Mandrill mothers associate with infants who look like their own offspring using phenotype matching.

Behavioral discrimination of kin is a key process structuring social relationships in animals. In this study, we provide evidence for discrimination towards non-kin by third-parties through a mechanism of phenotype matching. In mandrills, we recently demonstrated increased facial resemblance among paternally related juvenile and adult females indicating adaptive opportunities for paternal kin recognition. Here, we hypothesize that mandrill mothers use offspring's facial resemblance with other infants to guide offspring's social opportunities towards similar-looking ones. Using deep learning for face recognition in 80 wild mandrill infants, we first show that infants sired by the same father resemble each other the most, independently of their age, sex or maternal origin, extending previous results to the youngest age class. Using long-term behavioral observations on association patterns, and controlling for matrilineal origin, maternal relatedness and infant age and sex, we then show, as predicted, that mothers are spatially closer to infants that resemble their own offspring more, and that this maternal behavior leads to similar-looking infants being spatially associated. We then discuss the different scenarios explaining this result, arguing that an adaptive maternal behavior is a likely explanation. In support of this mechanism and using theoretical modeling, we finally describe a plausible evolutionary process whereby mothers gain fitness benefits by promoting nepotism among paternally related infants. This mechanism, that we call 'second-order kin selection', may extend beyond mother-infant interactions and has the potential to explain cooperative behaviors among non-kin in other social species, including humans.

Seasonality and interindividual variation in mandrill feeding ecology revealed by stable isotope analyses of hair and blood.

Mandrills are large-bodied terrestrial forest primates living in particularly large social groups of several hundred individuals. Following these groups in the wild to assess differences in diet over time as well as among individuals is demanding. We here use isotope analyses in blood and hair obtained during repeated captures of 43 identified free-ranging mandrills (Mandrillus sphinx) from Southern Gabon, to test how dietary variation relates to the season as well as an individual's age and sex. We measured the stable carbon (δ13 C‰) and nitrogen (δ15 N‰) isotope ratios in 46 blood and 214 hair section samples as well as from a small selection of mandrill foods (n = 24). We found some seasonal isotopic effects, with lower δ13 C values but higher δ15 N values observed during the highly competitive long dry season compared to the fruit-rich long rainy season. Variation in δ13 C was further predicted by individual age, with higher δ13 C values generally found in younger individuals suggesting that they may consume more high canopy fruit than older individuals, or that older individuals consume more low canopy foliage. The best predictor for δ15 N values was the interaction between age and sex, with mature and reproductively active males revealing the highest δ15 N values, despite the observation that males consume substantially less animal food items than females. We interpret high δ15 N values in these mature male mandrill blood and hair sections to be the result of nutritional stress associated with intense male-male competition, particularly during mating season. This is the first study showing isotopic evidence for nutritional stress in a free-ranging primate species and may spark further investigations into male mandrill diet and energy balance.

Author Correction: Genomes of all known members of a Plasmodium subgenus reveal paths to virulent human malaria.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Genomes of all known members of a Plasmodium subgenus reveal paths to virulent human malaria.

Plasmodium falciparum, the most virulent agent of human malaria, shares a recent common ancestor with the gorilla parasite Plasmodium 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.

Mandrills use olfaction to socially avoid parasitized conspecifics.

The evolutionary transition from a solitary to a social lifestyle entails an elevated parasite cost because the social proximity associated with group living favors parasite transmission. Despite this cost, sociality is widespread in a large range of taxonomic groups. In this context, hosts would be expected to have evolved behavioral mechanisms to reduce the risk of parasite infection. Few empirical studies have focused on the influence of pathogen-mediated selection on the evolution of antiparasitic behavior in wild vertebrates. We report an adaptive functional relationship between parasitism and social behavior in mandrills, associated with evidence that they are able to gauge parasite status of their group members. Using long-term observations, controlled experiments, and chemical analyses, we show that (i) wild mandrills avoid grooming conspecifics infected with orofecally transmitted parasites; (ii) mandrills receive significantly more grooming after treatment that targets these parasites; (iii) parasitism influences the host's fecal odors; and (iv) mandrills selectively avoid fecal material from parasitized conspecifics. These behavioral adaptations reveal that selecting safe social partners may help primates to cope with parasite-mediated costs of sociality and that "behavioral immunity" plays a crucial role in the coevolutionary dynamics between hosts and their parasites.

The host specificity of ape malaria parasites can be broken in confined environments.

