Skip to main content

Genetic perspectives on “Lion Conservation Units” in Eastern and Southern Africa

Conservation Genetics volume 14, pages 741–755 (2013)Cite this article

Abstract

Current understanding of genetic variation in lions (Panthera leo) is inadequate to guide many management decisions necessary for conservation of the species. We studied sequence variation in the mitochondrial cytochrome-b (cyt-b) gene of 75 lions and nuclear variation at 11 microsatellite loci of 480 lions across 8 range states (Cameroon, Uganda, Kenya, Zambia, Zimbabwe, South Africa, Botswana, and Namibia) and 13 Lion Conservation Units (LCUs) plus two other unassigned sites (Cameroon and Zimbabwe). A total of 11 cyt-b haplotypes were found, whose variation follows an isolation-by-distance model. In combination with previously known sequences, the haplotypes document the close relationship, derived position, and limited variability of Asian and West and Central African lions relative to other extant lions. Both phylogenetic analyses and substitution networks identify two clades in Eastern and Southern Africa—one restricted to Namibia and South Africa and the other more widespread across the region. However, these analyses are equivocal on which of these is closest to the ancestor of modern lions. Microsatellite analyses showed high levels of variation within and among populations, subdivision among most LCUs, and evidence of isolation by distance. While rates of gene flow are generally low, admixture among lions in northern Botswana, Caprivi Strip (Namibia) and Zambia is apparent from STRUCTURE analyses. Conservation management plans should incorporate information on genetic variability and gene flow in delimiting management units and in guiding translocations of lions to minimize inbreeding and to control problem animals.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Anderson J (1981) The re-establishment and management of a lion Panthera leo population in Zululand, South Africa. Biol Conserv 19:107–117

    Google Scholar 

  • Antunes A, Troyer JL, Roelke ME, Pecon-Slattery J, Packer C, Winterbach C, Winterbach H, Hemson G, Frank L, Stander P, Siefert L, Driciru M, Funston PJ, Alexander KA, Prager KC, Mills G, Wildt D, Bush M, O’Brien SJ, Johnson WE (2008) The evolutionary dynamics of the lion Panthera leo revealed by host and viral population genomics. PLoS Genet 4:1–11

    Article  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    PubMed  Article  CAS  Google Scholar 

  • Barnett R, Yamaguchi N, Barnes I, Cooper A (2006a) Lost populations and preserving genetic diversity in the lion Panthera leo: implications for its ex situ conservation. Conserv Genet 7:507–514

    Article  Google Scholar 

  • Barnett R, Yamaguchi N, Barnes I, Cooper A (2006b) The origin, current diversity and future conservation of the modern lion (Panthera leo). Proc R Soc Lond B 273:2119–2125

    Article  Google Scholar 

  • Barnett R, Shapiro B, Barnes I, Ho SYW, Burger J, Yamaguchi N, Higham TFG, Wheeler HT, Rosendahl W, Sher AV (2009) Phylogeography of lions (Panthera leo ssp.) reveals three distinct taxa and a late Pleistocene reduction in genetic diversity. Mol Ecol 18:1668–1677

    PubMed  Article  Google Scholar 

  • Barton N, Slatkin M (1986) A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Hered 56:409–416

    Article  Google Scholar 

  • Bauer H, de Iongh HH (2005) Lion (Panthera leo) home ranges and livestock conflicts in Waza National Park, Cameroon. Afr J Ecol 43:208–214

    Article  Google Scholar 

  • Bauer H, Van Der Merwe S (2004) Inventory of free-ranging lions Panthera leo in Africa. Oryx 38:26–31

    Article  Google Scholar 

  • Bertola LD, van Hooft WF, Vrieling K, Uit de Weerd DR, York DS, Bauer H, Prins HHT, Funston PJ, Udo de Haes HA, Leirs H (2011) Genetic diversity, evolutionary history and implications for conservation of the lion (Panthera leo) in West and Central Africa. J Biogeogr 38:1356–1367

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Burger J, Rosendahl W, Loreille O, Hemmer H, Eriksson T, Gotherstrom A, Hiller J, Collins MJ, Wess T, Alt KW (2004) Molecular phylogeny of the extinct cave lion Panthera leo spelaea. Mol Phylogen Evol 30:841–849

    Article  CAS  Google Scholar 

  • Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35:31–52

    PubMed  Article  CAS  Google Scholar 

  • Burton AC, Buedi EB, Balangtaa C, Kpelle DG, Sam MK, Brashares JS (2011) The decline of lions in Ghana’s Mole National Park. Afr J Ecol 49:122–126

