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Genetic rescue of an isolated African lion population

Abstract

Fragmented wildlife populations are challenged by limited gene flow that can lead to significant inbreeding. The lion (Panthera leo) population in South Africa’s Hluhluwe-iMfolozi Park (HiP) started from a small founder population of one adult male (1958), one adult female, followed by two lionesses and three cubs (two females and one male; 1965; unrelated to the male). A genetic rescue effort was launched after signs of inbreeding were observed in the 1990s. Sixteen lions (13 females and three males) were translocated into the HiP population from Pilanesberg National Park and Madikwe Game Reserve. We assessed the genetic consequences 10 to 15 years post translocation (n = 91), using microsatellite markers. Structure analysis revealed integration of the translocated animals and evidence of a unique post-translocation genetic cluster. Allelic richness increased from 2.26 to 3.88, and heterozygosity from 0.40 to 0.65. However, overall relatedness within (0.19) and among (0.15) existing prides remained higher than in an open system, and both allelic richness and heterozygosity were declining in later post-translocation generations. Thus, although genetic rescue is a valuable tool for the recovery of inbred, isolated populations, genetic augmentation should be performed at regular intervals to ensure continued population viability.

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References

  1. Adamack AT, Gruber B (2014) Hypersonic: model analysis and checking in the cloud. Methods Ecol Evol 5:384–387. https://doi.org/10.1111/2041-210x.12158

  2. Bjorklund M (2003) The risk of inbreeding due to habitat loss in the lion (Panthera leo). Conserv Genet 4:515–523

  3. Borrego N, Ozgul A, Slotow R, Packer C (2018) Lion population dynamics: do nomadic males matter? Behav Ecol 29:660–666. https://doi.org/10.1093/beheco/ary018

  4. Driscoll CA, Menotti-Raymond M, Nelson G, Goldstein D, O’Brien SJ (2002) Genomic microsatellites as evolutionary chronometers: a test in wild cats. Genome Res 12:414–423. https://doi.org/10.1101/gr.185702

  5. Dubach J, Patterson BD, Briggs MB, Venzke K, Flamand J, Stander P, Scheepers L, Kays RW (2005) Molecular genetic variation across the southern and eastern geographic ranges of the African lion, Panthera leo. Conserv Genet 6:15–24. https://doi.org/10.1007/s10592-004-7729-6

  6. Dubach JM, Briggs MB, White PA, Ament BA, Patterson BD (2013) Genetic perspectives on “Lion Conservation Units” in Eastern and Southern Africa. Conserv Genet 14:741–755. https://doi.org/10.1007/s10592-013-0453-3

  7. 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

  8. Fenster CB, Ballou JD, Dudash MR, Eldridge MDB, Frankham R, Lacy RC, Ralls K, Sunnucks P (2018) Conservation and genetics. Yale J Biol Med 91:491–501

  9. Frankham R (2009) Genetic considerations in reintroduction programmes for top-order, terrestrial predators. In: Hayward MW, Somers MJ (eds) Reintroduction of top-order predators. Wiley-Blackwell, Oxford, pp 371–387

  10. Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618. https://doi.org/10.1111/mec.13139

  11. Frankham R (2016) Genetic rescue benefits persist to at least the F3 generation, based on a meta-analysis. Biol Conserv 195:33–36. https://doi.org/10.1016/J.BIOCON.2015.12.038

  12. Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, Second edn. Cambridge University Press, Cambridge

  13. Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475

  14. Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: Revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63

  15. Frankham R, Ballou JD, Ralls K, Eldridge MDB, Dudash MR, Fenster CB, Lacy RC, Sunnucks P (2017) Genetic management of fragmented animal and plant populations, 1st edn. Oxford University Press, Oxford

  16. Fredrickson RJ, Siminski P, Woolf M, Hedrick PW (2007) Genetic rescue and inbreeding depression in Mexican wolves. Proc Biol Sci 274:2365–2371. https://doi.org/10.1098/rspb.2007.0785

  17. Funston PJ (2008) Conservation and management of lions in Southern Africa: status, threats, utilization and the restoration option. In: Croes B, Deiongh HH, Bauer H (eds) Management and conservation of large carnivores in West and Central Africa. Institute of Environmental Sciences, Leiden, pp 109–131

  18. Funston PJ, Levendal M (2015) Biodiversity management plan for African Lion (Panthera leo). Department of Environmental Affairs, Pretoria

  19. Hayward MW, Somers MI (2009) Reintroduction of top-order predators: using science to restore one of the drivers of biodiversity. In: Hayward MW, Somers MJ (eds) Reintroduction of top-order predators. Wiley-Blackwell, Oxford, pp 1–9

