5. Barilani M, Bernard-Laurent A, Mucci N et al (2007) Hybridisation with introduced chukars (Alectoris chukar) threatens the gene pool integrity of native rock (A. graeca) and red-legged (A. rufa) partridge populations. Biol Conserv 137:57–69.  https://doi.org/10.1016/j.biocon.2007.01.014 CrossRefGoogle Scholar
  6. Benjamin-fink N, Reilly BK (2017) Conservation implications of wildlife translocations; the state’ s ability to act as conservation units for wildebeest populations in South Africa. Glob Ecol Conserv 12:46–58.  https://doi.org/10.1016/j.gecco.2017.08.008 CrossRefGoogle Scholar
  7. Birss C, Rushworth I, Collins N et al (2017) Inferred natural distribution ranges of certain large mammals in South Africa. Unpublished GIS coverageGoogle Scholar
  8. Boecklen WJ, Howard DJ (1997) Genetic Analysis of hybrid zones: numbers of markers and power of resolution. Ecology 78:2611.  https://doi.org/10.2307/2265918 CrossRefGoogle Scholar
  9. Brink JS (1993) Postcranial evidence for the evolution of the Black Wildebeest, Connochaetes gnou: an exploratory study. Palaeont Afr 30:61–69Google Scholar
  10. Brink J (2005) The evolution of the black wildebeest (Connochaetes gnou) and modern large mammal faunas of central southern Africa. University of Stellenbosch, StellenboschGoogle Scholar
  11. Buckland RA, Evans HJ (1978) Cytogenetic aspects of phylogeny in the Bovidae. I. G-banding. Cytogenet Cell Genet 21:42–63CrossRefPubMedGoogle Scholar
  12. Buerkle CA, Wolf DE, Rieseberg LH (2003) The origin and extinction of species through hybridization. Springer, Berlin, pp 117–141Google Scholar
  13. Corbet SW, Robinson TJ (1991) Genetic divergence in South African Wildebeest: comparative cytogenetics and analysis of mitochondrial DNA. J Hered 82:447–452CrossRefPubMedGoogle Scholar
  14. Corbet SW, Grant WS, Robinson TJ (1994) Genetic divergence in South African wildebeest: analysis of allozyme variability. J Hered 85:479–483CrossRefPubMedGoogle Scholar
  15. Cullingham CI, Cooke JEK, Dang S et al (2011) Mountain pine beetle host-range expansion threatens the boreal forest. Mol Ecol 20:2157–2171.  https://doi.org/10.1111/j.1365-294X.2011.05086.x CrossRefPubMedPubMedCentralGoogle Scholar
  16. Currens KP, Hemmingsen AR, French RA et al (1997) Introgression and susceptibility to disease in a wild population of rainbow trout. N Am J Fish Manag 17:1065–1078CrossRefGoogle Scholar
  17. De Klerk B (2007) An osteological documentation of hybrid wildebeest and its bearing on black wildebeest (Connochaetes gnou) evolution. University of the Witwatersrand, JohannesburgGoogle Scholar
  18. Du Plessis S (1969) The past and present geographical distribution of the Perissodactyla and Artiodactyla in southern Africa. University of Pretoria, PretoriaGoogle Scholar
  19. Earl DA, vonHoldt BM (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 CrossRefGoogle Scholar
  20. East R (1999) African antelope database 1998Google Scholar
  21. Estes RD (2013) Connochaetes taurinus common wildebeest. In: Kingdon J, Hoffmann M (eds) The mammals of Africa. Bloomsbury Publishing, London, pp 533–543Google Scholar
  22. Estes RD, East R (2009) Status of the wildebeest (Connochaetes taurinus) in the wild 1967–2005. WCS Working Paper 37. Wildlife Conservation Society, New YorkGoogle Scholar
  23. 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.  https://doi.org/10.1111/j.1365-294X.2005.02553.x CrossRefPubMedGoogle Scholar
  24. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567.  https://doi.org/10.1111/j.1755-0998.2010.02847.x CrossRefPubMedGoogle Scholar
  25. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50.  https://doi.org/10.1111/j.1755-0998.2010.02847.x CrossRefGoogle Scholar
  26. Fabricius C, Lowry D, Van den Berg P (1988) Fecund black wildebeest × blue wildebeest hybrids. South Afr J Wildl Res 18:35–37Google Scholar
  27. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578.  https://doi.org/10.1111/j.1471-8286.2007.01758.x CrossRefPubMedPubMedCentralGoogle Scholar
  28. Goldberg TL, Grant EC, Inendino KR et al (2005) Increased infectious disease susceptibility resulting from outbreeding depression. Conserv Biol 19:455–462.  https://doi.org/10.1111/j.1523-1739.2005.00091.x CrossRefGoogle Scholar
  29. Goodman SJ, Barton NH, Swanson G et al (1999) Introgression through rare hybridization: a genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll. Scotl Genet 152:355–371Google Scholar