    Article  Google Scholar 

  • Deraniyagala PEP (1939) Some fossil animals from Ceylon Part II. J R Asiatic Soc (Ceylon Br) 34:231–239

    Google Scholar 

  • Dubach JM, Patterson BD, Briggs MB, Venzke K, Flammand 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 7:15–24

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Funston PJ (2011) Population characteristics of lions (Panthera leo) in the Kgalagadi Transfrontier Park. S Afr J Wildl Res 41:1–10

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Accessed on http://www.unil.ch./izea/softwares/fstat.html

  • Guggisberg CAW (1961) Simba, the life of the lion. Howard Timmins, Capetown

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372

    PubMed  Article  CAS  Google Scholar 

  • Hayward MW, Kerley GIH (2009) Fencing for conservation: restriction of evolutionary potential or a riposte to threatening processes? Biol Conserv 142:1–13

    Article  Google Scholar 

  • Hemmer H (1974) Zur Artgeschichte des Löwen Panthera (Panthera) leo (Linnaeus, 1758). Veroff Zool Staatssamml München 17:167–280

    Google Scholar 

  • Hunter LTB, Pretorius K, Carlisle LC, Rickelton M, Walker C, Slotow R, Skinner JD (2007) Restoring lions Panthera leo to northern KwaZulu-Natal, South Africa: short-term biological and technical success but equivocal long-term conservation. Oryx 41:196–204

    Article  Google Scholar 

  • IUCN (2012) IUCN Red List of Threatened Species. Version 2011.2

  • IUCN SSC Cat Specialist Group (2006a) Conservation strategy for the lion in West and Central Africa. IUCN, Gland, pp 1–60

    Google Scholar 

  • IUCN SSC Cat Specialist Group (2006b) Regional conservation strategy for the lion Panthera leo in Eastern and Southern Africa. IUCN, Gland, pp 1–60

    Google Scholar 

  • Kiffner C, Meyer B, Mühlenberg M, Waltert M (2009) Plenty of prey, few predators: what limits lions Panthera leo in Katavi National Park, western Tanzania? Oryx 43:52–59

    Article  Google Scholar 

  • Liedloff AC (1999) Mantel Nonparametric Test Calculator. Version 2.0. School of Natural Resource Sciences, Queensland University of Technology, Brisbane

  • Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum charateribus, differentiis, synonymis, locis. 10th edn. Imprint Holmiae, Impensis L. Salvii

  • Lyke MMK (2008) Molecular genetic analysis of African lion (Panthera leo) population structure in Etosha National Park. Northeastern Illinois University

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

    Google Scholar 

  • Manamendra-Arahchi K, Pethiyagoda R, Dissanayake R, Meegaskumbura M (2005) A second big cat from the late Quaternary of Sri Lanka. Raffles Bull Zool 12:423–434

    Google Scholar 

  • Marshall T, Slate J, Kruuk L, Pemberton J (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    PubMed  Article  CAS  Google Scholar 

  • Menotti-Raymond M, David VA, Lyons LA, Schäffer AA, Tomlin JF, Hutton MK, O’Brien SJ (1999) A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57:9–23

    PubMed  Article  CAS  Google Scholar 

  • Newman D, Tallmon DA (2002) Experimental evidence for beneficial fitness effects of gene flow in recently isolated populations. Conserv Biol 15:1054–1063

    Article  Google Scholar 

  • O’Brien SJ, Martenson JS, Packer C, Herbst L, de Vos V, Joslin P, Ott-Joslin J, Wildt DE, Bush M (1987) Biochemical genetic variation in geographic isolates of African and Asiatic lions. Nat Geogr Res 3:114–124

    Google Scholar 

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

    Article  Google Scholar 

  • Packer C, Ikanda D, Kissui B, Kushnir H (2005) Lion attacks on humans in Tanzania. Nature 436:927–928

    PubMed  Article  CAS  Google Scholar 

  • Park SJ (2001) Microsatellite Toolkit for Excel, v.3.1. Trinity College. University of Dublin, Dublin

  • Patterson BD, Kasiki SM, Selempo E, Kays RW (2004) Livestock predation by lions (Panthera leo) and other carnivores on ranches neighboring Tsavo National Parks, Kenya. Biol Conserv 119:507–516

    Article  Google Scholar 

  • Patterson BD, Kays RW, Kasiki SM, Sebestyen VM (2006) Developmental effects of climate on the lion’s mane (Panthera leo). J Mamm 87:193–200

