A plethora of Plasmodium species in wild apes: a source of human infection?

Abstract

Recent studies of captive and wild-living apes in Africa have uncovered evidence of numerous new Plasmodium species, one of which was identified as the immediate precursor of human Plasmodium falciparum. These findings raise the question whether wild apes could be a recurrent source of Plasmodium infections in humans. This question is not new, but was the subject of intense investigation by researchers in the first half of the last century. Re-examination of their work in the context of recent molecular findings provides a new framework to understand the diversity of Plasmodium species and to assess the risk of future cross-species transmissions to humans in the context of proposed malaria eradication programs.

Figure 1

Geographic distribution, species association and prevalence of ape Plasmodium infections in sub-Saharan Africa. Field sites where wild-living chimpanzees and bonobos (a), or gorillas (b) were sampled are shown. Sites where ape Plasmodium infections were detected are highlighted in yellow, with the estimated prevalence indicated . The upper panel depicts the ranges of the four subspecies of the common chimpanzee (Pan troglodytes verus, gray; P. t. ellioti, magenta; P. t. troglodytes, red; and P. t. schweinfurthii, blue) and of the bonobo (P. paniscus, orange). The lower panel depicts the ranges of western (Gorilla gorilla, green) and eastern (G. beringei, brown) gorillas (map courtesy of Lilian Pintea, The Jane Goodall Institute, Arlington, Virginia, USA.).

Figure 2

Phylogeny of ape-derived Plasmodium mitochondrial sequences: identifying six clades within the Laverania subgenus. A summary representation of an analysis of nearly 700 SGA-derived ape Plasmodium cytb sequences is shown (modified from Supplementary Figure 3 in [25]). Clades are summarized as triangles; the height of each triangle reflects the number of sequences, whereas the depth denotes the maximum divergence within each clade. Green and magenta colors highlight Laverania parasites from gorillas (G1–G3) and chimpanzees (C1–C3), respectively (non-Laverania parasites are shown in yellow). Each clade reflects a distinct species; pre-existing or proposed names for these species are shown on the right. The black triangle indicates human P. falciparum sequences, which form a monophyletic clade within the G1 radiation of gorilla parasites.

Figure 3

Proximity of Plasmodium-infected wild-living apes to human habitation. The location of chimpanzee fecal samples collected near a village (black triangle) in southeastern Cameroon (inset) is shown. Plasmodium-positive and -negative samples are depicted by red and yellow triangles, respectively. Samples are numbered with capital letters indicating the field site, with their location determined using global positioning system (GPS) coordinates. Plasmodium-positive samples were found within 315 m of human habitation and in close proximity to a nearby road (brown line). The map was generated using Google Maps Pro (the scale bar represents 1 km); white areas indicate cloud cover.

Figure I

Non-invasive testing of ape Plasmodium infections. An ape fecal sample is collected at a remote forest site by an experienced tracker and preserved for shipment and storage in RNAlater (Ambion).