Abstract

In the 20th century, thirteen distinct human immunodeficiency viruses emerged following independent cross-species transmission events involving simian immunodeficiency viruses (SIV) from African primates. In the late 1900s, pathogenic SIV strains also emerged in the United Sates among captive Asian macaque species following their unintentional infection with SIV from African sooty mangabeys (SIVsmm). Since their discovery in the 1980s, SIVs from rhesus macaques (SIVmac) and pig-tailed macaques (SIVmne) have become invaluable models for studying HIV pathogenesis, vaccine design and the emergence of viruses. SIV isolates from captive crab-eating macaques (SIVmfa) were initially described but lost prior to any detailed molecular and genetic characterization. In order to infer the origins of the lost SIVmfa lineage, we located archived material and colony records, recovered its genomic sequence by PCR, and assessed its phylogenetic relationship to other SIV strains. We conclude that SIVmfa is the product of two cross-species transmission events. The first was the established transmission of SIVsmm to rhesus macaques, which occurred at the California National Primate Research Center in the late 1960s and the virus later emerged as SIVmac. In a second event, SIVmac was transmitted to crab-eating macaques, likely at the Laboratory for Experimental Medicine and Surgery in Primates in the early 1970s, and it was later spread to the New England Primate Research Center colony in 1973 and eventually isolated in 1986. Our analysis suggests that SIVmac had already emerged by the early 1970s and had begun to diverge into distinct lineages. Furthermore, our findings suggest that pathogenic SIV strains may have been more widely distributed than previously appreciated, raising the possibility that additional isolates may await discovery.

Highlights

  • During the 20th century, simian immunodeficiency viruses (SIV) from African primates were transmitted to humans on no fewer than 13 occasions [1]

  • To determine SIV prevalence among the macaque species housed at New England Primate Research Center (NEPRC), Daniel et al screened sera from animals for reactivity with SIVs from rhesus macaques (SIVmac) antigens [20]

  • We propose that rhesus macaques were initially infected with SIVsmm and that this virus adapted to the rhesus macaque host, which included adaptions to overcome restriction factor variants that are uniquely found at high allelic frequencies in this species, and emerged as SIVmac

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Summary

Introduction

During the 20th century, simian immunodeficiency viruses (SIV) from African primates were transmitted to humans on no fewer than 13 occasions [1]. One event, involving an SIV from chimpanzees, initiated the global human immunodeficiency virus type-1 (HIV-1) pandemic (group M) in the early 1900s [2,3,4]. In the mid 1960s, SIV strains from captive sooty mangabeys (SIVsmm) were unintentionally transmitted to macaques housed in United States primate centers [11,12,13,14,15]. SIVmac and SIVmne and their respective hosts have since become valued non-human models for HIV pathogenesis and vaccinology. Because these viruses emerged in captive animals from which historical samples and veterinary records were archived, the study of these viruses has been useful for elucidating the process of cross-species transmission, viral adaptation, and the emergence of pathogenic immunodeficiency viruses [21]

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