Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Taï Forest, Côte d'Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2

Abstract

Simian immunodeficiency virus of sooty mangabeys (SIVsmm) is recognized as the progenitor of human immunodeficiency virus type 2 (HIV-2) and has been transmitted to humans on multiple occasions, yet the epidemiology and genetic diversity of SIVsmm infection in wild-living populations remain largely unknown. Here, we report the first molecular epidemiological survey of SIVsmm in a community of approximately 120 free-ranging sooty mangabeys in the Taï Forest, Côte d'Ivoire. Fecal samples (n = 39) were collected from 35 habituated animals (27 females and 8 males) and tested for SIVsmm virion RNA (vRNA). Viral gag (800 bp) and/or env (490 bp) sequences were amplified from 11 different individuals (eight females and three males). Based on the sensitivity of fecal vRNA detection and the numbers of samples analyzed, the prevalence of SIVsmm infection was estimated to be 59% (95% confidence interval, 0.35 to 0.88). Behavioral data collected from this community indicated that SIVsmm infection occurred preferentially in high-ranking females. Phylogenetic analysis of gag and env sequences revealed an extraordinary degree of genetic diversity, including evidence for frequent recombination events in both the recent and distant past. Some sooty mangabeys harbored near-identical viruses (<2% interstrain distance), indicating epidemiologically linked infections. These transmissions were identified by microsatellite analyses to involve both related (mother/daughter) and unrelated individuals, thus providing evidence for vertical and horizontal transmission in the wild. Finally, evolutionary tree analyses revealed significant clustering of the Taï SIVsmm strains with five of the eight recognized groups of HIV-2, including the epidemic groups A and B, thus pointing to a likely geographic origin of these human infections in the eastern part of the sooty mangabey range.

FIG. 1.

Historical range of the sooty mangabey (C. atys atys) from south of the Casamance River in Senegal to the Nzo/Sassandra River systems in Côte d'Ivoire. The geographic origin of previously reported SIVsmm strains from Sierra Leone, Liberia, and western Côte d'Ivoire is shown in relation to the location of the Taï field site. Red dots indicate known capture locations of SIVsmm-infected sooty mangabeys, while yellow dots indicate sites where infected sooty mangabeys were identified in captivity (CI2 and CI8 were captured in western Côte d'Ivoire, close to the Liberian border). Green areas depict remaining coastal forest areas (http://www.globalforestwatch.org). The range of the white-crowned mangabey (C. atys lunulatus) extends from east of the Sassandra River to the Volta River in Ghana (26, 38). Country boundaries and major cities are indicated.

FIG. 2.

Male (left) and subadult female (right) sooty mangabeys from the Taï Forest community.

FIG. 3.

Phylogenetic relationships of SIVsmm from the Taï Forest to previously characterized SIVsmm and HIV-2 strains in gag and env regions. SIVsmm from Côte d'Ivoire is highlighted in red (CI2 and CI8 from captive sooty mangabeys are shown in pink); the eight groups of HIV-2 are shown in blue. The trees were inferred by the Bayesian method; numbers on branches are percent posterior probabilities (values of 95% and above are shown). The scale bars indicate 0.1 substitutions per site.

FIG. 4.

Phylogenetic relationships of SIVsmm from the Taï Forest to previously characterized SIVsmm and HIV-2 strains in gag and env regions, with probable recombinant sequences excluded (see text for details). SIVsmm from Côte d'Ivoire is highlighted in red, while the eight groups of HIV-2 are shown in blue. The green arrows indicate where the excluded Sierra Leonean SIVsmm sequences would join (in the gag tree, SIVsmm strains SL92a, SL92e, SL92f, SL93-134, and SL93-135 join on the Taï33/Taï22 branch, whereas the other excluded strains join on the F098 branch; in the env tree, all excluded sequences join the Sierra Leonean SIVsmm cluster). The trees were inferred as described in the legend of Fig. 3.

FIG. 5.

Female sooty mangabey dominance rank and SIVsmm infection. SIVsmm vRNA-positive and -negative individuals are shown, with their relative dominance rank indicated by filled circles (also see Table 2).