Recent studies have revealed a large diversity of Plasmodium spp. among African great apes. Some of these species are related to Plasmodium falciparum, the most virulent agent of human malaria (subgenus Laverania), and others to Plasmodium ovale, Plasmodium malariae and Plasmodium vivax (subgenus Plasmodium), three other human malaria agents. Laverania parasites exhibit strict host specificity in their natural environment. Plasmodium reichenowi, Plasmodium billcollinsi, Plasmodium billbrayi and Plasmodium gaboni infect only chimpanzees, while Plasmodium praefalciparum, Plasmodium blacklocki and Plasmodium adleri are restricted to gorillas and Plasmodium falciparum is pandemic in humans. This host specificity may be due to genetic and/or environmental factors. Infrastructures hosting captive primates, such as sanctuaries and health centres, usually concentrate different primate species, thus favouring pathogen exchanges. Using molecular tools, we analysed blood samples from captive non-human primates living in Gabon to evaluate the risk of Plasmodium spp. transfers between host species. We also included blood samples from workers taking care of primates to assess whether primate-human parasite transfers occurred. We detected four transfers of Plasmodium from gorillas towards chimpanzees, one from chimpanzees to gorillas, three from humans towards chimpanzees and one from humans to mandrills. No simian Plasmodium was found in the blood samples from humans working with primates. These findings demonstrate that the genetic barrier that determines the apparent host specificity of Laverania is not completely impermeable and that parasite exchanges between gorillas and chimpanzees are possible in confined environments.

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

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.

Environmental and individual determinants of parasite richness across seasons in a free-ranging population of Mandrills (Mandrillus sphinx).

OBJECTIVES: Parasites are ubiquitous and evolve fast. Therefore, they represent major selective forces acting on their hosts by influencing many aspects of their biology. Humans are no exception, as they share many parasites with animals and some of the most important outbreaks come from primates. While it appears important to understand the factors involved in parasite dynamics, we still lack a clear understanding of the determinants underlying parasitism. In this 2-year study, we identified several factors that influence parasite patterns in a wild population of free-ranging mandrills (Mandrillus sphinx). METHODS: We explored the potential impact of seasonal factors-rainfall and temperature-and host characteristics, including sex, age, rank, and reproductive status, on parasite richness. We analyzed 12 parasite taxa found in 870 fecal samples collected from 63 individuals. Because nematodes and protozoa have different life-cycles, we analyzed these two types of parasites separately. RESULTS: Contrary to other studies where humid conditions seem favorable to parasite development, we report here that rainfall and high temperatures were associated with lower nematode richness and were not associated with lower protozoa richness. In contrast, female reproductive status seemed to reflect the seasonal patterns found for protozoa richness, as early gestating females harbored more protozoa than other females. Sex and dominance rank had no impact on overall parasite richness. However, age was associated with a specific decrease in nematode richness. CONCLUSION: Our study emphasizes the need to consider the ecological context, such as climatic conditions and habitat type, as well as the biology of both parasite and host when analyzing determinants of parasite richness.

Social organization and space use of a wild mandrill (Mandrillus sphinx) group.

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.

Malaria-like symptoms associated with a natural Plasmodium reichenowi infection in a chimpanzee.

Although Plasmodium infections have never been clearly associated with symptoms in non-human primates, the question of the pathogenicity of Plasmodium parasites in non-human primates still remains unanswered. A young chimpanzee, followed before and after release to a sanctuary, in a semi-free ranging enclosure located in an equatorial forest, showed fever and strong anaemia associated with a high Plasmodium reichenowi infection, shortly after release. The animal recovered from anaemia after several months despite recurrent infection with other Plasmodium species. This may be the first description of malaria-like symptoms in a chimpanzee infected with Plasmodium.

The oxidative cost of unstable social dominance.

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.

Age-related tooth wear differs between forest and savanna primates.

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.

Diversity, host switching and evolution of Plasmodium vivax infecting African great apes.

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.

Anopheles moucheti and Anopheles vinckei are candidate vectors of ape Plasmodium parasites, including Plasmodium praefalciparum in Gabon.

During the last four years, knowledge about the diversity of Plasmodium species in African great apes has considerably increased. Several new species were described in chimpanzees and gorillas, and some species that were previously considered as strictly of human interest were found to be infecting African apes. The description in gorillas of P. praefalciparum, the closest relative of P. falciparum which is the main malignant agent of human malaria, definitively changed the way we understand the evolution and origin of P. falciparum. This parasite is now considered to have appeared recently, following a cross-species transfer from gorillas to humans. However, the Plasmodium vector mosquito species that have served as bridge between these two host species remain unknown. In order to identify the vectors that ensure ape Plasmodium transmission and evaluate the risk of transfer of these parasites to humans, we carried out a field study in Gabon to capture Anopheles in areas where wild and semi-wild ape populations live. We collected 1070 Anopheles females belonging to 15 species, among which An. carnevalei, An. moucheti and An. marshallii were the most common species. Using mtDNA-based PCR tools, we discovered that An. moucheti, a major human malaria vector in Central Africa, could also ensure the natural transmission of P. praefalciparum among great apes. We also showed that, together with An. vinckei, An. moucheti was infected with P. vivax-like parasites. An. moucheti constitutes, therefore, a major candidate for the transfer of Plasmodium parasites from apes to humans.