Impact of simian immunodeficiency virus infection on chimpanzee population dynamics

Abstract

Like human immunodeficiency virus type 1 (HIV-1), simian immunodeficiency virus of chimpanzees (SIVcpz) can cause CD4+ T cell loss and premature death. Here, we used molecular surveillance tools and mathematical modeling to estimate the impact of SIVcpz infection on chimpanzee population dynamics. Habituated (Mitumba and Kasekela) and non-habituated (Kalande) chimpanzees were studied in Gombe National Park, Tanzania. Ape population sizes were determined from demographic records (Mitumba and Kasekela) or individual sightings and genotyping (Kalande), while SIVcpz prevalence rates were monitored using non-invasive methods. Between 2002-2009, the Mitumba and Kasekela communities experienced mean annual growth rates of 1.9% and 2.4%, respectively, while Kalande chimpanzees suffered a significant decline, with a mean growth rate of -6.5% to -7.4%, depending on population estimates. A rapid decline in Kalande was first noted in the 1990s and originally attributed to poaching and reduced food sources. However, between 2002-2009, we found a mean SIVcpz prevalence in Kalande of 46.1%, which was almost four times higher than the prevalence in Mitumba (12.7%) and Kasekela (12.1%). To explore whether SIVcpz contributed to the Kalande decline, we used empirically determined SIVcpz transmission probabilities as well as chimpanzee mortality, mating and migration data to model the effect of viral pathogenicity on chimpanzee population growth. Deterministic calculations indicated that a prevalence of greater than 3.4% would result in negative growth and eventual population extinction, even using conservative mortality estimates. However, stochastic models revealed that in representative populations, SIVcpz, and not its host species, frequently went extinct. High SIVcpz transmission probability and excess mortality reduced population persistence, while intercommunity migration often rescued infected communities, even when immigrating females had a chance of being SIVcpz infected. Together, these results suggest that the decline of the Kalande community was caused, at least in part, by high levels of SIVcpz infection. However, population extinction is not an inevitable consequence of SIVcpz infection, but depends on additional variables, such as migration, that promote survival. These findings are consistent with the uneven distribution of SIVcpz throughout central Africa and explain how chimpanzees in Gombe and elsewhere can be at equipoise with this pathogen.

Figure 1. Map of Gombe National Park, Tanzania.

The 2007 ranges of the habituated Kasekela (brown) and Mitumba (blue) communities are shown in relation to minimal (solid lines) and likely (broken lines) ranges of the unhabituated Kalande (orange) community. The inset depicts the location of Gombe within Tanzania. Yellow circles indicate observed locations (2002–2009) of Kalande chimpanzees (within the park) and their nests (outside the park). Vegetation cover is colored based on classification from remote sensing as beach/grassland (yellow), open woodland (light green), thicket woodland (medium green), or evergreen forest/vine tangle (dark green).

Figure 2. SIVcpz prevalence, population sizes, and median population growth rates for the Gombe communities.

Data are color coded according to community (Mitumba: blue; Kasekela: brown; Kalande: orange). (A) Proportion of individuals infected with SIVcpz in the three Gombe communities, as determined by biannual sampling between 2002 and 2009 (based on Figure S1). (B) Population size of the three Gombe communities (including minimum and maximum estimates for Kalande) between 1998 and 2009. Dotted and solid lines connect data points before and after the start of regular SIVcpz sampling in 2002, respectively. (C, D) Mean biannual prevalence (C) and annual growth rates (D) in each Gombe community from 2002–2009 (error bars indicate standard deviations).

Figure 3. Kinship of Kalande chimpanzees.

Males are shown as squares and females as circles. Individuals not known to have resided in Kalande are indicated by dashed lines. SIVcpz infected individuals are highlighted in red. Current residents of Kalande are identified by bold thick-lined shapes. Vertical lines connect parents and offspring, while horizontal lines connect siblings. Fathers are linked to offspring by dashed lines. Blue lines indicate that the relationship is significant at the P<0.001 level in KINSHIP. The diagonal connection between Ch-024 and Ch-092 indicates a likely sibling or other close matrilineal relationship.

Figure 4. Phylogeny of SIVcpz in Gombe.

A phylogenetic tree was constructed from available pol sequences, using SIVcpzPts strains from the Democratic Republic of Congo (ANT and BF1167) as outgroups. Viruses (and their chimpanzee hosts) are color coded according to their most recent community (Mitumba, blue; Kasekela, brown; Kalande orange), while branch colors indicate the likely origin of these infections (e.g., Ch-099 resided in Kasekela from 2004 to 2006, but acquired TAN6 in Kalande). Striped lines indicate uncertain origin (genetic and demographic data suggest that Ch-033 and Ch-089 acquired their infections in Kalande and Kasekela, respectively; the location where Ch-022 acquired SIVcpz is unknown). The phylogenetic position of TAN16 is approximated (arrow) based on the position of its env-nef sequences (see Figure S2B in reference [2]). The tree was inferred by Bayesian methods ; numbers on nodes indicate posterior probabilities (only values above 0.95 are shown). The scale bar represents 0.1 substitutions per site.

Figure 5. Abundance of food plants in Gombe.

Data are color coded according to the range of the respective community (Mitumba: blue; Kasekela: brown; Kalande minimal range: vertical orange hatching; Kalande likely range: solid orange). (A) Total basal area of food trees (m²) and total number of stems of smaller food plants (vines and shrubs, shown in thousands of stems). (B) Per capita abundance of food plants. Population sizes are from 2007, using the median estimate for Kalande, and food plant abundance data are from 2007–2009. Range data for Kasekela and Mitumba communities are from 2007. Because available range data are more limited for Kalande, we used all available information from 2002–2009.

Figure 6. Predicted critical prevalence of SIVcpz (f^*) for different levels of the mortality multiplier (ρ).

Three different lines are given for different levels of the fertility multiplier (α). The most recent empirical estimates for these parameters are ρ = 10–16 and α = 0.5.

Figure 7. Stochastic simulations.

The number of infectious females, the number of infectious males, the SIVcpz prevalence, and the number of susceptible individuals (females in green, males in brown) are shown (y-axis) in relation to time in years (x-axis). (A) Representative run illustrating population extinction. (B) Representative run illustrating SIVcpz extinction.