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Cytonuclear genomic dissociation in African elephant species

Abstract

African forest and savanna elephants are distinct species separated by a hybrid zone1,2,3,4. Because hybridization can affect the systematic and conservation status of populations, we examined gene flow between forest and savanna elephants at 21 African locations. We detected cytonuclear dissociation, indicative of different evolutionary histories for nuclear and mitochondrial genomes. Both paternally (n = 205 males) and biparentally (n = 2,123 X-chromosome segments) inherited gene sequences indicated that there was deep genetic separation between forest and savanna elephants. Yet in some savanna locales distant from present-day forest habitats, many individuals with savanna-specific nuclear genotypes carried maternally transmitted forest elephant mitochondrial DNA. This extreme cytonuclear dissociation implies that there were ancient episodes of hybridization between forest females and savanna males, which are larger and reproductively dominant to forest or hybrid males1,2,5,6,7. Recurrent backcrossing of female hybrids to savanna bulls replaced the forest nuclear genome. The persistence of residual forest elephant mitochondria in savanna elephant herds renders evolutionary interpretations based on mitochondrial DNA alone misleading and preserves a genomic record of ancient habitat changes.

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Figure 1: Map indicates locations of sampled elephant populations in Africa.
Figure 2: Haplotypes for three biparentally transmitted X-linked genes show almost complete differentiation among three elephant taxa.
Figure 3: Phylogenetic relationships for Asian, African forest and African savanna elephant gene sequences inferred using maximum likelihood for (a) 1,551 bp of the paternally inherited Y-chromosome AMELY gene, including 205 male African elephants (−ln L = 2227.88057) and (b) 319 bp of the maternally inherited mitochondrial ND5 gene, including 281 African elephants (−ln L = 658.63700).

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References

  1. Groves, C.P. & Grubb, P. Do Loxodonta cyclotis and L. africana interbreed? Elephant 2, 4–7 (2000).

    Article  Google Scholar 

  2. Grubb, P., Groves, C.P., Dudley, J.P. & Shoshani, J. Living African elephants belong to two species: Loxodonta africana (Blumenbach, 1797) and Loxodonta cyclotis (Matschie, 1900). Elephant 2, 1–4 (2000).

    Article  Google Scholar 

  3. Roca, A.L., Georgiadis, N., Pecon-Slattery, J. & O'Brien, S.J. Genetic evidence for two species of elephant in Africa. Science 293, 1473–1477 (2001).

    CAS  Article  Google Scholar 

  4. Comstock, K.E. et al. Patterns of molecular genetic variation among African elephant populations. Mol. Ecol. 11, 2489–2498 (2002).

    CAS  Article  Google Scholar 

  5. Poole, J.H. Signals and assessment in African elephants: evidence from playback experiments. Animal Behaviour 58, 185–193 (1999).

    CAS  Article  Google Scholar 

  6. Slotow, R., van Dyk, G., Poole, J., Page, B. & Klocke, A. Older bull elephants control young males. Nature 408, 425–426 (2000).

    CAS  Article  Google Scholar 

  7. Sukumar, R. The Living Elephants: Evolutionary Ecology, Behavior, and Conservation (Oxford University Press, Oxford, 2003).

    Google Scholar 

  8. Maglio, V.J. Origin and evolution of the Elephantidae. Trans. Am. Phil. Soc. Phila. New Series 63, 1–149 (1973).

    Article  Google Scholar 

  9. Georgiadis, N. et al. Structure and history of African elephant populations: I. Eastern and southern Africa. J. Heredity 85, 100–104 (1994).

    CAS  Article  Google Scholar 

  10. Nyakaana, S., Arctander, P. & Siegismund, H.R. Population structure of the African savannah elephant inferred from mitochondrial control region sequences and nuclear microsatellite loci. Heredity 89, 90–98 (2002).

    CAS  Article  Google Scholar 

  11. Eggert, L.S., Rasner, C.A. & Woodruff, D.S. 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, 1993–2006 (2002).

    CAS  Article  Google Scholar 

  12. Debruyne, R. How many species of elephants in Africa? Appraisal of an apparent controversy between molecular phylogenies. Cladistics 20, 80–81 (2004).

    Google Scholar 

  13. Murphy, W.J., Sun, S., Chen, Z.Q., Pecon-Slattery, J. & O'Brien, S.J. Extensive conservation of sex chromosome organization between cat and human revealed by parallel radiation hybrid mapping. Genome Res 9, 1223–1230 (1999).

    CAS  Article  Google Scholar 

  14. White, F. The Vegetation of Africa (UNESCO, Paris, 1983).

    Google Scholar 

  15. Blanc, J.J. et al. African Elephant Status Report 2002 (IUCN, Gland, Switzerland, 2003).

  16. Nyakaana, S., Abe, E.L., Arctander, P. & Siegismund, H.R. DNA evidence for elephant social behaviour breakdown in Queen Elizabeth National Park, Uganda. Animal Conservation 4, 231–237 (2001).

    Article  Google Scholar 

  17. Nagao, Y. et al. Decreased physical performance of congenic mice with mismatch between the nuclear and the mitochondrial genome. Genes Genet. Syst. 73, 21–27 (1998).