    Article  Google Scholar 

  • Pocock RI (1931) The lions of Asia. J Bombay Nat Hist Soc 34:638–665

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    Google Scholar 

  • Pritchard JK, Wen W, Falush D (2003) Documentation for structure software: version 2. Department of Human Genetics, University of Chicago, Chicago, IL, pp 1–38

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Riggio J, Jacobson A, Dollar L, Bauer H, Becker M, Dickman A, Funston P, Groom R, Henschel P, Iongh Hd, Lichtenfeld L, Pimm S (2012) The size of savannah Africa: a lion’s (Panthera leo) view. Biodiv Conserv. doi:10.1007/s10531-10012-10381-10534

    Google Scholar 

  • Sanderson EW, Redford KH, Chetkiewicz CLB, Medellin RA, Rabinowitz AR, Robinson JG, Taber AB (2002) Planning to save a species: the jaguar as a model. Conserv Biol 16:58–72

    Article  Google Scholar 

  • Schnitzler AE (2011) Past and present distribution of the North African–Asian lion subgroup: a review. Mamm Rev 41:220–243

    Article  Google Scholar 

  • Smith H (1858) Introduction to mammalia. Jardine’s naturalist’s library 35:177

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. WH Freeman, New York

    Google Scholar 

  • StatSoft Inc (2005) Statistica (data analysis software system), version 7.1. www.statsoft.com. Accessed 12 Apr 2006

  • Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87:173–180

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    PubMed  Article  CAS  Google Scholar 

  • Todd NB (1966) Metrical and non-metrical variation in the skulls of Gir lions. J Bombay Nat Hist Soc 62:507–520

    Google Scholar 

  • 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

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Yamaguchi N, Haddane B (2002) The North African Barbary lion and the Atlas Lion Project. Int Zoo News 49:465–481

    Google Scholar 

  • Yamaguchi N, Kitchener AC, Driscoll CA, Macdonald DW (2009) Divided infraorbital foramen in the lion (Panthera leo): its implications for colonisation history, population bottlenecks, and conservation of the Asian lion (P. l. persica). Contrib Zool 78:77–83

    Google Scholar 

Download references

Acknowledgments

We thank Luke Hunter and Lisanne Petracca for providing the GIS layer for the LCUs and Steve Judd for help editing the STRUCTURE diagram. JMD received partial funding through a grant from the Conservation Medicine Center of Chicago, from N. Alberts, and from Drs. Kalina. MBB thanks the Namibian Ministry of Environment and Tourism for its support of fieldwork in Etosha, Bushmanland, and the Caprivi Strip. He also thanks the Botswana Department of Wildlife and National Parks for its support of fieldwork in collection of all samples originating in Botswana. PAW thanks the Zambia Wildlife Authority for permission to conduct this research, the Professional Hunters Association of Zambia for their kind assistance with all aspects of the field work, and the Safari Club International Foundation, Dallas Safari Club, Shikar Safari Club and several individual donors for their generous support. BDP thanks the Earthwatch Institute (#5123, 2002–2009), Field Museum of Natural History (Barbara E. Brown and Marshall Field Funds), and Dr. S. Kasiki of the Kenya Wildlife Service for support and facilitation in the field. We gratefully acknowledge two anonymous reviewers whose comments improved the value of this contribution.

Author information

Authors and Affiliations

  1. Department of Comparative Medicine, Loyola University Medical School, 2160 S. First Ave., Maywood, IL, 60153, USA

    J. M. Dubach

  2. APCRO, Inc., 289 Butte View Drive, Bolingbrook, IL, 60490, USA

    M. B. Briggs & B. A. Ament

  3. Center for Tropical Research, University of California, Los Angeles, CA, 90095-1496, USA

    P. A. White

  4. Science & Education, Field Museum of Natural History, Chicago, IL, 60605-2496, USA

    B. D. Patterson

Authors
  1. J. M. Dubach
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. B. Briggs
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. A. White
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B. A. Ament
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. D. Patterson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B. D. Patterson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 754 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dubach, J.M., Briggs, M.B., White, P.A. et al. Genetic perspectives on “Lion Conservation Units” in Eastern and Southern Africa. Conserv Genet 14, 741–755 (2013). https://doi.org/10.1007/s10592-013-0453-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-013-0453-3

Keywords

  • Panthera leo
  • Lion
  • Cytochrome-b
  • Haplotype
  • Microsatellite
  • Gene flow
  • Isolation-by-distance