Plasmodium falciparum is the most prevalent and lethal of the malaria parasites infecting humans, yet the origin and evolutionary history of this important pathogen remain controversial. Here we develop a single-genome amplification strategy to identify and characterize Plasmodium spp. DNA sequences in faecal samples from wild-living apes. Among nearly 3,000 specimens collected from field sites throughout central Africa, we found Plasmodium infection in chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla), but not in eastern gorillas (Gorilla beringei) or bonobos (Pan paniscus). Ape plasmodial infections were highly prevalent, widely distributed and almost always made up of mixed parasite species. Analysis of more than 1,100 mitochondrial, apicoplast and nuclear gene sequences from chimpanzees and gorillas revealed that 99% grouped within one of six host-specific lineages representing distinct Plasmodium species within the subgenus Laverania. One of these from western gorillas comprised parasites that were nearly identical to P. falciparum. In phylogenetic analyses of full-length mitochondrial sequences, human P. falciparum formed a monophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla origin and not of chimpanzee, bonobo or ancient human origin.
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SGA-derived Plasmodium nucleotide sequences have been deposited in GenBank under accession numbers HM234976–HM235117 and HM237301 (cytb), HM235118–HM235143 (ldh), HM235144–HM235170 (clpC), HM235171–HM235268 (mtDNA-3.3 kb) and HM235269–HM235404 (mtDNA-3.4 kb) (also see Supplementary Table 6).
We thank C. Neel, S. Loul, A. Mebanga, B. Yangda and F. Liegeois for field work in Cameroon; the Cameroonian Ministries of Health, Forestry and Wildlife, and Research for permission to collect samples in Cameroon; the Water and Forest Ministry for permission to collect samples in the Central African Republic; the Ministries of Science and Technology and Forest Economy for permission to collect samples in the Republic of the Congo; the Ministry of Scientific Research and Technology and the Department of Ecology and Management of Plant and Animal Resources of the University of Kisangani for permission to collect samples in the Democratic Republic of the Congo; M. Ndunda, S. Coxe, A. Lokasola, A. Todd and the staff of the World Wildlife Fund in the Central African Republic for logistical support; R. Carter for helpful discussions; M. Salazar, Y. Chen and B. Cochran for technical assistance; and J. White for artwork and manuscript preparation. This work was supported by grants from the National Institutes of Health (R01 AI50529, R01 AI58715, U19 AI 067854, R03 AI074778, T32 GM008111, T32 AI007245, P30 AI 27767), the Bill & Melinda Gates Foundation (37874), the National Science Foundation (0755823), the Agence Nationale de Recherche sur le Sida (12152/12182), the Great Ape Conservation Fund of the US Fish and Wildlife Service, the Arthur L. Greene Fund, the Wallace Global Fund, the Bristol Myers Freedom to Discover Program and the Wellcome Trust. R.S.R. was supported by a Howard Hughes Medical Institute Med-into-Grad Fellowship.
This file contains Supplementary Figures 1-8 with legends and Supplementary Tables 1-7.