  30. Grobler JP, Van der Bank FH (1995) Allozyme divergence among four representatives of the subfamily Alcelaphinae (family: Bovidae). Comp Biochem Physiol 112:303–308CrossRefGoogle Scholar
  31. Grobler JP, Hartl GB, Grobler N et al (2005) The genetic status of an isolated black wildebeest (Connochaetes gnou) population from the Abe Bailey Nature Reserve, South Africa: Microsatellite data on a putative past hybridization with blue wildebeest (C-taurinus). Mamm Biol 70:35–45.  https://doi.org/10.1078/1616-5047-00174 CrossRefGoogle Scholar
  32. Grobler JP, Rushworth I, Brink JS et al (2011) Management of hybridization in an endemic species: decision making in the face of imperfect information in the case of the black wildebeest-Connochaetes gnou. Eur J Wildl Res 57:997–1006.  https://doi.org/10.1007/s10344-011-0567-1 CrossRefGoogle Scholar
  33. Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361.  https://doi.org/10.2307/2532296 CrossRefPubMedGoogle Scholar
  34. Hedrick PW (2009) Conservation genetics and North American bison (Bison bison). J Hered 100:411–420.  https://doi.org/10.1093/jhered/esp024 CrossRefPubMedGoogle Scholar
  35. Hirst SM (1975) Ungulate-habitat relationships in a South African woodland/savanna ecosystem. Wildl Monogr 44:3–60.  https://doi.org/10.2307/3830376 CrossRefGoogle Scholar
  36. Hoban SM, McCleary TS, Schlarbaum SE et al (2012) Human-impacted landscapes facilitate hybridization between a native and an introduced tree. Evol Appl 5:720–731.  https://doi.org/10.1111/j.1752-4571.2012.00250.x CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332.  https://doi.org/10.1111/j.1755-0998.2009.02591.x CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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 23:1801–1806.  https://doi.org/10.1093/bioinformatics/btm233 CrossRefPubMedGoogle Scholar
  39. Karsten M, van Vuuren BJ, Goodman P, Barnaud A (2011) The history and management of black rhino in KwaZulu-Natal: a population genetic approach to assess the past and guide the future. Anim Conserv 14:363–370.  https://doi.org/10.1111/j.1469-1795.2011.00443.x CrossRefGoogle Scholar
  40. Kirkman AH (1938) Conservation notes. Connochaetes gnou. J Soc Preserv Wild Fauna Emp 35:50Google Scholar
  41. Lepais O, Petit RJ, Guichoux E et al (2009) Species relative abundance and direction of introgression in oaks. Mol Ecol 18:2228–2242.  https://doi.org/10.1111/j.1365-294X.2009.04137.x CrossRefPubMedGoogle Scholar
  42. Levin DA, Francisco-Ortega J, Jansen RK (1996) Hybridization and the extinction of rare plant species. Conserv Biol 10:10–16.  https://doi.org/10.1046/j.1523-1739.1996.10010010.x CrossRefGoogle Scholar
  43. Lingle S (1992) Escape gaits of white-tailed deer, mule deer and their hybrids: gaits observed and patterns of limb coordination. Behaviour 122:153–181.  https://doi.org/10.1163/156853992X00499 CrossRefGoogle Scholar
  44. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, SunderlandGoogle Scholar
  45. Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237.  https://doi.org/10.1016/j.tree.2005.02.010 CrossRefPubMedGoogle Scholar
  46. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  47. Nielsen EE, Bach LA, Kotlicki P (2006) HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Mol Ecol Notes 6:971–973.  https://doi.org/10.1111/j.1471-8286.2006.01433.x CrossRefGoogle Scholar
  48. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295.  https://doi.org/10.1111/j.1471-8286.2005.01155.x CrossRefGoogle Scholar
  49. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539.  https://doi.org/10.1093/bioinformatics/bts460 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  51. Randi E, Hulva P, Fabbri E et al (2014) Multilocus detection of wolf x dog hybridization in Italy, and guidelines for marker selection. PLoS ONE.  https://doi.org/10.1371/journal.pone.0086409 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Rawson PD, Burton RS (2002) Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod. Proc Natl Acad Sci USA 99:12955–12958.  https://doi.org/10.1073/pnas.202335899 CrossRefPubMedGoogle Scholar
  53. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109.  https://doi.org/10.1146/annurev.ecolsys.27.1.83 CrossRefGoogle Scholar
  54. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefPubMedGoogle Scholar
