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.

African Parks Network Lonehill Republic of South Africa

Batavia Coast Maritime Institute Geraldton WA Australia

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

Centre for Research and Conservation Royal Zoological Society of Antwerp Antwerp Belgium

Department of Biology University of Victoria Victoria Canada

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

Department of Forest and Conservation Sciences University of British Columbia Vancouver Canada

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

Division 12 Measles Mumps Rubella and Viruses Affecting Immune Compromised Patients Robert Koch Institute Berlin Germany

Dzanga Sangha Protected Areas WWF Central African Republic Bangui Central African Republic

Epidemiology of highly pathogenic microorganisms Robert Koch Institute Berlin Germany

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

Gashaka Primate Project Nigeria c o Department of Anthropology University College London London UK

German Centre for Integrative Biodiversity Research Leipzig Germany

Institute of Vertebrate Biology Academy of Sciences Brno Czech Republic

International Gorilla Conservation Programme Kigali Rwanda

KBA Secretariat c o BirdLife International Cambridge UK

Liberec Zoo Liberec Czech Republic

Max Planck Institute for Evolutionary Anthropology Leipzig Germany

North Carolina Zoological Park Asheboro USA

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

Royal Holloway University of London Egham UK

School of Biomedical and Healthcare Sciences University of Plymouth Devon UK

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

Viral Evolution Robert Koch Institute Berlin Germany

Wild Chimpanzee Foundation Leipzig Germany

Wildlife Conservation Society NY USA

World Wildlife Fund Germany Berlin Germany

WWF Cameroon Yaoundé Cameroon

Zoology Department Conservation Science Group University of Cambridge Cambridge UK

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