DNA Polymerase Sequences of New World Monkey Cytomegaloviruses: Another Molecular Marker with Which To Infer Platyrrhini Systematics

Abstract

Over the past few decades, a large number of studies have identified herpesvirus sequences from many mammalian species around the world. Among the different nonhuman primate species tested so far for cytomegaloviruses (CMVs), only a few were from the New World. Seeking to identify CMV homologues in New World monkeys (NWMs), we carried out molecular screening of 244 blood DNA samples from 20 NWM species from Central and South America. Our aim was to reach a better understanding of their evolutionary processes within the Platyrrhini parvorder. Using PCR amplification with degenerate consensus primers targeting highly conserved amino acid motifs encoded by the herpesvirus DNA polymerase gene, we characterized novel viral sequences from 12 species belonging to seven genera representative of the three NWM families. BLAST searches, pairwise nucleotide and amino acid sequence comparisons, and phylogenetic analyses confirmed that they all belonged to the genus. Previously determined host taxa allowed us to demonstrate a good correlation between the distinct monophyletic clades of viruses and those of the infected primates at the genus level. In addition, the evolutionary branching points that separate NWM CMVs were congruent with the divergence dates of their hosts at the genus level. These results significantly expand our knowledge of the host range of this viral genus and strongly support the occurrence of cospeciation between these viruses and their hosts. In this respect, we propose that NWM CMV DNA polymerase gene sequences may serve as reliable molecular markers with which to infer Platyrrhini phylogenetics. Investigating evolutionary processes between viruses and nonhuman primates has led to the discovery of a large number of herpesviruses. No study published so far on primate cytomegaloviruses has extensively studied New World monkeys (NWMs) at the subspecies, species, genus, and family levels. The present study sought to identify cytomegalovirus homologues in NWMs and to decipher their evolutionary relationships. This led us to characterize novel viruses from 12 of the 20 primate species tested, which are representative of the three NWM families. The identification of distinct viruses in these primates not only significantly expands our knowledge of the host range of this viral genus but also sheds light on its evolutionary history. Phylogenetic analyses and molecular dating of the sequences obtained support a virus-host coevolution.

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).…”

“…Finally, different studies indicated that congenital RhCMV transmission recapitulates congenital HCMV pathogenesis, with spontaneous abortions or fetuses with brain and neurological defects [42]. Red-facied spider monkey Ateles paniscus cytomegalovirus (ApanCMV) [10] Note: ICTV-recognized viral species are in italic; bold and asterisks denote complete genome sequences.…”

“…The first CMV identified in a NHP was isolated in 1962 from an African green monkey (Cercopithecus aethiops) [44]. Thereafter, natural CMV infection was reported in a multitude of NHPs [9,10,33,35,37]. Initially, NHP CMVs were detected mostly in captive animals, but in the last few years surveys were extended to animals living in the wild, so as to generate a more accurate picture of the genetic diversity and distribution of these viruses in nature [9,10,33,35].…”

“…Indeed, cross-species transmission is repeatedly reported for members of the Alphaherpesvirinae and the Gammaherpesvirinae subfamilies [3][4][5][6]. Conversely, in betaherpesviruses, inter-species transmissions are rare events, indicating that, in natura, these viruses are restricted to their natural host [7][8][9][10] (see below).…”