Cytomegalovirus distribution and evolution in hominines

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.

Evolution and Genetic Diversity of Primate Cytomegaloviruses

“…For example, in breeding colonies of rhesus macaques, almost the totality of animals are seropositive for RhCMV (rhesus macaque CMV) before the first year of age. High rates of infection were also reported for other NHPs in the wild [10,33,41]. Overlaps between HCMV and NHP CMVs are also observed in terms of infection outcome and clinical presentation.…”

“…As anticipated above, CMVs infect a wide variety of NHPs (Table 1) [7][8][9][10][11][33][34][35][36][37][38][39][40]. As detailed in the following section, NHP-infecting CMVs share with HCMV a similar genomic organization and coding content, as well as the course of viral infection (lifelong persistence).…”

Multiple DNA viruses identified in multimammate mouse (Mastomys natalensis) populations from across regions of sub-Saharan Africa

“…[10][11][12][13]39]). It is tempting to interpret this pattern as suggesting that these viruses co-diverged with their hosts and are M. natalensis-specific, since co-divergence is an important process in shaping herpesvirus and polyomavirus evolution [2,4,14,15,28,33]. Therefore, despite the commensality, abundance, and extensive geographic range of this rodent species, we do not expect these DNA viruses to represent a major zoonotic threat.…”

Mouse Cytomegalovirus M34 Encodes a Non-essential, Nuclear, Early-Late Expressed Protein Required for Efficient Viral Replication

“…Resulting from millions of years of co-evolution, cytomegaloviruses (CMVs) specifically adapted to their corresponding host species. Although cross-species infections may occur and contribute to the evolution of CMVs (Murthy et al, 2019), CMV species are usually restricted to one or few closely related host species in natura. In agreement with the species specificity, HCMV is incapable to productively replicate in small animals such as mice or rats.…”