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Conservation Genetics

, Volume 19, Issue 1, pp 155–167 | Cite as

Origin and phylogeography of African savannah elephants (Loxodonta africana) in Kruger and nearby parks in southern Africa

  • Alida de FlaminghEmail author
  • Alfred L. Roca
  • Rudi J. van Aarde
Research Article

Abstract

African savannah elephants (Loxodonta africana) occur in fragmented and isolated populations across southern Africa. Transfrontier conservation efforts aim at preventing the negative effects of population fragmentation by maintaining and restoring linkages between protected areas. We sought to identify genetic linkages by comparing the elephants in Kruger National Park (South Africa) to populations in nearby countries (Botswana, Mozambique, Zambia and Zimbabwe). We used a 446 base pair mitochondrial DNA (mtDNA) control region fragment (141 individuals) and 9 nuclear DNA (nDNA) microsatellite markers (69 individuals) to investigate phylogenetic relationships and gene flow among elephant populations. The mtDNA and nDNA phylogeographic patterns were incongruent, with mtDNA patterns likely reflecting the effects of ancient female migrations, with patterns persisting due to female philopatry, and nDNA patterns likely reflecting male-mediated dispersal. Kruger elephant heterozygosity and differentiation were examined, and were not consistent with genetic isolation, a depleted gene pool or a strong founder effect. Mitochondrial DNA geographic patterns suggested that the Kruger population was founded by elephants from areas both north and south of Kruger, or has been augmented through migration from more than one geographic source. We discuss our findings in light of the need for conservation initiatives that aim at maintaining or restoring connectivity among populations. Such initiatives may provide a sustainable, self-regulating management approach for elephants in southern Africa while maintaining genetic diversity within and gene flow between Kruger and nearby regions.

Keywords

African elephant Loxodonta africana Phylogeography Population structure Gene flow Kruger National Park Fecal DNA 

Notes

Acknowledgements

The projected was funded through grants to RJvA from the International Fund for Animal Welfare and the Conservation Foundation (Zambia). Elephants Without Borders (Botswana) kindly facilitated sample collection. The Zambian Wildlife Authority, the Department of Wildlife and National Parks (Botswana), South African National Parks (SANParks) and the Department of Agriculture, Forestry and Fisheries (South Africa) sanctioned our research activities. We acknowledge the support of a team of post-graduate students that assisted with the collection of study material, the support provided by the University of Pretoria’s Sequencing Facility, and Prof. Sydney Cameron for her help in the early stages of manuscript preperation. Travel and research support for AdeF was provided through the Francis M. and Harlie M. Clark Research Support Grant (2016), the Harley J. Van Cleave Research Award, and the University of Illinois Graduate College Dissertation Project Travel Grant. AdeF was also supported by the Cooperative State Research, Education, and Extension Service, US Department of Agriculture, under project number ILLU 875–952. ALR was supported by the US Fish and Wildlife Service African Elephant Conservation Fund.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10592_2017_1005_MOESM1_ESM.docx (4.7 mb)
Supplementary material 1 (DOCX 4842 KB)

