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Cytonuclear genomic dissociation in African elephant species

Nature Genetics volume 37, pages 96–100 (2005)Cite this article

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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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.

Author information

Authors and Affiliations

  1. Laboratory of Genomic Diversity, Basic Research Program, SAIC-Frederick, Frederick, 21702, Maryland, USA

    Alfred L Roca

  2. Mpala Research Center, PO Box 555, Nanyuki, Kenya

    Nicholas Georgiadis

  3. Laboratory of Genomic Diversity, National Cancer Institute, Frederick, 21702, Maryland, USA

    Stephen J O'Brien

Authors
  1. Alfred L Roca
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  2. Nicholas Georgiadis
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  3. Stephen J O'Brien
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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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