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Ancient co-speciation of simian foamy viruses and primates

Nature volume 434, pages 376–380 (2005)Cite this article

Abstract

Although parasite–host co-speciation is a long-held hypothesis, convincing evidence for long-term co-speciation remains elusive, largely because of small numbers of hosts and parasites studied and uncertainty over rates of evolutionary change1,2,3,4,5. Co-speciation is especially rare in RNA viruses, in which cross-species transfer is the dominant mode of evolution6,7,8,9. Simian foamy viruses (SFVs) are ubiquitous, non-pathogenic retroviruses that infect all primates10,11. Here we test the co-speciation hypothesis in SFVs and their primate hosts by comparing the phylogenies of SFV polymerase and mitochondrial cytochrome oxidase subunit II from African and Asian monkeys and apes. The phylogenetic trees were remarkably congruent in both branching order and divergence times, strongly supporting co-speciation. Molecular clock calibrations revealed an extremely low rate of SFV evolution, 1.7 × 10-8 substitutions per site per year, making it the slowest-evolving RNA virus documented so far. These results indicate that SFVs might have co-speciated with Old World primates for at least 30 million years, making them the oldest known vertebrate RNA viruses.

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Figure 1: Congruence of host/parasite phylogenies.
Figure 2: Co-evolutionary relationships of primate COII and SFV pol phylogenetic trees based on reconciliation analysis.
Figure 3: Correlation of branch lengths (substitutions per site) of primate COII and SFV pol phylogenetic trees.

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Acknowledgements

We thank the veterinary staff at all zoological gardens and primate centres who kindly provided blood specimens from the primates living at their institutions; R. Heberle and P. Johnston for the SFV-infected baboon and orangutan isolates; A. Hussain and A. Wright for expert technical assistance; and A. Vandamme, C. Coulibaly, M. Peeters, F. Bibollet-Ruche, V. Hirsch, J. Allan, T. Butler and H. McClure for providing additional primate samples for this study.

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Authors and Affiliations

  1. HIV and Retrovirology Branch, Division of HIV/AIDS Prevention, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, 1600 Clifton Road, MS G-19, Atlanta, Georgia, 30333, USA

    William M. Switzer, Vedapuri Shanmugam, Mian-er Cong, Vinod Bhullar & Walid Heneine

  2. Department of Pathology, Immunology and Laboratory Medicine, University of Florida, 1600 SW Archer Road, Gainesville, Florida, 32610, USA

    Marco Salemi

  3. Human Vaccine Institute, Duke University, 0112E Research Park III, Durham, North Carolina, 27710, USA

    Feng Gao

  4. Los Alamos National Laboratory, Los Alamos, New Mexico, 87545, USA

    Carla Kuiken

  5. Southern Research Institute, 431 Aviation Way, Frederick, Maryland, 21701, USA

    Brigitte E. Beer

  6. CNRS-Université Rennes I, Ethology, Evolution, Ecology, Station Biologique, 35380, Paimpont, France

    Dominique Vallet & Annie Gautier-Hion

  7. Cercopan, 4 Ishie Lane, c/o Housing Estate, PO Box 826, Cross River State, Calabar, Nigeria

    Zena Tooze

  8. Department of Pathology, Winship Cancer Center, Emory University, 1365B Clifton Road, Atlanta, Georgia, 30322, USA

    Francois Villinger

  9. Department of Zoology, University of Oxford, South Parks Road, OXI 3PS, Oxford, UK

    Edward C. Holmes

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  1. William M. Switzer
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Correspondence to William M. Switzer.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Tables 1 and 2

This file includes a list of the specimens used in this study and the corresponding taxon codes for the primate and SFV sequences shown in Figs 1-3. (PDF 39 kb)

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Switzer, W., Salemi, M., Shanmugam, V. et al. Ancient co-speciation of simian foamy viruses and primates. Nature 434, 376–380 (2005). https://doi.org/10.1038/nature03341

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