Abstract

While the circumstances surrounding the origin and spread of HIV are becoming clearer, the particulars of the origin of simian immunodeficiency virus (SIV) are still unknown. Specifically, the age of SIV, whether it is an ancient or recent infection, has not been resolved. Although many instances of cross-species transmission of SIV have been documented, the similarity between the African green monkey (AGM) and SIVagm phylogenies has long been held as suggestive of ancient codivergence between SIVs and their primate hosts. Here, we present well-resolved phylogenies based on full-length AGM mitochondrial genomes and seven previously published SIVagm genomes; these allowed us to perform the first rigorous phylogenetic test to our knowledge of the hypothesis that SIVagm codiverged with the AGMs. Using the Shimodaira–Hasegawa test, we show that the AGM mitochondrial genomes and SIVagm did not evolve along the same topology. Furthermore, we demonstrate that the SIVagm topology can be explained by a pattern of west-to-east transmission of the virus across existing AGM geographic ranges. Using a relaxed molecular clock, we also provide a date for the most recent common ancestor of the AGMs at approximately 3 million years ago. This study substantially weakens the theory of ancient SIV infection followed by codivergence with its primate hosts.

Highlights

  • More than 30 nonhuman primate species in sub-Saharan Africa are naturally infected with simian immunodeficiency virus (SIV) [1]; the evolutionary forces shaping simian immunodeficiency viruses (SIVs) diversity remain unclear

  • HIV is understood to have originated from simian immunodeficiency viruses (SIVs) infecting nonhuman African primates, but the length of time the virus has been present in these apes and monkeys is not known

  • Our results suggest that SIV did not infect these monkeys until after speciation and subsequently swept across their geographical ranges

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Summary

Introduction

More than 30 nonhuman primate species in sub-Saharan Africa are naturally infected with simian immunodeficiency virus (SIV) [1]; the evolutionary forces shaping SIV diversity remain unclear. One of the most important unanswered questions regarding SIV evolution is whether it is an ancient infection that has been codiverging with its primate hosts for millions of years, or whether the virus may have arrived more recently and swept across already established primate lineages. Recent genomic analysis suggests that endogenous lentiviruses may have been infecting mammals for the last 7 million years [6]. The AGM genus, Chlorocebus, consists of four species (C. aethiops, C. pygerythrus, C. sabaeus, and C. tantalus), each with its own corresponding SIV lineage (SIVgri, SIVver, SIVsab, and SIVtan) [8,9,10,11]. 12s analysis provides very low statistical support for the branching order among the AGM taxa, and these studies were unable to resolve whether C. pygerythrus from Tanzania and South Africa are monophyletic or paraphyletic

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