  55. Røed KH, Ernest EM, Midthjell L, Msoffe PLM (2011) Identification and characterization of 17 microsatellite loci in the blue wildebeest, Connochaetes taurinus. Conserv Genet Resour 3:181–183.  https://doi.org/10.1007/s12686-010-9319-x CrossRefGoogle Scholar
  56. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138.  https://doi.org/10.1046/j.1471-8286.2003.00566.x CrossRefGoogle Scholar
  57. Russo I-RM, Hoban S, Bloomer P et al (2018) “Intentional Genetic Manipulation” as a conservation threat. Conserv Genet Resour.  https://doi.org/10.1007/s12686-018-0983-6 CrossRefGoogle Scholar
  58. Sage RD, Heyneman D, Lim K-C, Wilson AC (1986) Wormy mice in a hybrid zone. Nature 324:60–63.  https://doi.org/10.1038/324060a0 CrossRefPubMedGoogle Scholar
  59. Sanz N, Araguas RM, Fernández R et al (2008) Efficiency of markers and methods for detecting hybrids and introgression in stocked populations. Conserv Genet 10:225–236.  https://doi.org/10.1007/s10592-008-9550-0 CrossRefGoogle Scholar
  60. Seehausen O, Schluter D, Coyne JA et al (2006) Conservation: losing biodiversity by reverse speciation. Curr Biol 16:R334–R337.  https://doi.org/10.1016/j.cub.2006.03.080 CrossRefPubMedGoogle Scholar
  61. Skinner JD, Chimimba CT (2005) The mammals of the Southern African subregion, 3rd edn. Cambridge University Press, Cape TownCrossRefGoogle Scholar
  62. Smith GR, Stewart JD, Carpenter NE (2013) Fossil and recent Mountain Suckers, Pantosteus, and significance of introgression in catostomin fishes of western United StatesGoogle Scholar
  63. Valbuena-Carabaña M, González-Martínez SC, Hardy OJ, Gil L (2007) Fine-scale spatial genetic structure in mixed oak stands with different levels of hybridization. Mol Ecol 16:1207–1219.  https://doi.org/10.1111/j.1365-294X.2007.03231.x CrossRefPubMedGoogle Scholar
  64. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538.  https://doi.org/10.1111/j.1471-8286.2004.00684.x CrossRefGoogle Scholar
  65. Van Wyk AM, Kotzé A, Randi E, Dalton DL (2013) A hybrid dilemma: a molecular investigation of South African bontebok (Damaliscus pygargus pygargus) and blesbok (Damaliscus pygargus phillipsi). Conserv Genet 14:589–599.  https://doi.org/10.1007/s10592-013-0448-0 CrossRefGoogle Scholar
  66. van Wyk AM, Dalton DL, Hoban S et al (2017) Quantitative evaluation of hybridization and the impact on biodiversity conservation. Ecol Evol 7:320–330.  https://doi.org/10.1002/ece3.2595 CrossRefPubMedGoogle Scholar
  67. Von Richter W (1971) Observations on the biology and ecology of the black wildebeest (Connochaetus gnou). South Afr J Wildl Res Wildl 1:3–16Google Scholar
  68. Von Richter W (1974) Connochaetes gnou. Mamm Species 50:1–6Google Scholar
  69. Vrahimis S (2013) Connochaetes gnou black wildebeest. In: Kingdon J, Happold D, Butynski T et al (eds) The mammals of Africa. Volume VI: Pigs, hippopotamuses, chevrotain, giraffes, deer and bovids. Bloomsbury Publishing, London, pp 528–532Google Scholar
  70. Vrahimis S, Grobler P, Brink J et al (2016) A conservation assessment of Connochaetes gnou. In: Child M, Roxburgh L, Do Linh San E et al (eds) The Red List of Mammals of South Africa, Swaziland and Lesotho. South African National Biodiversity Institute and Endangered Wildlife Trust, South Africa, pp 1–8Google Scholar
  71. Vuillaume B, Valette V, Lepais O et al (2015) Genetic evidence of hybridization between the endangered native species Iguana delicatissima and the invasive Iguana iguana (Reptilia, Iguanidae) in the Lesser Antilles: management implications. PLoS ONE 10:e0127575.  https://doi.org/10.1371/journal.pone.0127575 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Whitlock M, Phillips P, Moore FB, Tonsor S (1995) Multiple fitness peaks and epistasis. Annu Rev Ecol Syst 26:601–629CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Paul Grobler
    • 1
  • Anna M. van Wyk
    • 1
    • 2
  • Desiré L. Dalton
    • 1
    • 2
    Email author
  • Bettine Jansen van Vuuren
    • 3
  • Antoinette Kotzé
    • 1
    • 2
  1. 1.Department of GeneticsUniversity of the Free StateBloemfonteinSouth Africa
  2. 2.National Zoological GardenSouth African National Biodiversity InstitutePretoriaSouth Africa
  3. 3.Centre for Ecological Genomics and Wildlife Conservation, Department of ZoologyUniversity of JohannesburgAuckland ParkSouth Africa

Personalised recommendations