References

  1. Allendorf FW, Luikart G, Aitken SN (2013) Conservation and the genetics of populations, 2nd edn. Blackwell Publishing, Wiley and Sons. LTD, West SussexGoogle Scholar
  2. Andreasson H, Gyllensten U, Allen M (2002) Real-time DNA quantification of nuclear and mitochondrial DNA in forensic analysis. Biotechniques 33:402–411PubMedGoogle Scholar
  3. Archie EA, Hollister-Smith JA, Poole JH, Lee PC, Moss CJ, Maldonado JE, Fleischer RC, Alberts SC (2007) Behavioural inbreeding avoidance in wild African elephants. Mol Ecol 16:4138–4148CrossRefPubMedGoogle Scholar
  4. Archie EA, Maldonado JE, Hollister-Smith JA, Poole JH, Moss CJ, Fleischer RC, Alberts SC (2008) Fine-scale population genetic structure in a fission–fusion society. Mol Ecol 17:2666–2679CrossRefPubMedGoogle Scholar
  5. Bouckaert RR (2010) DensiTree: making sense of sets of phylogenetic trees. Bioinformatics 26(10):1372–1373CrossRefPubMedGoogle Scholar
  6. Comstock KE, Georgiadis N, Pecon-Slattery J, Roca AL, Ostrander EA, O’Brien SJ, Wasser SK (2002) Patterns of molecular genetic variation among African elephant populations. Mol Ecol 11:2489–2498. doi: 10.1046/j.1365-294X.2002.01615.x CrossRefPubMedGoogle Scholar
  7. Corander J, Waldmann P, Sillanpää MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374PubMedPubMedCentralGoogle Scholar
  8. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  9. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772CrossRefPubMedPubMedCentralGoogle Scholar
  10. de Flamingh A, Sole CL, van Aarde RJ (2014) Microsatellite repeat motif and amplicon length affect amplification success of degraded faecal DNA. Conserv Genet Resour 6:503–505. doi: 10.1007/s12686-014-0160-5 CrossRefGoogle Scholar
  11. de Flamingh A, Sole CL, Van Aarde RJ (2015) Genetic evidence for spatial structuring in a continuous African elephant (Loxodonta africana) population. Conserv Genet 16:613–623CrossRefGoogle Scholar
  12. Dublin HT, Niskanen L (2003). Guidelines for the in situ translocation of the African elephant for conservation purposes. IUCN, CambridgeGoogle Scholar
  13. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  14. Eggert LS, Rasner CA, Woodruff DS (2002) The evolution and phylogeography of the African elephant inferred from mitochondrial DNA sequence and nuclear microsatellite markers. Proc R Soc Lond B Biol Sci 269:1993–2006CrossRefGoogle Scholar
  15. Enk J, Devault A, Debruyne R, King CE, Treangen T, O’Rourke D, Salzberg SL, Fisher D, MacPhee R, Poinar H (2011) Complete Columbian mammoth mitogenome suggests interbreeding with woolly mammoths. Genome Biol 12:1CrossRefGoogle Scholar
  16. 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. doi: 10.1111/j.1755-0998.2010.02847.x CrossRefPubMedGoogle Scholar
  17. Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280. doi: 10.1111/j.1466-8238.2007.00287.x CrossRefGoogle Scholar
  18. Fishlock V, Lee PC (2013) Forest elephants: fission–fusion and social arenas. Anim Behav 85:357–363CrossRefGoogle Scholar
  19. Fitzpatrick JL, Evans JP (2009) Reduced heterozygosity impairs sperm quality in endangered mammals. Biol Lett 5:320–323. doi: 10.1098/rsbl.2008.0734 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gilbert MTP, Drautz DI, Lesk AM, Ho SY, Qi J, Ratan A, Hsu C-H, Sher A, Dalén L, Götherström, A et al (2008) Intraspecific phylogenetic analysis of Siberian woolly mammoths using complete mitochondrial genomes. Proc Natl Acad Sci 105:8327–8332CrossRefPubMedPubMedCentralGoogle Scholar
  21. Guillot G, Mortier F, Estoup A (2005) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715. doi: 10.1111/j.1471-8286.2005.01031.x CrossRefGoogle Scholar
  22. Guillot G, Leblois R, Coulon A, Frantz AC (2009) Statistical methods in spatial genetics. Mol Ecol 18:4734–4756CrossRefPubMedGoogle Scholar
  23. Hall-Martin AJ (1992) Distribution and status of the African elephant Loxodonta africana in South Africa. Koedoe 35:65–88CrossRefGoogle Scholar
  24. Hanks J (2003) Transfrontier Conservation Areas (TFCAs) in Southern Africa: their role in conserving biodiversity, socioeconomic development and promoting a culture of peace. J Sustain For 17:127–148CrossRefGoogle Scholar
  25. Ishida Y, Oleksyk TK, Georgiadis NJ, David VA, Zhao K, Stephens RM, Kolokotronis S-O, Roca AL (2011) Reconciling apparent conflicts between mitochondrial and nuclear phylogenies in African elephants. PloS ONE 6:e20642CrossRefPubMedPubMedCentralGoogle Scholar
  26. Ishida Y, Georgiadis NJ, Hondo T, Roca AL (2013) Triangulating the provenance of African elephants using mitochondrial DNA. Evol Appl 6:253–265. doi: 10.1111/j.1752-4571.2012.00286.x CrossRefPubMedGoogle Scholar
  27. Krause J, Dear PH, Pollack JL, Slatkin M, Spriggs H, Barnes I, Lister AM, Ebersberger I, Pääbo S, Hofreiter M (2006) Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae. Nature 439:724–727CrossRefPubMedGoogle Scholar
  28. Li G, Davis BW, Eizirik E, Murphy WJ (2016) Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae). Genome Res 26:1–11CrossRefPubMedPubMedCentralGoogle Scholar
  29. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  30. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247CrossRefPubMedGoogle Scholar
