Mandrills use olfactory cues from feces of conspecifics to evaluate parasite status and avoid social contact with infectious animals.

Plasmodium falciparum, the most virulent agent of human malaria, shares a recent common ancestor with the gorilla parasite P. praefalciparum. Little is known about the other gorilla and chimpanzee-infecting species in the same (Laverania) subgenus as P. falciparum but none of them are capable of establishing repeated infection and transmission in humans. To elucidate underlying mechanisms and the evolutionary history of this subgenus, we have generated multiple genomes from all known Laverania species. The completeness of our dataset allows us to conclude that interspecific gene transfers as well as convergent evolution were important in the evolution of these species. Striking copy number and structural variations were observed within gene families and one, stevor shows a host specific sequence pattern. The complete genome sequence of the closest ancestor of P. falciparum enables us to estimate the timing of the beginning of speciation to be 40,000-60,000 years ago followed by a population bottleneck around 4,000-6,000 years ago. Our data allow us also to search in detail for the features of P. falciparum that made it the only member of the Laverania able to infect and spread in humans.

Plasmodium vivax is considered to be absent from Central and West Africa because of the protective effect of Duffy negativity. However, there are reports of persons returning from these areas infected with this parasite and observations suggesting the existence of transmission. Among the possible explanations for this apparent paradox, the existence of a zoonotic reservoir has been proposed. May great apes be this reservoir? We analyze the mitochondrial and nuclear genetic diversity of P. vivax parasites isolated from great apes in Africa and compare it to parasites isolated from travelers returning from these regions of Africa, as well as to human isolates distributed all over the world. We show that the P. vivax sequences from parasites of great apes form a clade genetically distinct from the parasites circulating in humans. We show that this clade's parasites can be infectious to humans by describing the case of a traveler returning from the Central African Republic infected with one of them. The relationship between this P. vivax clade in great apes and the human isolates is discussed.emergence | transfer | malaria | sylvatic | origin

Plasmodium falciparum, the most virulent agent of human malaria, shares a recent 25 common ancestor with the gorilla parasite P. praefalciparum. Little is known about the other gorilla 26 and chimpanzee-infecting species in the same (Laverania) subgenus as P. falciparum but none of 27 them are capable of establishing repeated infection and transmission in humans. To elucidate 28 underlying mechanisms and the evolutionary history of this subgenus, we have generated multiple 29 genomes from all known Laverania species. The completeness of our dataset allows us to conclude 30 that interspecific gene transfers as well as convergent evolution were important in the evolution of 31 these species. Striking copy number and structural variations were observed within gene families 32 and one, stevor shows a host specific sequence pattern. The complete genome sequence of the 33 closest ancestor of P. falciparum enables us to estimate confidently for the first time the timing of 34 the beginning of speciation to be 40,000-60,000 years ago followed by a population bottleneck 35 around 4,000-6,000 years ago. Our data allow us also to search in detail for the features of P. 36 falciparum that made it the only member of the Laverania able to infect and spread in humans. 37 39Main Text: 40The evolutionary history of Plasmodium falciparum, the most common and deadliest human 41 malaria parasite, has been the subject of uncertainty and debate 1,2 . Recently it has become clear that 42 P. falciparum is derived from a group of parasites infecting African Great Apes and known as the 43Laverania subgenus 2 . Until 2009, the only other species known in this subgenus was a parasite of 44 chimpanzees known as P. reichenowi, for which only one isolate was available 3 . It is now clear that 45 there are a total of at least seven species in Great Apes that naturally infect chimpanzees (P. gaboni, 46 P. billcollinsi and P. reichenowi), gorillas (P. praefalciparum, P. blacklocki and P. adleri) 4,5 , or 47 humans (P. falciparum) ( Fig. 1a). Within this group, P. falciparum is the only parasite that has 48 successfully adapted to humans after a transfer from gorillas and subsequently spread all over the 49 world 2 . 50Over time there have been various estimates concerning the evolutionary history of P. 51 falciparum with the speciation event having been estimated to be anywhere between 10,000 to 5.5 52 million years ago, the latter falsely based on the date of the chimpanzee-human split 6,7 . Others 53 report a bottleneck less than 10,000 years ago 8 , but suggest a drop to a single progenitor parasite. 54The latter seems unlikely due to the presence of allelic dimorphisms that predate speciation events 55 and therefore could not have both been transmitted if a new species were founded by a single 56 individual infection. Also, the dating of the speciation cannot be accurately estimated without the 57 genome sequence of P. praefalciparum, the closest living sister species to P. falciparum. 58The absence of in vitro culture or a usable animal mode...

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 (Plasmodium 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 specifici...

Mandrills (Mandrillus sphinx) are enigmatic Old World primates whose social organization and ecology remain poorly known. Previous studies indicated, for example, that groups are composed of only adult females and their young or that several units composed of one adult male and several females make up larger permanent social units. Here, we present the first data on group composition and male ranging patterns from the only habituated wild mandrill group and examine how home range size and daily path length varied with environmental and demographic factors over a 15-month period. Our study site is located in southern Gabon where we followed the group on a daily basis, collecting data on presence, ranging, behavior, and parasite load of its individual members. Throughout the study, the group was made up of about 120 individuals, including several non-natal and natal adult and sub-adult males. One-male units were never observed. The mandrills traveled an estimated 0.44-6.50 km/day in a home range area of 866.7 ha. Exploratory analyses revealed that precipitation, the number of adult males present, and the richness of protozoan parasites were all positively correlated with daily path length. These results clarify the social system of mandrills and provide first insights into the factors that shape their ranging patterns.

High social rank is expected to incur fitness costs under unstable social conditions. A disruption of the oxidative balance may underlie such effects, but how markers of oxidative stress vary in relation to social rank and stability is unknown. We examined in mandrills whether the mating season characterized by social instability between males (but not between females) affected their oxidative balance differently according to their social rank. Outside the mating season, high-ranking males showed the lowest levels of oxidative damage, while during the mating season, they were the only males to experience increased oxidative damage. In contrast, the mating season increased oxidative stress in all females, irrespective of their social rank. These results support the hypothesis that the coupling between social rank and social stability is responsible for differential costs in terms of oxidative stress, which may explain inter-individual differences in susceptibility to socially induced health issues.

Tooth wear in primates is caused by aging and ecological factors. However, comparative data that would allow us to delineate the contribution of each of these factors are lacking. Here, we contrast age-dependent molar tooth wear by scoring percent of dentine exposure (PDE) in two wild African primate populations from Gabonese forest and Kenyan savanna habitats. We found that forest-dwelling mandrills exhibited significantly higher PDE with age than savanna yellow baboons. Mandrills mainly feed on large tough food items, such as hard-shell fruits, and inhabit an ecosystem with a high presence of mineral quartz. By contrast, baboons consume large amounts of exogenous grit that adheres to underground storage organs but the proportion of quartz in the soils where baboons live is low. Our results support the hypothesis that not only age but also physical food properties and soil composition, particularly quartz richness, are factors that significantly impact tooth wear. We further propose that the accelerated dental wear in mandrills resulting in flatter molars with old age may represent an adaptation to process hard food items present in their environment.