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

Abstract

We investigated two mitochondrial genes (cytb and cox1), one plastid gene (tufA), and one nuclear gene (ldh) in blood samples from 12 chimpanzees and two gorillas from Cameroon and one lemur from Madagascar. One gorilla sample is related to Plasmodium falciparum, thus confirming the recently reported presence in gorillas of this parasite. The second gorilla sample is more similar to the recently defined Plasmodium gaboni than to the P. falciparum-Plasmodium reichenowi clade, but distinct from both. Two chimpanzee samples are P. falciparum. A third sample is P. reichenowi and two others are P. gaboni. The other chimpanzee samples are different from those in the ape clade: two are Plasmodium ovale, and one is Plasmodium malariae. That is, we have found three human Plasmodium parasites in chimpanzees. Four chimpanzee samples were mixed: one species was P. reichenowi; the other species was P. gaboni in three samples and P. ovale in the fourth sample. The lemur sample, provisionally named Plasmodium malagasi, is a sister lineage to the large cluster of primate parasites that does not include P. falciparum or ape parasites, suggesting that the falciparum + ape parasite cluster (Laverania clade) may have evolved from a parasite present in hosts not ancestral to the primates. If malignant malaria were eradicated from human populations, chimpanzees, in addition to gorillas, might serve as a reservoir for P. falciparum.T here is a revolution afoot concerning our understanding of human malaria. It was shown in 1994/1995 that the closest relative of Plasmodium falciparum, the agent of malignant malaria was Plasmodium reichenowi, a chimpanzee parasite, the only ape malaria parasite that had been molecularly characterized (1-4). The close phylogenetic relationship between P. falciparum and Plasmodium reichenowi, their distinctness from the three other known human malaria parasites (Plasmodium vivax, Plasmodium ovale, and Plasmodium malariae), as well as from other primate parasites, and their remoteness from bird or lizard parasites, was soon confirmed by other studies (5-7). It was assumed, as a working hypothesis, that P. falciparum and P. reichenowi had evolved from a common ancestor parasite, independently in their respective hosts, humans and chimpanzees, as these two lineages gradually diverged from one another over the last 5-7 million years-the cospeciation hypothesis. Two alternative hypotheseseither (i) a human origin (P. reichenowi evolved from an introduction of P. falciparum into chimpanzee hosts) or (ii) a chimpanzee origin (P. falciparum evolved from the introduction of P. reichenowi into the human lineage)-could not be tested against each other or against the cospeciation hypothesis, because only one P. reichenowi isolate was available, which had been isolated from a captive chimpanzee.It was soon demonstrated by Rich et al. (8), Rich and Ayala (9), and Ayala and Rich (10) that P. falciparum has very low levels of neutral genetic polymorphism, a result that was subsequently confirmed by other investigators (11...

Plasmodium falciparumis not as lonely as previously considered

“…[5][6][7][8][9]11 This was not a complete surprise for P. malariae and P. vivax, since morphologically similar species had been previously reported in chimpanzees and gorillas. 1 This discovery was more surprising for P. ovale and even more for P. falciparum, which were, for a long time, considered as strictly human specific.…”

“…[5][6][7][8][9][10][11] The use of molecular tools for species identification, combined with the use of non-invasive methods 9,11 to explore the diversity of Plasmodium species present in great apes, have revealed five new phylogenetic species in less than a year. Figure 2 displays this diversity and the phylogenetic relationships between species.…”

“…1 This discovery was more surprising for P. ovale and even more for P. falciparum, which were, for a long time, considered as strictly human specific. For chimpanzees and bonobos, P. falciparum strains were discovered only in captive animals 5,8 while in gorillas, they were discovered in both captive and wild animals. 9,11 This latter observation, together with the fact that the diversity of gorilla P. falciparum is higher than the one observed in the human ones, has led Liu and colleagues 9 to propose that human P. falciparum may have originated from a transfer from gorillas.…”

RH5–Basigin interaction plays a major role in the host tropism of Plasmodium falciparum

“…T he most deadly of the malaria parasites, Plasmodium falciparum, is highly divergent from the other species of Plasmodium known to infect humans (1)(2)(3), with its closest relatives comprising a group of chimpanzee and gorilla parasites from the subgenus Laverania (3)(4)(5)(6)(7). Despite the origin of P. falciparum as a zoonosis, and the continuing coexistence of humans and apes in West and Central Africa, extensive field studies have failed to detect P. falciparum in wild-living chimpanzees and gorillas (5).…”

“…Despite the origin of P. falciparum as a zoonosis, and the continuing coexistence of humans and apes in West and Central Africa, extensive field studies have failed to detect P. falciparum in wild-living chimpanzees and gorillas (5). Although there are reports of P. falciparum infecting chimpanzees either in certain captive settings (2) or following splenectomy and deliberate transfer of P. falciparum-infected human blood (8)(9)(10), the resulting infections have low parasitemia and are not known to result in malignant tertian malaria, suggesting a host-specific barrier for replete infection. The existence of host-specific barriers within the Laverania subgenus is supported further by the strict host specificity exhibited by ape Laverania parasites in the wild: Plasmodium reichenowi, Plasmodium billcollinsi, and Plasmodium gaboni infect only chimpanzees, and Plasmodium praefalciparum, Plasmodium blacklocki, and Plasmodium adleri are restricted to gorillas (3)(4)(5)(6).…”