Abstract

Cross-species transmission (CST) has led to many devastating epidemics, but is still a poorly understood phenomenon. HIV-1 and HIV-2 (human immunodeficiency virus 1 and 2), which have collectively caused over 35 million deaths, are the result of multiple CSTs from chimpanzees, gorillas, and sooty mangabeys. While the immediate history of HIV is known, there are over 45 lentiviruses that infect specific species of primates, and patterns of host switching are not well characterized. We thus took a phylogenetic approach to better understand the natural history of SIV recombination and CST. We modeled host species as a discrete character trait on the viral phylogeny and inferred historical host switches and the pairwise transmission rates between each pair of 24 primate hosts. We identify 14 novel, well-supported, ancient cross-species transmission events. We also find that lentiviral lineages vary widely in their ability to infect new host species: SIVcol (from colobus monkeys) is evolutionarily isolated, while SIVagms (from African green monkeys) frequently move between host subspecies. We also examine the origins of SIVcpz (the predecessor of HIV-1) in greater detail than previous studies, and find that there are still large portions of the genome with unknown origins. Observed patterns of CST are likely driven by a combination of ecological circumstance and innate immune factors.

Highlights

  • As demonstrated by the recent epidemics of EBOV and MERS, and by the global HIV pandemic, viral cross-species transmissions (CST) can be devastating [1,2]

  • In order to reconstruct the lentiviral phylogeny, we first had to address the issue of recombination, which is frequent among lentiviruses [16]

  • Evidence of recombination between viral lineages endemic to different hosts is evidence that at one point in time, viruses from those two lineages were in the same animal

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Summary

Introduction

As demonstrated by the recent epidemics of EBOV and MERS, and by the global HIV pandemic, viral cross-species transmissions (CST) can be devastating [1,2]. HIV-2 arose from multiple cross-species transmissions of SIVsmm (simian immunodeficiency virus, sooty mangabey) from sooty mangabeys to humans [6,7,8]. HIV-1 is the result of four independent cross-species transmissions from chimpanzees and gorillas. SIVcpz was transmitted directly from chimpanzees to humans twice; one of these transmissions generated HIV-1 group M, which is the primary cause of the human pandemic [9]. SIVcpz was transmitted once to gorillas, generating SIVgor [10], which was in turn transmitted twice to humans [11]

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