    CAS  Article  Google Scholar 

  18. Backhaus, D. Zur Variabilität der äusseren systematischen Merkmale des afrikanischen Elefanten (Loxodonta Cuvier, 1825). Säugetierk. Mitt. 6, 166–173 (1958).

    Google Scholar 

  19. Thompson, L.G. et al. Kilimanjaro ice core records: evidence of Holocene climate change in tropical Africa. Science 298, 589–593 (2002).

    CAS  Article  Google Scholar 

  20. Maley, J. & Brenac, P. Vegetation dynamics, palaeoenvironments and climatic changes in the forests of western Cameroon during the last 28,000 years BP. Rev. Palaeobot. Palynol. 99, 157–187 (1998).

    Article  Google Scholar 

  21. Shaw, P.A., Stokes, S., Thomas, D.S.G., Davies, F.B.M. & Holmgren, K. Palaeoecology and age of a Quaternary high lake level in the Makgadikgadi basin of the middle Kalahari, Botswana. S. Afr. J. Sci. 93, 273–276 (1997).

    CAS  Google Scholar 

  22. Rohwer, S., Bermingham, E. & Wood, C. Plumage and mitochondrial DNA haplotype variation across a moving hybrid zone. Evolution Int. J. Org. Evolution 55, 405–422 (2001).

    CAS  Article  Google Scholar 

  23. Silver, L.M. Mouse Genetics: Concepts and Applications (Oxford University Press, Oxford, 1995).

    Google Scholar 

  24. Coyne, J.A. & Orr, H.A. Speciation (Sinauer Associates, Sunderland, Massachusetts, 2004).

    Google Scholar 

  25. Nyakaana, S. & Arctander, P. 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, 1105–1115 (1999).

    CAS  Article  Google Scholar 

  26. Barriel, V., Thuet, E. & Tassy, P. Molecular phylogeny of Elephantidae. Extreme divergence of the extant forest African elephant. C. R. Acad. Sci. III 322, 447–454 (1999).

    CAS  Article  Google Scholar 

  27. Hebert, P.D.N., Cywinska, A., Ball, S.L. & deWaard, J.R. Biological identification through DNA barcodes. Proc. R. Soc. Lond. B Biol. Sci. 270, 313–321 (2003).

    CAS  Article  Google Scholar 

  28. Blaxter, M. Molecular systematics: Counting angels with DNA. Nature 421, 122–124 (2003).

    CAS  Article  Google Scholar 

  29. Roca, A.L., Geogiadis, N. & O'Brien, S.J. African elephant genetics: request for samples. Pachyderm 33, 93–95 (2002).

    Google Scholar 

  30. Vignaud, P. et al. Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Nature 418, 152–155 (2002).

    CAS  Article  Google Scholar 

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Acknowledgements

We thank R. Ruggiero, W. J. Murphy, A. Brandt, M. P. Gough, J. Brucksch, B. Gough, M. J. Malasky, J. Arthur, R. L. Hill, D. Munroe, E. Teeling, E. Eizirik, N. Yuhki, S. Cevario, G. K. Pei, K. M. Helgen and M. W. Smith for assistance or advice; A. Turkalo, J. M. Fay, R. Weladji, W. Karesh, M. Lindeque, W. Versvelt, K. Hillman Smith, F. Smith, M. Tchamba, S. Gartlan, P. Aarhaug, A. M. Austmyr, Bakari, Jibrila, J. Pelleteret, L. White, M. Habibou, M. W. Beskreo, D. Pierre, C. Tutin, M. Fernandez, R. Barnes, B. Powell, G. Doungoubé, M. Storey, M. Phillips, B. Mwasaga, A. Mackanga-Missandzou, K. Comstock, M. Keele, D. Olson, B. York, A. Baker and M. Bush for elephant samples; and the governments of Botswana, Cameroon, the Central African Republic, Congo (Brazzaville), Congo (Kinshasa), Gabon, Kenya, Namibia, South Africa, Tanzania and Zimbabwe for permission to collect samples. For funding we thank the US Fish and Wildlife Service, National Geographic Society and European Union (through the Wildlife Conservation Society). This publication has been funded in part with federal funds from the National Cancer Institute, National Institutes of Health. The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government.

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Correspondence to Alfred L Roca or Stephen J O'Brien.

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Supplementary information

Supplementary Fig. 1

Haplotype labels. (PDF 89 kb)

Supplementary Fig. 2

Variable sites among gene haplotypes. (PDF 84 kb)

Supplementary Table 1

Gene allele summary by locale. (PDF 100 kb)

Supplementary Table 2

Gene alleles by locale. (PDF 95 kb)

Supplementary Table 3

Cytonuclear dissociation by locale. (PDF 98 kb)

Supplementary Methods (PDF 98 kb)

Supplementary Note

Hybridization generations and time frames. (PDF 96 kb)

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Roca, A., Georgiadis, N. & O'Brien, S. Cytonuclear genomic dissociation in African elephant species. Nat Genet 37, 96–100 (2005). https://doi.org/10.1038/ng1485

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