African monkeys are infected by Plasmodium falciparum nonhuman primate-specific strains

Abstract

Recent molecular exploration of the Plasmodium species circulating in great apes in Africa has revealed the existence of a large and previously unknown diversity of Plasmodium. For instance, gorillas were found to be infected by parasites closely related to Plasmodium falciparum, suggesting that the human malignant malaria agent may have arisen after a transfer from gorillas. Although this scenario is likely in light of the data collected in great apes, it remained to be ascertained whether P. falciparum-related parasites may infect other nonhuman primates in Africa. Using molecular tools, we here explore the diversity of Plasmodium species infecting monkeys in Central Africa. In addition to previously described Hepatocystis and Plasmodium species (Plasmodium gonderi and Plasmodium sp DAJ-2004), we have found one African monkey to be infected by a P. falciparum-related parasite. Examination of the nuclear and mitochondrial genomes of this parasite reveals that it is specific of nonhuman primates, indicating that P. falciparum-related pathogens can naturally circulate in some monkey populations in Africa. We also show that at least two distinct genetic entities of P. falciparum infect nonhuman primates and humans, respectively. Our discoveries bring into question the proposed gorilla origin of human P. falciparum.human malaria | laverania clade | parasite host transfer | cytochrome b | biological evolution U ntil very recently, only one species (Plasmodium reichenowi) was known to be a phylogenetic sister lineage of Plasmodium falciparum, the agent of malignant human malaria. These two species were the only known representatives of the subgenus Laverania (1). In 2009 and 2010, several studies have revealed the existence of a number of distinct phylogenetic species belonging to this subgenus and infecting chimpanzees, bonobos, and gorillas in Africa (2-6), drastically modifying our understanding of the evolution of the Laverania lineage, and P. falciparum in particular (7).Liu et al. (4) have proposed that the human strains of P. falciparum arose after a single gorilla-to-human transmission (4, 7). This scenario is based on the discovery of P. falciparum-related strains naturally circulating in lowland gorillas (2, 4, 6) that display greater genetic diversity than human strains (4). In contrast, no P. falciparum strains were found in wild chimpanzees or bonobos despite similar sampling efforts (4). Strains of P. falciparum had been found only in chimpanzees and bonobos living either in captivity or sanctuaries, with the possibility of a crossspecies infection from humans to them (2, 3). It, however, remains possible that P. falciparum-related strains circulate in wild chimpanzees and bonobos at a lower prevalence than in gorillas (8) and/or in geographic areas not yet explored. Given the propensity of Plasmodium parasites to switch hosts (e.g., the transfer of P. knowlesi from macaques to humans (9) and P. vivax and P. malariae between humans and New World monkeys; ref. 10), one cannot exclude that P. falciparum-r...

Reply to Sharp et al.: Host species sampling bias and Plasmodium falciparum origin paradigm shifts

“…The results of Prugnolle et al (2) did not disprove that human Plasmodium falciparum has a gorilla origin but brought that conclusion into question, which is what we asserted (and yes, a single isolate in a single monkey species is enough to question it).…”

Ape malaria transmission and potential for ape-to-human transfers in Africa

“…DAJ. P. gonderi is one of the only two Plasmodium species infecting monkeys in west and central Africa (38,39). Its natural known hosts are the primates of the genera Cercocebus, Mandrillus, and Cercopithecus, well represented in both study sites (La Lopé and La Lékédi).…”

Wild African great apes as natural hosts of malaria parasites: current knowledge and research perspectives

“…Cross-species transmission between AGAs and other NHPs sharing their habitat is probably exceptional. So far, the only published finding showing such potential is that of P. praefalciparum detected in a single captive greater spot-nosed monkey, Cercopithecus nictitans (Prugnolle et al, 2011). Yet, during a subsequent study which tested blood from a significant number of wild spot-nosed monkeys (N = 292), only Hepatocystis spp.…”