Genomic diversity and evolution of papillomaviruses in rhesus monkeys

Abstract

We are studying the diversity of and relationships among papillomaviruses (PVs) to understand the modes and timescales of PV evolution and in the hope of finding animal PVs that may serve as model systems for disease caused by human PVs (HPVs). Toward this goal, we have examined 326 genital samples from rhesus monkeys and long-tailed macaques with a PCR protocol optimized for detecting genital HPV types. In 28 of the rhesus monkey samples, we found amplicons derived from 12 different and novel PV genomes, RhPV-a to RhPV-m, with the likely taxonomic status of "type." The frequency with which novel RhPVs were detected suggests that rhesus monkeys may play host to PVs with a diversity similar to that of humans. In phylogenetic trees, all 12 of the different RhPVs and the previously described type RhPV-1 were members of the genital HPV supergroup and formed three minor branches distinct from the 11 branches formed by genital HPVs. We also identified a novel PV amplicon, MfPV-a, from a long-tailed macaque, a species belonging to the same genus as rhesus monkeys. MfPV-a turned out to be a close relative of five RhPVs. It appears that the evolution of primate lineages leading to the genus Macaca and to humans created transmission barriers for PVs, resulting in viral evolution closely linked to the host. Additional support for the linked-evolution hypothesis comes from considering the phylogenetic association of two other ape and monkey PVs with the genital HPVs, the supergroup formed by at least seven ungulate PVs, and the isolated phylogenetic position of the only known bird PV.

Genetic characterization of the first chiropteran papillomavirus, isolated from a basosquamous carcinoma in an Egyptian fruit bat: The Rousettus aegyptiacus papillomavirus type 1

“…The limited number of non-human PVs that has been characterized to date covers a broad range of host species, including mostly domestic and wild mammals and two bird species (Sundberg, 1987;Sundberg et al, 1997;Tachezy et al, 2002b). Taken together with the numerous partial sequences of putative novel non-human PVs that have been reported (Chan et al, 1997;Antonsson and Hansson, 2002;Ogawa et al, 2004) this suggest that every vertebrate species could carry its own set of species-specific PVs.…”

Role of viruses in human evolution

“…Host-linked evolution: A form of cospeciation, in which well-adapted viruses living in single hosts, through ancient association with them, have diverged and speciated along with their hosts. Isolation of virus populations and selection pressure exerted by the host are important factors in this process, which results in a correlation between virus and host phylogenies (Chan et al, 1997).…”

“…The Papovaviridae present a phylogeny similar to that of the herpesviruses, with ancient branching points and evidence of cospeciation (Ong et al, 1993;Shadan and Villareal, 1993;Van Ranst et al, 1995; Chan et al, 1997). This family of very small DNA viruses makes maximal use of minimal genomes by using overlapping reading frames on both DNA strands, thus putting a selective constraint on its ability to mutate and resulting in slow rates of evolution, on the same order as cellular DNA (Chan et al, 1992;Hatwell and Sharp, 2000).…”

“…5), which cause prolonged latent infections in birds and mammals (Bailey and Mautner, 1994;Kidd et al, 1995;and Song et al, 1996). Interpretation of adenovirus relationships is complicated, however, by evidence of recombination in its "virus-associated RNA" (VA RNA), i.e., small, regulatory RNAs abundant in the Chan et al (1997), and Shadan and Villareal (1993). Viruses that regularly infect humans are indicated by bold amd italicized capitals.…”

An Introduction to the Evolutionary Ecology of Viruses

“…Papillomaviruses often cluster phylogenetically into monophyletic groups whose viral taxa exploit one tissue type (e.g., genital versus epidermal epithelial) yet encompass more than one host species (Chan et al, 1995(Chan et al, , 1997. In addition, no single papillomavirus type is known to infect more than one host species.…”