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Ape Malaria Transmission and Potential for Ape-To-Human Transfers

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Ape Malaria Transmission and Potential for Ape-To-Human Transfers Ape malaria transmission and potential for SEE COMMENTARY ape-to-human transfers in Africa Boris Makangaa,b,c,1,2, Patrick Yangaria,b, Nil Raholaa,b, Virginie Rougerona,b, Eric Elgueroa, Larson Boundengab, Nancy Diamella Moukodoumb, Alain Prince Okougab, Céline Arnathaua, Patrick Duranda, Eric Willaumed, Diego Ayalaa,b, Didier Fontenillea, Francisco J. Ayalae,2, François Renauda, Benjamin Ollomob, Franck Prugnollea,b,1,2, and Christophe Paupya,b,1,2 aLaboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle, Unité Mixte de Recherche 224-5290 Centre National de la Recherche Scientifique (CNRS), Institut de Recherche pour le Développement (IRD)-Université de Montpellier, Centre IRD de Montpellier, 34394 Montpellier, France; bCentre International de Recherches Médicales de Franceville, BP769, Franceville, Gabon; cInstitut de Recherche en Ecologie Tropicale, BP13354, Libreville, Gabon; dParc de la Lékédi, Société d’Exploitation du Parc de la Lékédi/Entreprise de Recherche et d’Activités Métallurgiques/Compagnie Minière de l’Ogooué, BP 52, Bakoumba, Gabon; and eDepartment of Ecology and Evolutionary Biology, Ayala School of Biological Sciences, University of California, Irvine, CA 92697-2525 Contributed by Francisco J. Ayala, March 4, 2016 (sent for review October 14, 2015; reviewed by Carlos A. Machado and Kenneth D. Vernick) Recent studies have highlighted the large diversity of malaria (2, 4, 7) or during experimental infections (5). All this suggests parasites infecting African great apes (subgenus Laverania) and therefore a strong host specificity of the Laverania parasites. their strong host specificity. Although the existence of genetic in- The origin of this host specificity in the Laverania could result compatibilities preventing the cross-species transfer may explain from an incompatibility at the parasite/vertebrate host interface, host specificity, the existence of vectors with a high preference for at the vector/host interface, or at the parasite/vector interface a determined host represents another possibility. To test this hy- (5). The first hypothesis has already received much attention and pothesis, we undertook a 15-mo-long longitudinal entomological some studies have concluded to the potential existence of a ge- survey in two forest regions of Gabon, where wild apes live, at netic barrier precluding the transfer of parasites from one host different heights under the canopy. More than 2,400 anopheline species to another (especially from great apes to humans) (5, 8). mosquitoes belonging to 18 species were collected. Among This barrier would be the consequence of specific receptor/ligand Anopheles them, only three species of were found infected with interactions at the host red blood cell/parasite interface. Plasmodium Anopheles vinckei Anopheles moucheti ape : , , and However, this hypothesis is at odds with observations made in Anopheles marshallii . Their role in transmission was confirmed conditions of artificial confinement such as in ape sanctuaries, by the detection of the parasites in their salivary glands. Among where different host species (humans and great apes) live in An. vinckei these species, showed significantly the highest preva- close proximity and where human-to-ape transfers were docu- lence of infection and was shown to be able to transmit parasites mented. For instance, bonobos (Pan paniscus), from a sanctuary of both chimpanzees and gorillas. Transmission was also shown to ECOLOGY in the Democratic Republic of Congo, were found infected with be conditioned by seasonal factors and by the heights of capture P. falciparum, a parasite supposed to be human-specific (4). A under the canopy. Moreover, human landing catches of sylvan similar phenomenon was observed in chimpanzees in a Cameroonian Anopheles demonstrated the propensity of these three vector spe- cies to feed on humans when available. Our results suggest there- fore that the strong host specificity observed in the Laveranias is Significance not linked to a specific association between the vertebrate host and the vector species and highlight the potential role of these African great apes were recently found to host a large diversity vectors as bridge between apes and humans. of parasites (subgenus Laverania) related to the main agent of human malaria (Plasmodium falciparum). Despite their close Plasmodium | Laverania | Anopheles | ape-to-human infection | genetic relationships, these parasites are highly host-specific, African rainforest infecting either chimpanzees or gorillas. This host specificity could result from incompatibilities between parasites and hosts ecent studies on great apes