Cytomegalovirus distribution and evolution in hominines

Author:

Murthy Sripriya1,O’Brien Kathryn2,Agbor Anthony34,Angedakin Samuel3,Arandjelovic Mimi3,Ayimisin Emmanuel Ayuk3,Bailey Emma3,Bergl Richard A5,Brazzola Gregory3,Dieguez Paula3,Eno-Nku Manasseh6,Eshuis Henk3,Fruth Barbara78,Gillespie Thomas R9,Ginath Yisa3,Gray Maryke1011,Herbinger Ilka12,Jones Sorrel313,Kehoe Laura141516,Kühl Hjalmar317,Kujirakwinja Deo18,Lee Kevin319,Madinda Nadège F320,Mitamba Guillain18,Muhindo Emmanuel18,Nishuli Radar21,Ormsby Lucy J3,Petrzelkova Klara J22232425,Plumptre Andrew J182627,Robbins Martha M3,Sommer Volker28,Ter Heegde Martijn20,Todd Angelique29,Tokunda Raymond22,Wessling Erin329,Jarvis Michael A2,Leendertz Fabian H20,Ehlers Bernhard1,Calvignac-Spencer Sébastien2030ORCID

Affiliation:

1. Division 12 “Measles, Mumps, Rubella and Viruses Affecting Immune-Compromised Patients” Robert Koch Institute, Berlin, Germany

2. School of Biomedical and Healthcare Sciences, University of Plymouth, Devon, UK

3. Max Planck Institute for Evolutionary Anthropology (MPI EVA), Leipzig, Germany

4. African Parks Network, Lonehill, Republic of South Africa

5. North Carolina Zoological Park, Asheboro, USA

6. WWF Cameroon, Yaoundé, Cameroon

7. Faculty of Science, School of Natural Sciences and hPsychology, Liverpool John Moores University, Liverpool, UK

8. Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, Belgium

9. Department of Environmental Sciences and Program in Population Biology, Ecology, and Evolutionary Biology, Emory University, Atlanta, USA

10. International Gorilla Conservation Programme, Kigali, Rwanda

11. Batavia Coast Maritime Institute, Geraldton, WA, Australia

12. World Wildlife Fund (WWF) Germany, Berlin, Germany

13. Royal Holloway, University of London, Egham, UK

14. Wild Chimpanzee Foundation (WCF), Leipzig, Germany

15. Department of Biology, University of Victoria, Victoria, Canada

16. Department of Forest and Conservation Sciences, University of British Columbia, Vancouver, Canada

17. German Centre for Integrative Biodiversity Research (iDiv), Leipzig, Germany

18. Wildlife Conservation Society, NY, USA

19. School of Human Evolution and Social Change, Arizona State University, Tempe, USA

20. Epidemiology of highly pathogenic microorganisms, Robert Koch Institute, Berlin, Germany

21. Réserve de Faune à Okapis, Institut Congolais pour la Conservation de la Nature, Kinshasa, Democratic Republic of the Congo

22. Institute of Vertebrate Biology, Academy of Sciences, Brno, Czech Republic

23. Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences, Brno, Czech Republic

24. Biology Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, Ceske Budejovice, Czech Republic

25. Liberec Zoo, Liberec, Czech Republic

26. KBA Secretariat, c/o BirdLife International, Cambridge, UK

27. Zoology Department, Conservation Science Group, University of Cambridge, Cambridge, UK

28. Gashaka Primate Project, Nigeria c/o Department of Anthropology, University College London, London, UK

29. Dzanga Sangha Protected Areas, WWF Central African Republic, Bangui, Central African Republic

30. Viral Evolution, Robert Koch Institute, Berlin, Germany

Abstract

Abstract Herpesviruses are thought to have evolved in very close association with their hosts. This is notably the case for cytomegaloviruses (CMVs; genus Cytomegalovirus) infecting primates, which exhibit a strong signal of co-divergence with their hosts. Some herpesviruses are however known to have crossed species barriers. Based on a limited sampling of CMV diversity in the hominine (African great ape and human) lineage, we hypothesized that chimpanzees and gorillas might have mutually exchanged CMVs in the past. Here, we performed a comprehensive molecular screening of all 9 African great ape species/subspecies, using 675 fecal samples collected from wild animals. We identified CMVs in eight species/subspecies, notably generating the first CMV sequences from bonobos. We used this extended dataset to test competing hypotheses with various degrees of co-divergence/number of host switches while simultaneously estimating the dates of these events in a Bayesian framework. The model best supported by the data involved the transmission of a gorilla CMV to the panine (chimpanzee and bonobo) lineage and the transmission of a panine CMV to the gorilla lineage prior to the divergence of chimpanzees and bonobos, more than 800,000 years ago. Panine CMVs then co-diverged with their hosts. These results add to a growing body of evidence suggesting that viruses with a double-stranded DNA genome (including other herpesviruses, adenoviruses, and papillomaviruses) often jumped between hominine lineages over the last few million years.

Publisher

Oxford University Press (OUP)

Subject

Virology,Microbiology

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