  31. Maikaeu U, Wajjwalku W, Siripholwat V, Mahasawankul S (2007) The study of nucleotides arrangement of mitochondrial DNA in Thai elephants. KKU Vet J 17:11–21Google Scholar
  32. McDonald JH (2009) Handbook of biological statistics. Sparky House Publishing, BaltimoreGoogle Scholar
  33. Miller EJ, Eldridge M.D.B., Morris KD, Zenger KR, Herbert CA (2011) Genetic consequences of isolation: island tammar wallaby (Macropus eugenii) populations and the conservation of threatened species. Conserv Genet 12:1619–1631. doi: 10.1007/s10592-011-0265-2 CrossRefGoogle Scholar
  34. Nyakaana S, Arctander P (1999) Population genetic structure of the African elephant in Uganda based on variation at mitochondrial and nuclear loci: evidence for male-biased gene flow. Mol Ecol 8:1105–1115CrossRefPubMedGoogle Scholar
  35. Okello JB, Masembe C, Rasmussen HB, Wittemyer G, Omondi P, Kahindi O, Muwanika VB, Arctander P, Douglas-Hamilton I, Nyakaana S et al (2008) Population genetic structure of savannah elephants in Kenya: conservation and management implications. J Hered 99:443–452CrossRefPubMedGoogle Scholar
  36. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  37. Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-BëEr E, Robinson S, VáSquez-Carrillo C, Pauli JN, PalsbøLl PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines: RELIABILITY OF GENETIC BOTTLENECK TESTS. Mol Ecol 21:3403–3418. doi: 10.1111/j.1365-294X.2012.05635.x CrossRefPubMedGoogle Scholar
  38. Petit RJ, Excoffier L (2009) Gene flow and species delimitation. Tree 24:386–393PubMedGoogle Scholar
  39. Pienaar UDV (1963) Large mammals of the Kruger National Park—Their distribution and present-day status. Koedoe 6:1–137Google Scholar
  40. Rambaut A, Suchard M, Xie D, Drummond A (2014) Tracer v1.6. Tracer V16 Available HttpbeastbioedacukTracer 6Google Scholar
  41. Ripple WJ, Newsome TM, Wolf C, Dirzo R, Everatt KT, Galetti M, Hayward MW, Kerley GIH, Levi T, Lindsey PA, Macdonald DW, Malhi Y, Painter LE, Sandom CJ, Terborgh J, Van Valkenburgh B (2015) Collapse of the world’s largest herbivores. Sci Adv. doi: 10.1126/sciadv.1400103 PubMedPubMedCentralGoogle Scholar
  42. Roca AL, Georgiadis N, Pecon-Slattery J, O’Brien SJ (2001) Genetic evidence for two species of elephant in Africa. Science 293:1473–1477CrossRefPubMedGoogle Scholar
  43. Roca AL, Ishida Y, Brandt AL, Benjamin NR, Zhao K, Georgiadis NJ (2015) Elephant natural history: a genomic perspective. Annu Rev Anim Biosci 3:139–167CrossRefPubMedGoogle Scholar
  44. Roever CL, van Aarde RJ, Leggett K (2013) Functional connectivity within conservation networks: delineating corridors for African elephants. Biol Conserv 157:128–135. doi: 10.1016/j.biocon.2012.06.025 CrossRefGoogle Scholar
  45. Rogaev EI, Moliaka YK, Malyarchuk BA, Kondrashov FA, Derenko MV, Chumakov I, Grigorenko AP, 2006. Complete mitochondrial genome and phylogeny of Pleistocene mammoth Mammuthus primigenius. PLoS Biol 4:e73CrossRefPubMedPubMedCentralGoogle Scholar
  46. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  47. Scholes RJ, Mennell KG (eds) (2008) Elephant management: a scientific assessment for South Africa. Wits University Press, JohannesburgGoogle Scholar
  48. Schwarz C, Debruyne R, Kuch M, McNally E, Schwarcz H, Aubrey AD, Bada J, Poinar H (2009) New insights from old bones: DNA preservation and degradation in permafrost preserved mammoth remains. Nucleic Acids Res 37:3215–3229. doi: 10.1093/nar/gkp159 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol Evol 14:323–327CrossRefPubMedGoogle Scholar
  50. van Aarde RJ, Jackson TP (2007) Megaparks for metapopulations: addressing the causes of locally high elephant numbers in southern Africa. Biol Conserv 134:289–297CrossRefGoogle Scholar
  51. van Aarde RJ, Whyte I, Pimm S (1999) Culling and the dynamics of the Kruger National Park African elephant population. Anim Conserv 2:287–294CrossRefGoogle Scholar
  52. Wheeler DC, Waller LA, Biek R (2010) Spatial analysis of feline immunodeficiency virus infection in cougars. Spat Spatiotemporal Epidemiol 1:151–161CrossRefPubMedPubMedCentralGoogle Scholar
  53. Whitehouse AM, Harley EH (2001) Post-bottleneck genetic diversity of elephant populations in South Africa, revealed using microsatellite analysis. Mol Ecol 10:2139–2149CrossRefPubMedGoogle Scholar
  54. Whyte I (2001) Conservation management of the Kruger National Park elephant population. University of Pretoria, PhD thesis: ZoologyGoogle Scholar
  55. Young KD, Ferreira SM, van Aarde RJ (2009) The influence of increasing population size and vegetation productivity on elephant distribution in the Kruger National Park. Austral Ecol 34:329–342. doi: 10.1111/j.1442-9993.2009.01934.x CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Conservation Ecology Research Unit, Department of Zoology and EntomologyUniversity of PretoriaPretoriaSouth Africa
  2. 2.Program in Ecology, Evolution and Conservation Biology, School of Integrative BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  3. 3.Department of Animal SciencesUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  4. 4.Carl R. Woese Institute for Genomic BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

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