in Africa have revealed the ex- or from a strong host tropism of the vectors. To test this second Ristence of a large diversity of Plasmodium parasites infecting hypothesis, we performed a large entomological survey in the chimpanzees and gorillas, some being related to the most deadly heart of the Gabonese rainforest (central Africa) to identify the Plasmodium human parasite Plasmodium falciparum (subgenus Laverania), vector species involved in ape transmission. Our others to the human parasites Plasmodium malariae, Plasmodium results demonstrated that all ape parasites are transmitted by ovale,orPlasmodium vivax (subgenus Plasmodium)(1–4). the same three vector species, thus rejecting the hypothesis that Laverania Within the subgenus Laverania, eight species are currently vectors could be responsible for the host specificity. recognized. Among them, four species (Plasmodium reichenowi, Author contributions: B.M., D.F., F.J.A., F.R., B.O., F.P., and C.P. designed research; B.M., P.Y., Plasmodium gaboni, Plasmodium billcollinsi, and Plasmodium N.R., V.R., E.E., L.B., N.D.M., A.P.O., C.A., P.D., E.W., D.A., F.P., and C.P. performed research; billbrayi) were observed only in chimpanzees and three (Plas- B.M., E.E., F.P., and C.P. analyzed data; and B.M., F.J.A., B.O., F.P., and C.P. wrote the paper. modium praefalciparum, Plasmodium adleri,andPlasmodium Reviewers: C.A.M., University of Maryland; and K.D.V., Institut Pasteur. blacklocki) only in gorillas (2, 3, 5). In this subgenus, only The authors declare no conflict of interest. P. falciparum infects humans. In natura, although these different Data deposition: The sequences reported in this paper have been deposited in the Gen- host species cooccur in the same habitat where their ranges overlap, Bank database [accession nos. KU317980–KU318030 (Cytochrome Oxydase Subunit II) and no transfer of Laverania parasites was ever documented between KU318031–KU318110 (Cytochrome b)]. humans and apes or between gorillas and chimpanzees despite large See Commentary on page 5153. sampling efforts (2, 3, 6). Similarly, ancient reciprocal transplant 1B.M., F.P., and C.P. contributed equally to this study. experiments of Laverania parasites between humans and apes 2To whom correspondence may be addressed. Email: [email protected], fjayala@ (mostly chimpanzees) failed to produce infections (5). On the con- uci.edu, [email protected], or [email protected]. trary, for parasites of the subgenus Plasmodium,likeP. vivax or This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. P. malariae, transfers were documented in natural populations 1073/pnas.1603008113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1603008113 PNAS | May 10, 2016 | vol. 113 | no. 19 | 5329–5334 Downloaded by guest on September 27, 2021 sanctuary (9), suggesting that host switches are possible under based nested PCR method. Eighty were positive (62 whole certain conditions, and hence that the species barrier might bodies and 18 salivary glands; Table S1). Overall, nine known be porous. Therefore, other factors could contribute to this Anopheles species and one undetermined Anopheles species were strong host/parasite association observed in natura in the found infected (Table S1). The average prevalences of Plasmo- Laveranias. One possibility could be that the segregation of the dium-infected Anopheles whole bodies were 5.02% in La Lopé parasites in different hosts (i.e., chimpanzees and gorillas) is (Mikongo), 2.06% near the orphan sanctuaries, and 2.17% in the the result of specific interactions between parasites and mos- wild sites of La Lékédi (Table S1). The average sporozoite rates quitoes (governed by genetic factors) or mosquitoes and hosts in these sites were 1.45%, 0.96%, and 0.94%, respectively. (i.e., feeding behavior). Alignment of the 80 parasite Cyt-b sequences with the references The previous observations highlight the need to characterize the and phylogenetic analyses revealed that they belonged to five major mode of transmission of the Laveranias among great apes and clades (Fig. 1). Four of them match with known parasites infecting particularly to identify the mosquito species involved and their bi- several mammal host species (apes, rodents, bats) and one corre- ology and dynamics in rainforests of Africa. To date, few studies sponds to parasites recently found in African antelopes (14). have addressed this question, and the natural transmission of ape Among the sequences belonging to the known parasite clades, some Plasmodium remains poorly understood, as does the transmission of (clades 1 and 2) come from parasites of great apes (57.5%), in- other zoonotic Plasmodium (e.g., rodent Plasmodium). Indeed, most cluding parasites from the subgenus Plasmodium (25% of P. vivax- information about Plasmodium mosquito vectors were acquired in like,
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