  20. Hayward MW, Adendorff J, Moolman LC, O’Brien J, Sholto-Douglas A, Bissett C, Bean P, Fogarty A, Howarth D, Slater R, Kerley GIH (2007) The reintroduction of large carnivores to the Eastern Cape, South Africa: an assessment. Oryx 41:205–214. https://doi.org/10.1017/S0030605307001767

  21. Hedrick PW, Fredrickson R (2010) Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv Genet 11:615–626. https://doi.org/10.1007/s10592-009-9999-5

  22. Hedrick PW, Garcia-Dorado A (2016) Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol Evol 31:940–952. https://doi.org/10.1016/J.TREE.2016.09.005

  23. Hedrick PW, Peterson RO, Vucetich LM, Adams JR, Vucetich JA (2014) Genetic rescue in Isle Royale wolves: genetic analysis and the collapse of the population. Conserv Genet 15:1111–1121. https://doi.org/10.1007/s10592-014-0604-1

  24. Hlokwe TM, De Klerk-Lorist L-M, Michel AL (2016) Wildlife on the move: a hidden tuberculosis threat to conservation areas and game farms through introduction of untested animals. J Wildl Dis 52:837–843. https://doi.org/10.7589/2015-10-281

  25. Johnson WE, Onorato DP, Roelke ME, Land ED, Cunningham M, Belden RC, McBride R, Jansen D, Lotz M, Shindle D, Howard J, Wildts DE, Penfold LM, Hostetler JA, Oli MK, O’Brien SJ (2010) Genetic restoration of the Florida panther. Science 329:1641–1645

  26. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129

  27. Keet DF, Michel A, Meltzer DGA (2000) Tuberculosis in free-ranging lions (Panthera leo) in the Kruger National Park. In: Proceedings of the South African Veterinary Association Biennial Congress, 20–22 Sept, Durban, KwaZulu-Natal, pp 232–241

  28. Kettles R, Slotow R (2009) Management of free-ranging lions on an enclosed game reserve. S Afr J Wildl Res 39:23–33. https://doi.org/10.3957/056.039.0103

  29. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, 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

  30. Kronenberger JA, Gerberich JC, Fitzpatrick SW, Broder ED, Angeloni LM, Funk WC (2018) An experimental test of alternative population augmentation scenarios. Conserv Biol 32:838–848. https://doi.org/10.1111/cobi.13076

  31. Kyriazis CC, Wayne RK, Lohmueller KE (2019) High genetic diversity can contribute to extinction in small populations. bioRxiv. https://doi.org/10.1101/678524

  32. Maddock A, Anderson A, Carlisle F, Galli N, James A, Verster A, Whitfield W (1996) Changes in lion numbers in Umfolozi-Hluhluwe Game Park. Lammergeyer 44:6–18

  33. McEvoy OK, Miller SM, Beets W, Bodasing T, Borrego N, Burger A, Courtenay B, Ferreira S, Hanekom C, Hofmeyr M, Packer C, Robertson D, Stratford K, Slotow R, Parker DM (2019) The use of contraceptive techniques in managed wild African lion (Panthera leo) populations to mimic open system cub recruitment. Wildl Res. https://doi.org/10.1071/WR18079

  34. Michel AL (2002) Implications of tuberculosis in African wildlife and livestock. Ann N Y Acad Sci 969:251–255

  35. Michel AL, Bengis RG, Keet DF, Hofmeyr M, de Klerk LM, Cross PC, Jolles AE, Cooper D, Whyte IJ, Buss P, Godfroid J (2006) Wildlife tuberculosis in South African conservation areas: Implications and challenges. Vet Microbiol 112:91–100

  36. Michel AL, Coetzee M, Keet D, Mare L, Warren R, Cooper D, Bengis R, Kremer K, van Helden P (2009) Molecular epidemiology of Mycobacterium bovis isolates from free-ranging wildlife in South African game reserves. Vet Microbiol 133:335–343. https://doi.org/10.1016/J.VETMIC.2008.07.023

  37. Miller SM, Funston PJ (2014) Rapid growth rates of lion (Panthera leo) populations in small, fenced reserves in South Africa: a management dilemma. S Afr J Wildl Res 44:43–55

  38. Miller SM, Bissett C, Burger A, Courtenay B, Dickerson T, Druce DJ, Ferreira S, Funston PJ, Hofmeyr D, Kilian PJ, Matthews W, Naylor S, Parker DM, Slotow R, Toft M, Zimmermann D (2013) Management of reintroduced lions in small, fenced reserves in South Africa: An assessment and guidelines. South African J Wildl Res 43:138–154. https://doi.org/10.3957/056.043.0202

  39. Miller SM, Harper CK, Bloomer P, Hofmeyr J, Funston PJ (2014a) Evaluation of microsatellite markers for population studies and forensic identification of African lions (Panthera leo). J Hered 105:762–772. https://doi.org/10.1093/jhered/esu054

