Why Are Nigeria-Cameroon Chimpanzees (Pan troglodytes ellioti) Free of SIVcpz Infection?

Abstract

Simian immunodeficiency virus (SIV) naturally infects two subspecies of chimpanzee: Pan troglodytes troglodytes from Central Africa (SIVcpzPtt) and P. t. schweinfurtii from East Africa (SIVcpzPts), but is absent in P. t. verus from West Africa and appears to be absent in P. t. ellioti inhabiting Nigeria and western Cameroon. One explanation for this pattern is that P. t. troglodytes and P. t schweinfurthii may have acquired SIVcpz after their divergence from P. t. verus and P. t. ellioti. However, all of the subspecies, except P. t. verus, still occasionally exchange migrants making the absence of SIVcpz in P. t. ellioti puzzling. Sampling of P. t. ellioti has been minimal to date, particularly along the banks of the Sanaga River, where its range abuts that of P. t. troglodytes. This study had three objectives. First, we extended the sampling of SIVcpz across the range of chimpanzees north of the Sanaga River to address whether under-sampling might account for the absence of evidence for SIVcpz infection in P. t. ellioti. Second, we investigated how environmental variation is associated with the spread and prevalence of SIVcpz in the two chimpanzee subspecies inhabiting Cameroon since environmental variation has been shown to contribute to their divergence from one another. Finally, we compared the prevalence and distribution of SIVcpz with that of Simian Foamy Virus (SFV) to examine the role of ecology and behavior in shaping the distribution of diseases in wild host populations. The dataset includes previously published results on SIVcpz infection and SFVcpz as well as newly collected data, and represents over 1000 chimpanzee fecal samples from 41 locations across Cameroon. Results revealed that none of the 181 P. t. ellioti fecal samples collected across the range of P. t. ellioti tested positive for SIVcpz. In addition, species distribution models suggest that environmental variation contributes to differences in the distribution and prevalence of SIVcpz and SFVcpz. The ecological niches of these two viruses are largely non-overlapping, although stronger statistical support for this conclusion will require more sampling. Overall this study demonstrates that SIVcpz infection is absent or very rare in P. t. ellioti, despite multiple opportunities for transmission. The reasons for its absence remain unclear, but might be explained by one or more factors, including environmental variation, viral competition, and/or local adaptation-all of which should be explored in greater detail through continued surveillance of this region.

Fig 1. (A) Phylogeny of SIVs and HIVs infecting ape species. (B) Distribution of the genus Pan and SIVcpz viruses.

The map background layer is “percent tree cover” from the MODIS satellite [81].

Fig 2. Chimpanzees sample locations.

The locations are plotted against the distributions of P. t. ellioti (purple) and P. t. troglodytes (orange). SIVcpz positive locations are shown in black and SIVcpz negative locations are shown in white. The map background layer is “percent tree cover” from the MODIS satellite [81]. Rivers are from the HydroSHEDS hydrography layer [82].

Fig 3. Simulation results estimating ß, the likelihood of erroneously concluding the virus is absent, for a given average prevalence of SIVcpz.

Since a single SIV+ case would refute the hypothesis of zero prevalence, ß is equal to the proportion of times zero SIV+ cases are returned when in fact the virus is present. For the uniform distribution (plotted in blue), each data point represents -log₁₀ of the proportion of 90,000 simulations returning zero SIVcpz positive cases, assuming each sample site has the same underlying prevalence. For simulations of the Poisson distribution (plotted in red), prevalence is equal to the λ parameter. For each run, sample site prevalence were randomly assigned from sampling the Poisson distribution with a particular λ. A total of 5,000 independent Poisson samples were taken, and the proportion of times zero SIVcpz-positive cases was estimated from 18 binomial sampling runs. Thus, each data point represents the -log₁₀ of the proportion of 90,000 simulations returning zero SIVcpz positive cases.

Fig 4. SIVcpz predictions of occurrence and prevalence across Cameroon.

(A) Temperature Seasonality, (B) SIVcpz occurrence calculated using Maxent [41], (C) SIVcpz prevalence calculated using randomForest [48]. SIVcpz positive sites are shown in red and SIVcpz negative sites are shown in black in A and B. Circles in C correspond to prevalence according to the color ramp to the left.

Fig 5. Predicted prevalence of SIVcpz and SFVcpz across Cameroon.

Areas with predicted prevalence of >10% include red where only SIVcpz is present; medium blue where only SFVcpz is present; and purple where SIVcpz and SFVcpz overlap. Light blue denotes areas where SIVcpz and SFVcpz may overlap with one another but at a prevalence of <10%.

Fig 6. Regression analysis of SFVcpz prevalence on SIVcpz prevalence in Pan troglodytes ellioti (3 populations) and Pan troglodytes troglodytes (9 populations) from Cameroon.

p value = 0.0335 (one-tailed test).