Bats, Primates, and the Evolutionary Origins and Diversification of Mammalian Gammaherpesviruses

Author:

Escalera-Zamudio Marina1ORCID,Rojas-Anaya Edith2,Kolokotronis Sergios-Orestis3,Taboada Blanca4,Loza-Rubio Elizabeth2,Méndez-Ojeda Maria L.5,Arias Carlos F.4ORCID,Osterrieder Nikolaus5,Greenwood Alex D.16

Affiliation:

1. Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research (IZW), Berlin, Germany

2. Centro Nacional de Investigación Disciplinaria en Microbiología Animal—INIFAP, Mexico City, Mexico

3. Department of Epidemiology and Biostatistics, School of Public Health, SUNY Downstate Medical Center, Brooklyn, New York, USA

4. Departamento de Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico

5. Facultad de Medicina Veterinaria y Zootecnia, Universidad Veracruzana, Veracruz, Mexico, and Institut für Virologie, Robert von Ostertag-Haus-Zentrum für Infektionsmedizin, Department of Veterinary Medicine, Freie Universität Berlin, Berlin, Germany

6. Department of Veterinary Medicine, Freie Universität Berlin, Berlin, Germany

Abstract

ABSTRACT Gammaherpesviruses (γHVs) are generally considered host specific and to have codiverged with their hosts over millions of years. This tenet is challenged here by broad-scale phylogenetic analysis of two viral genes using the largest sample of mammalian γHVs to date, integrating for the first time bat γHV sequences available from public repositories and newly generated viral sequences from two vampire bat species ( Desmodus rotundus and Diphylla ecaudata ). Bat and primate viruses frequently represented deep branches within the supported phylogenies and clustered among viruses from distantly related mammalian taxa. Following evolutionary scenario testing, we determined the number of host-switching and cospeciation events. Cross-species transmissions have occurred much more frequently than previously estimated, and most of the transmissions were attributable to bats and primates. We conclude that the evolution of the Gammaherpesvirinae subfamily has been driven by both cross-species transmissions and subsequent cospeciation within specific viral lineages and that the bat and primate orders may have potentially acted as superspreaders to other mammalian taxa throughout evolutionary history. IMPORTANCE It has long been believed that herpesviruses have coevolved with their hosts and are species specific. Nevertheless, a global evolutionary analysis of bat viruses in the context of other mammalian viruses, which could put this widely accepted view to the test, had not been undertaken until now. We present two main findings that may challenge the current view of γHV evolution: multiple host-switching events were observed at a higher rate than previously appreciated, and bats and primates harbor a large diversity of γHVs which may have led to increased cross-species transmissions from these taxa to other mammals.

Publisher

American Society for Microbiology

Subject

Virology,Microbiology

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