African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum

Abstract

Plasmodium reichenowi, a chimpanzee parasite, was until very recently the only known close relative of Plasmodium falciparum, the most virulent agent of human malaria. Recently, Plasmodium gaboni, another closely related chimpanzee parasite, was discovered, suggesting that the diversity of Plasmodium circulating in great apes in Africa might have been underestimated. It was also recently shown that P. reichenowi is a geographically widespread and genetically diverse chimpanzee parasite and that the world diversity of P. falciparum is fully included within the much broader genetic diversity of P. reichenowi. The evidence indicates that all extant populations of P. falciparum originated from P. reichenowi, likely by a single transfer from chimpanzees. In this work, we have studied the diversity of Plasmodium species infecting chimpanzees and gorillas in Central Africa (Cameroon and Gabon) from both wild-living and captive animals. The studies in wild apes used noninvasive sampling methods. We confirm the presence of P. reichenowi and P. gaboni in wild chimpanzees. Moreover, our results reveal the existence of an unexpected genetic diversity of Plasmodium lineages circulating in gorillas. We show that gorillas are naturally infected by two related lineages of parasites that have not been described previously, herein referred to as Plasmodium GorA and P. GorB, but also by P. falciparum, a species previously considered as strictly human specific. The continuously increasing contacts between humans and primate populations raise concerns about further reciprocal host transfers of these pathogens.cytochrome b gene | ecology | evolution | host specificity | infectious diseases P lasmodium falciparum is the agent of malignant malaria, one of the worst scourges of mankind, with 2 million infant deaths and ∼500 million clinical cases per year, 85% in sub-Saharan Africa. Plasmodium reichenowi, a chimpanzee parasite, was the only known closely related sister lineage (Fig. 1A), of which only one single exemplar was known (1, 2). It was assumed that the two parasites had evolved along with their hosts since the separation of the two lineages, ∼7 million years ago (the cospeciation hypothesis). The existence of only one P. reichenowi strain did not allow testing two alternative hypotheses: whether P. reichenowi was ancestral to P. falciparum or vice versa (1, 3). Recent genetic analysis of eight previously undescribed isolates of P. reichenowi from wild-born chimpanzees in Cameroon and Ivory Coast has shown that P. reichenowi is a geographically widespread and genetically diverse chimpanzee parasite and that P. falciparum is fully included within the much broader genetic diversity of P. reichenowi (4). Phylogenetic analysis indicates that all extant P. falciparum populations originated from P. reichenowi, likely by a single transfer from chimpanzees. Also recently, a unique closely related species, named Plasmodium gaboni, was discovered in two wild-born chimpanzees kept as pets in remote villages of Gabon (5), suggesting the po...

African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus

“…The chimpanzee samples proved to be extremely diversified. Two samples (CPZcam46 and CPZcam137) cluster with P. falciparum, suggesting that this parasite is present not only in gorillas, as already shown by Prugnolle et al (29) and as observed by us, and in bonobos (30), but also in chimpanzees. A third chimpanzee sample (CPZcam61) appears to be P. reichenowi, and two others (CPZcam80 and CPZcam155) associate with P. gaboni.…”

“…One gorilla sample (GGcam10) belongs within the P. falciparum cluster, thus confirming the presence of P. falciparum-related parasites in gorillas, as reported by Prugnolle et al (29). The second gorilla sample (GGcam13) appears to be closest to P. gaboni, although statistically not closer to gaboni than to the falciparum-reichenowi clade.…”

“…Five chimpanzees, CPZcam61 plus the four chimpanzees with mixed infection (CPZcam63, CPZcam72, CPZcam86, and CPZcam103), were infected with P. reichenowi, the parasite previously considered chimpanzee specific but recently shown to infect gorillas as well (29). Five chimpanzees are infected with P. gaboni, the recently identified chimpanzee parasite (26,29): CPZcam80, CPZcam155, and the doubly infected CPZcam72, CPZcam86, and CPZcam103.…”

“…Prugnolle et al (29) have analyzed partial Cytb sequences (704 nucleotides) from five chimpanzee and seven gorilla DNA samples, obtained from fecal samples from wild chimpanzees (n = 125) and gorillas (n = 84) from Cameroon, plus three blood samples from captive wild-born gorillas from Gabon. The chimpanzee isolates clustered with either P. reichenowi or P. gaboni, congruent with previous observations.…”

Lignes directrices pour de meilleures pratiques en matière de suivi de la santé et de contrôle des maladies des populations de grands singes

“…Murray et al 2013). Les agents pathogènes et les anticorps produits contre ces agents peuvent être décelés dans les échantillons de fèces Kaiser et al 2010 ;Köndgen et al 2010 ;Prugnolle et al 2010 ;Reed et al 2014). La salive trouvée sur un aliment partiellement consommé et abandonné peut fournir des informations sur des agents pathogènes spécifiques (Schaumburg et al 2013 ;Smiley Evans et al 2015).…”