Ancient co-speciation of simian foamy viruses and primates


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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


  1. 1

    Hafner, M. S. et al. Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265, 1087–1090 (1994)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Page, R. D. M. Temporal congruence and cladistic analysis of biogeography and cospeciation. Syst. Zool. 39, 205–226 (1990)

    Article  Google Scholar 

  3. 3

    Brooks, D. R. Analysis of host-parasite coevolution. Int. J. Parasitol. 17, 291–297 (1987)

    CAS  Article  Google Scholar 

  4. 4

    Charrel, R. N., De Micco, P. & de Lamballerie, X. Phylogenetic analysis of GB viruses A and C: evidence for cospeciation between virus isolates and their primate hosts. J. Gen. Virol. 80, 2329–2335 (1999)

    CAS  Article  Google Scholar 

  5. 5

    McGeoch, D. J., Dolan, A. & Ralph, A. C. Toward a comprehensive phylogeny for mammalian and avian herpesviruses. J. Virol. 74, 10401–10406 (2000)

    CAS  Article  Google Scholar 

  6. 6

    Charleston, M. A. & Robertson, D. L. Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst. Biol. 51, 528–535 (2002)

    CAS  Article  Google Scholar 

  7. 7

    Salemi, M. et al. Mosaic genomes of the six major primate lentivirus lineages revealed by phylogenetic analyses. J. Virol. 77, 7202–7213 (2003)

    CAS  Article  Google Scholar 

  8. 8

    Jackson, A. P. & Charleston, M. A. A cophylogenetic perspective of RNA-virus evolution. Mol. Biol. Evol. 21, 45–57 (2004)

    CAS  Article  Google Scholar 

  9. 9

    Holmes, E. C. Molecular clocks and the puzzle of RNA virus origins. J. Virol. 77, 3893–3897 (2003)

    CAS  Article  Google Scholar 

  10. 10

    Meiering, C. D. & Linial, M. L. Historical perspective of foamy virus epidemiology and infection. Clin. Microbiol. Rev. 14, 165–176 (2001)

    CAS  Article  Google Scholar 

  11. 11

    Hussain, A. I. et al. Screening for simian foamy virus infection by using a combined antigen Western blot assay: evidence for a wide distribution among Old World primates and identification of four new divergent viruses. Virology 309, 248–257 (2003)

    CAS  Article  Google Scholar 

  12. 12

    Disotell, T. R., Honeycutt, R. L. & Ruvolo, M. Mitochondrial DNA phylogeny of the Old-World monkey tribe Papionini. Mol. Biol. Evol. 9, 1–13 (1992)

    CAS  PubMed  Google Scholar 

  13. 13

    Ruvolo, M., Disotell, T. R., Allard, M. W., Brown, W. M. & Honeycutt, R. L. Resolution of the African hominoid trichotomy by use of a mitochondrial gene sequence. Proc. Natl Acad. Sci. USA 88, 1570–1574 (1991)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Adkins, R. M. & Honeycutt, R. L. Evolution of the primate cytochrome C oxidase subunit II gene. J. Mol. Evol. 38, 215–231 (1994)

    ADS  CAS  Article  Google Scholar 

  15. 15

    van der Kuyl, A. C., Kuiken, C. L., Dekker, J. T. & Goudsmit, J. Phylogeny of African monkeys based upon mitochondrial 12S rRNA sequences. J. Mol. Evol. 40, 173–180 (1995)

    ADS  CAS  Article  Google Scholar 

  16. 16

    Page, S. L., Chiu, C. H. & Goodman, M. Molecular phylogeny of Old World monkeys (Cercopithecidae) as inferred from gamma-globin DNA sequences. Mol. Phylogenet. Evol. 13, 348–359 (1999)

    CAS  Article  Google Scholar 

  17. 17

    Harris, E. E. & Disotell, T. R. Nuclear gene trees and the phylogenetic relationships of the mangabeys (Primates: Papionini). Mol. Biol. Evol. 15, 892–900 (1998)

    CAS  Article  Google Scholar 

  18. 18

    Goodman, M. et al. Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence. Mol. Phylogenet. Evol. 9, 585–598 (1998)

    CAS  Article  Google Scholar 

  19. 19

    Page, S. L. & Goodman, M. Catarrhine phylogeny: noncoding DNA evidence for a diphyletic origin of the mangabeys and for a human-chimpanzee clade. Mol. Phylogenet. Evol. 18, 14–25 (2001)

    CAS  Article  Google Scholar 

  20. 20

    Murphy, W. J. et al. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294, 2348–2351 (2001)

    ADS  CAS  Article  Google Scholar 

  21. 21

    Sanderson, M. J. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301–302 (2003)

    CAS  Article  Google Scholar 

  22. 22

    Ruvolo, M. et al. Mitochondrial COII sequences and modern human origins. Mol. Biol. Evol. 10, 1115–1135 (1993)

    CAS  PubMed  Google Scholar 

  23. 23

    Shadan, F. F. & Villarreal, L. P. Coevolution of persistently infecting small DNA viruses and their hosts linked to host-interactive regulatory domains. Proc. Natl Acad. Sci. USA 90, 4117–4121 (1993)

    ADS  CAS  Article  Google Scholar 

  24. 24

    Johnson, W. E. & Coffin, J. M. Constructing primate phylogenies from ancient retrovirus sequences. Proc. Natl Acad. Sci. USA 96, 10254–10260 (1999)

    ADS  CAS  Article  Google Scholar 

  25. 25

    Suzuki, Y., Yamaguchi-Kabata, Y. & Gojobori, T. Nucleotide substitution rates of HIV-1. AIDS Rev. 2, 39–47 (2000)

    Google Scholar 

  26. 26

    Löchelt, M. Foamy virus transactivation and gene expression. Curr. Top. Microbiol. Immunol. 277, 27–61 (2003)

    PubMed  Google Scholar 

  27. 27

    Woelk, C. H. & Holmes, E. C. Reduced positive selection in vector-borne RNA viruses. Mol. Biol. Evol. 19, 2333–2336 (2002)

    CAS  Article  Google Scholar 

  28. 28

    Groves, C. Primate Taxonomy (Smithsonian Institution Press, Washington DC, 2001)

    Google Scholar 

  29. 29

    Sanderson, M. J. Estimate absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19, 101–109 (2002)

    CAS  Article  Google Scholar 

  30. 30

    Page, R. D. M. Parallel phylogenies: reconstructing the history of host-parasite assemblages. Cladistics 10, 155–173 (1994)

    Article  Google Scholar 

Download references


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.

Author information



Corresponding author

Correspondence to William M. Switzer.

Ethics declarations

Competing interests

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)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.