  40. Miller SM, Harper CK, Bloomer P, Hofmeyr J, Funston PJ (2014b) Data from: Evaluation of microsatellite markers for populations studies and forensic identification of African lions (Panthera leo). J Hered 105:856–866. https://doi.org/10.5061/dryad.f61vq

  41. Miller SM, Harper CK, Bloomer P, Hofmeyr J, Funston PJ (2015) Fenced and fragmented: conservation value of managed metapopulations. PLoS ONE. https://doi.org/10.1371/journal.pone.0144605

  42. Miller SM, Riggio J, Funston PJ, Power RJ, Williams VL, Child MF (2016) A conservation assessment of Panthera leo. In: The red list of mammals of South Africa, Swaziland and Lesotho. South African National Biodiversity Institute and Endangered Wildlife Trust, South Africa

  43. Nowell K, Jackson P (1996) Status survey and conservation action plan wild cats. Gland, Switzerland

  44. Packer C, Gilbert DA, Pusey AE, O’Brien SJ (1991a) A molecular genetic analysis of kinship in lions. Nature 351:562–565

  45. Packer C, Pusey AE, Rowley H, Gilbert DA, Maternson J, O’Brien SJ (1991b) Case study of a population bottleneck: lions of the Ngorogoro Crater. Conserv Biol 5:219–230

  46. Packer C, Loveridge A, Canney S, Caro T, Garnett ST, Pfeifer M, Zander KK, Swanson A, MacNulty D, Balme G, Bauer H, Begg CM, Begg KS, Bhalla S, Bissett C, Bodasing T, Brink H, Burger A, Burton AC et al (2013) Conserving large carnivores: dollars and fence. Ecol Lett 16:635–641. https://doi.org/10.1111/ele.12091

  47. Pardo-Diaz C, Salazar C, Jiggins CD (2015) Towards the identification of the loci of adaptive evolution. Methods Ecol Evol 6:445–464. https://doi.org/10.1111/2041-210X.12324

  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

  49. Pilgrim KL, McKelvey KS, Riddle EE, Schwartz MK (2005) Felid sex identification based on noninvasive genetic samples. Mol Ecol Notes 5:60–61. https://doi.org/10.1111/j.1471-8286.2004.00831.x

  50. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67:170–181. https://doi.org/10.1086/302959

  51. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/

  52. Ralls K, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC, Sunnucks P, Frankham R (2018) Call for a paradigm shift in the genetic management of fragmented populations. Conserv Lett 11:e12412. https://doi.org/10.1111/conl.12412

  53. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237. https://doi.org/10.1046/j.1523-1739.2003.01236.x

  54. RStudio Team (2016) RStudio: integrated development for R. RStudio, Inc, Boston, MA. http://www.rstudio.com/

  55. Slotow R, Hunter LTB (2009) Reintroduction decisions taken at the incorrect social scale devalue their conservation contribution: the African lion in South Africa. In: Hayward M, Somers M (eds) Reintroduction of top-order predators. Wiley-Blackwell, Oxford, pp 41–73

  56. Somers MJ, Becker P, Druce DJ, Graf J, Gunther M, Hayward MW (2017) Reassembly of the predator guild into Hluhluwe-iMfolozi Park. In: Cromsigt JPGM, Archibald S, Owen-Smith N (eds) Conserving Africa’s mega-diversity in the Antrhopocene: the Hluhluwe-iMfolozi Park story. Cambridge University Press, Cambridge, pp 286–310

  57. Spong G, Stone J, Creel S, Björklund M (2002) Genetic structure of lions (Panthera leo L.) in the Selous Game Reserve: implications for the evolution of sociality. J Evol Biol 15:945–953. https://doi.org/10.1046/j.1420-9101.2002.00473.x

  58. Stein B (1999) Genetic variation and depletion in a population of lions (Panthera leo) in Hluhluwe-Umfolozi Park. University of Natal, Pietermaritzburg

  59. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496

  60. Tambling CJ, Ferreira SM, Adendorff J, Kerley GIH (2013) Lessons from management interventions: consequences for lion-buffalo interactions. South African J Wildl Res 43:1–11. https://doi.org/10.3957/056.043.0116

  61. Tensen L, Groom RJ, Khuzwayo J, Jansen van Vuuren B (2018) The genetic tale of a recovering lion population (Panthera leo) in the Savé Valley region (Zimbabwe): a better understanding of the history and managing the future. PLoS ONE 13:e0190369. https://doi.org/10.1371/journal.pone.0190369

  62. Tilman D, Clark M, Williams DR, Kimmel K, Polasky S, Packer C (2017) Future threats to biodiversity and pathways to their prevention. Nature 546:73–81. https://doi.org/10.1038/nature22900

