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Article Dans Une Revue Proceedings of the National Academy of Sciences of the United States of America Année : 2016

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

Céline Arnathau
Eric Willaume
  • Fonction : Auteur

Résumé

Recent studies have highlighted the large diversity of malaria parasites infecting African great apes (subgenus Laverania) and their strong host specificity. Although the existence of genetic incompatibilities preventing the cross-species transfer may explain host specificity, the existence of vectors with a high preference for a determined host represents another possibility. To test this hypothesis , we undertook a 15-mo-long longitudinal entomological survey in two forest regions of Gabon, where wild apes live, at different heights under the canopy. More than 2,400 anopheline mosquitoes belonging to 18 species were collected. Among them, only three species of Anopheles were found infected with ape Plasmodium: Anopheles vinckei, Anopheles moucheti, and Anopheles marshallii. Their role in transmission was confirmed by the detection of the parasites in their salivary glands. Among these species, An. vinckei showed significantly the highest prevalence of infection and was shown to be able to transmit parasites of both chimpanzees and gorillas. Transmission was also shown to be conditioned by seasonal factors and by the heights of capture under the canopy. Moreover, human landing catches of sylvan Anopheles demonstrated the propensity of these three vector species to feed on humans when available. Our results suggest therefore that the strong host specificity observed in the Laveranias is not linked to a specific association between the vertebrate host and the vector species and highlight the potential role of these vectors as bridge between apes and humans. Plasmodium | Laverania | Anopheles | ape-to-human infection | African rainforest R ecent studies on great apes in Africa have revealed the existence of a large diversity of Plasmodium parasites infecting chimpanzees and gorillas, some being related to the most deadly human parasite Plasmodium falciparum (subgenus Laverania), others to the human parasites Plasmodium malariae, Plasmodium ovale, or Plasmodium vivax (subgenus Plasmodium) (1-4). Within the subgenus Laverania, eight species are currently recognized. Among them, four species (Plasmodium reichenowi, Plasmodium gaboni, Plasmodium billcollinsi, and Plasmodium billbrayi) were observed only in chimpanzees and three (Plas-modium praefalciparum, Plasmodium adleri, and Plasmodium blacklocki) only in gorillas (2, 3, 5). In this subgenus, only P. falciparum infects humans. In natura, although these different host species cooccur in the same habitat where their ranges overlap, no transfer of Laverania parasites was ever documented between humans and apes or between gorillas and chimpanzees despite large sampling efforts (2, 3, 6). Similarly, ancient reciprocal transplant experiments of Laverania parasites between humans and apes (mostly chimpanzees) failed to produce infections (5). On the contrary , for parasites of the subgenus Plasmodium, like P. vivax or P. malariae, transfers were documented in natural populations (2, 4, 7) or during experimental infections (5). All this suggests therefore a strong host specificity of the Laverania parasites. The origin of this host specificity in the Laverania could result from an incompatibility at the parasite/vertebrate host interface, at the vector/host interface, or at the parasite/vector interface (5). The first hypothesis has already received much attention and some studies have concluded to the potential existence of a genetic barrier precluding the transfer of parasites from one host species to another (especially from great apes to humans) (5, 8). This barrier would be the consequence of specific receptor/ligand interactions at the host red blood cell/parasite interface. However, this hypothesis is at odds with observations made in conditions of artificial confinement such as in ape sanctuaries, where different host species (humans and great apes) live in close proximity and where human-to-ape transfers were documented. For instance, bonobos (Pan paniscus), from a sanctuary in the Democratic Republic of Congo, were found infected with P. falciparum, a parasite supposed to be human-specific (4). A similar phenomenon was observed in chimpanzees in a Cameroonian Significance African great apes were recently found to host a large diversity of parasites (subgenus Laverania) related to the main agent of human malaria (Plasmodium falciparum). Despite their close genetic relationships, these parasites are highly host-specific, infecting either chimpanzees or gorillas. This host specificity could result from incompatibilities between parasites and hosts or from a strong host tropism of the vectors. To test this second hypothesis, we performed a large entomological survey in the heart of the Gabonese rainforest (central Africa) to identify the vector species involved in ape Plasmodium transmission. Our results demonstrated that all ape parasites are transmitted by the same three vector species, thus rejecting the hypothesis that vectors could be responsible for the Laverania host specificity.

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Dates et versions

hal-01957780 , version 1 (17-12-2018)

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Boris Makanga, Patrick Yangari, Nil Rahola, Virginie Rougeron, Eric Elguero, et al.. Ape malaria transmission and potential for ape-to-human transfers in Africa. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113 (19), pp.5329-5334. ⟨10.1073/pnas.1603008113⟩. ⟨hal-01957780⟩
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