Cross-species pathogen transmission and disease emergence in primates

Abstract

Many of the most virulent emerging infectious diseases in humans, e.g., AIDS and Ebola, are zoonotic, having shifted from wildlife populations. Critical questions for predicting disease emergence are: (1) what determines when and where a disease will first cross from one species to another, and (2) which factors facilitate emergence after a successful host shift. In wild primates, infectious diseases most often are shared between species that are closely related and inhabit the same geographic region. Therefore, humans may be most vulnerable to diseases from the great apes, which include chimpanzees and gorillas, because these species represent our closest relatives. Geographic overlap may provide the opportunity for cross-species transmission, but successful infection and establishment will be determined by the biology of both the host and pathogen. We extrapolate the evolutionary relationship between pathogen sharing and divergence time between primate species to generate "hotspot" maps, highlighting regions where the risk of disease transfer between wild primates and from wild primates to humans is greatest. We find that central Africa and Amazonia are hotspots for cross-species transmission events between wild primates, due to a high diversity of closely related primate species. Hotspots of host shifts to humans will be most likely in the forests of central and west Africa, where humans come into frequent contact with their wild primate relatives. These areas also are likely to sustain a novel epidemic due to their rapidly growing human populations, close proximity to apes, and population centers with high density and contact rates among individuals.

Figure 1

Three key stages of disease emergence: (1) opportunity, (2) infection and transmission, and (3) establishment. The biogeography of both hosts and pathogens will contribute to the opportunity for cross-species transmission. For natural populations, opportunity for new pathogens may be restricted to neighboring species; however, wildlife trade, invasive species, and domestic animals also may be a source of new pathogens. The ability for a pathogen to infect and be transmitted within the new host species is likely driven by ecological and evolutionary barriers, such as phylogenetic relatedness of the hosts and the evolutionary potential of the pathogen. Lastly, multiple demographic factors will affect the ultimate sustainability and establishment of a pathogen following a host shift, including population density, contact rates, and the rate of spread of the pathogen.

Figure 2

Frequency histogram of the phylogenetic risk of host shifts (PRHS: summation of the number of overlapping primate species, weighted by the relationship between divergence time and pathogen sharing, see main text for details). Phylogenetic risk varied from 0 to 2.96, with most species having intermediate to low risk (median = 0.42).

Figure 3

a Scatter plot of phylogenetic risk against the number of overlapping species for each primate host. Risk correlated positively with overlap; however, there was still large variation in risk among species with the same number of neighbors. Variation in phylogenetic risk is a product of both number of neighbors and phylogenetic relationships in the primate tree. b Scatter plot of the proportion of host-specific pathogens against phylogenetic risk; symbol size is proportional to the total number of recorded pathogens for each host species respectively. Hosts with high phylogenetic risk have significantly fewer host-specific pathogens, supporting our hypothesis that host shifts are more frequent among high-risk species.

Figure 4

a Hotspot map of the summed phylogenetic risk for host shifts across wild primates. Central Africa and west Amazonia represent regions of high geographical overlap among many closely related primate species. We predict host shifts among primates to be frequent in these localities. b Phylogenetic risk of pathogens host shifting to humans from wild primates. West central Africa is a hotspot of high risk to humans, due to the overlapping ranges of many of our closest relatives. c The intersection between high phylogenetic risk and an index of human population growth (increase in density from 1990–2000), revealing regions where we expect high rates of human contact with primate species that pose the greatest risk of cross-species pathogen transmission to humans. Open circles indicate human population centers (>25,000) that may facilitate disease emergence following host shift events.

Figure 5

Representation of the interaction between phylogeny and geography that may determine the frequency of host shifts within host communities. In the maps, warmer colors represent areas with many overlapping species ranges (geographically clumped distributions). In the phylogeny, red branches represent samples of closely related taxa (phylogenetically clumped). We predict the greatest frequency of host shifts will be observed among species which are both phylogenetically clumped (those with many close relatives) and geographically clumped (species with many overlapping neighbors) (top left). Species that are neither geographically clumped nor phylogenetically clumped are predicted to have the lowest risk (bottom right). We expect intermediate risk of host shifts for species that are phylogenetically clumped but geographically dispersed, or geographically clumped but phylogenetically dispersed.