  63. Trinkel M, Ferguson N, Reid A, Reid C, Somers M, Turelli L, Graf J, Szykman M, Cooper D, Haverman P, Kastberger G, Packer C, Slotow R (2008) Translocating lions into an inbred lion population in the Hluhluwe-iMfolozi Park, South Africa. Anim Conserv 11:138–143. https://doi.org/10.1111/j.1469-1795.2008.00163.x

  64. Trinkel M, Cooper D, Packer C, Slotow R (2011) Inbreeding depression increases susceptibility to bovine tuberculosis in lions: an experimental test using an inbred-outbred contrast through translocation. J Wildl Dis 47:494–500. https://doi.org/10.7589/0090-3558-47.3.494

  65. Vilà C, Sundqvist A-K, Flagstad Ø, Seddon J, Björnerfeldt S, Kojola I, Casulli A, Sand H, Wabakken P, Ellegren H (2003) Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proc Biol Sci 270:91–97. https://doi.org/10.1098/rspb.2002.2184

  66. Viljoen IM, van Helden PD, Millar RP (2015) Mycobacterium bovis infection in the lion (Panthera leo): current knowledge, conundrums and research challenges. Vet Microbiol 177:252–260. https://doi.org/10.1016/J.VETMIC.2015.03.028

  67. Wang J (2011a) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145. https://doi.org/10.1111/j.1755-0998.2010.02885.x

  68. Wang J (2011b) Unbiased relatedness estimation in structured populations. Genetics 187:887–901. https://doi.org/10.1534/genetics.110.124438

  69. Wang J (2017) Estimating pairwise relatedness in a small sample of individuals. Heredity (Edinb) 119:302–313. https://doi.org/10.1038/hdy.2017.52

  70. Wang Q, Salter L, Pearl DK (2002) Estimation of evolutionary parameters with phylogenetic trees. J Mol Evol 55:684–695. https://doi.org/10.1007/s00239-002-2364-7

  71. Weeks AR, Stoklosa J, Hoffmann AA (2016) Conservation of genetic uniqueness of populations may increase extinction likelihood of endangered species: the case of Australian mammals. Front Zool 13:31. https://doi.org/10.1186/s12983-016-0163-z

  72. Weeks AR, Heinze D, Perrin L, Stoklosa J, Hoffmann AA, van Rooyen A, Kelly T, Mansergh I (2017) Genetic rescue increases fitness and aids rapid recovery of an endangered marsupial population. Nat Commun 8:1071. https://doi.org/10.1038/s41467-017-01182-3

  73. Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49. https://doi.org/10.1016/J.TREE.2014.10.009

  74. Wildt DE, Bush M, Goodrowe KL, Packer C, Pusey AE, Brown JL, Joslin P, O’Brien SJ (1987) Reproductive and genetic consequences of founding isolated lion populations. Nature 329:328–331

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Acknowledgements

We acknowledge Gus van Dyk formerly from Northwest Parks and Tourism Board, Pete Hartley and Dave Balfour from Ezemvelo KZN Wildlife (EKZNW) and Neil Ferguson from University of KwaZulu-Natal for discussions and planning that were integral to the genetic rescue effort. A large number of EKZNW staff and numerous research assistants, students and volunteers worked long hours at night, in difficult conditions, to collect samples. We especially thank Drs Dave Cooper and Birgit Eggers, the EKZNW veterinarians for assistance in immobilizing and sampling the lions. We acknowledge funding from a THRIP grant to N. Ferguson, NRF and UKZN funding to R. Slotow, NRF and UP funding to P. Bloomer, The Green Trust (WWF-SA) grant to M. Somers, NSF, Walt Disney Foundation and MGM Grand Hotels grants to C. Packer, Wild about Cats, Hluhluwe Tourism Association, Bateleurs, Wildlife Conservation Trust and Ezemvelo KZN Wildlife. Thanks also to Jacqui Bishop, Vincent Naude, and Gabi Leighton for helpful discussions during the data analysis stage. Thanks to three anonymous reviewers for helpful comments on an earlier version that improved this manuscript.

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Correspondence to Susan M. Miller.

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This project was approved by Ezemvelo KZN Wildlife (Project number: E/5107/04). Ethical clearance for animal sampling was obtained by R Slotow from the University of Kwazulu-Natal Animal Ethics Committee. Post-translocation samples were all collected as part of a larger monitoring project on Hluhluwe-iMfolozi Park by Ezemvelo KZN Wildlife.

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Miller, S.M., Druce, D.J., Dalton, D.L. et al. Genetic rescue of an isolated African lion population. Conserv Genet 21, 41–53 (2020). https://doi.org/10.1007/s10592-019-01231-y

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Keywords

  • Fragmented population
  • Genetic rescue
  • Inbreeding
  • Panthera leo