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

Parasites are sometimes capable of inducing phenotypic changes in their hosts to improve transmission [1]. Toxoplasma gondii, a protozoan that infects a broad range of warm-blooded species, is one example that supports the so-called 'parasite manipulation hypothesis': it induces modifications in rodents' olfactory preferences, converting an innate aversion for cat odor into attraction and probably favoring trophic transmission to feline species, its only definitive hosts [2]. In humans, T. gondii induces behavioral modifications such as personality changes, prolonged reaction times and decreased long-term concentration [3]. However, modern humans are not suitable intermediate hosts because they are no longer preyed upon by felines. Consequently, behavioral modifications in infected people are generally assumed to be side effects of toxoplasmosis or residual manipulation traits that evolved in appropriate intermediate hosts. An alternative hypothesis, however, states that these changes result from parasite manipulative abilities that evolved when human ancestors were still under significant feline predation [3,4]. As such, T. gondii also alters olfactory preferences in humans; infected men rate cat urine, but not tiger urine, as pleasant while non-infected men do not [5]. To unravel the origin of Toxoplasma-induced modifications in humans, we performed olfactory tests on a living primate still predated by a feline species. We found in our closest relative, the chimpanzee (Pan troglodytes troglodytes), that Toxoplasma-infected (TI) animals lost their innate aversion towards the urine of leopards (Panthera pardus), their only natural predator. By contrast, we observed no clear difference in the response of TI and Toxoplasma-non-infected (TN) animals towards urine collected from other definitive feline hosts that chimpanzees do not encounter in nature. Although the adaptive value of parasitically induced behavior should be assessed carefully, we suggest that the behavioral modification we report could increase the probability of chimpanzee predation by leopards for the parasite's own benefit. This possible parasite adaptation would hence suggest that Toxoplasma-induced modifications in modern humans are an ancestral legacy of our evolutionary past.

Many animals rely on facial traits to recognize their kin; however, whether these traits have been selected specifically for this function remains unknown. Using deep learning for face recognition, we present the first evidence that interindividual facial resemblance has been selected to signal paternal kinship. Mandrills (Mandrillus sphinx) live in matrilineal societies, in which females spend their entire lives not only with maternal half-sisters (MHS) but also with paternal half-sisters (PHS). We show that PHS have more differentiated social relationships compared to nonkin, suggesting the existence of kin recognition mechanisms. We further demonstrate that facial resemblance increases with genetic relatedness. However, PHS resemble each other visually more than MHS do, despite both kin categories sharing similar degrees of genetic relatedness. This paternally derived facial resemblance among PHS indicates selection to facilitate kin recognition. This study also highlights the potential of artificial intelligence to study phenotypic evolution.

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.

Detecting the risk of infection and minimizing parasite exposure represent the first lines of host defence against parasites. Individuals differ in the expression of these behavioural defences, but causes of such variation have received little empirical attention. We therefore experimentally investigated the effects of several individual and environmental factors on the expression level of faecal avoidance in the context of feeding, drinking, sleeping and defecating in a wild primate population. We found a strong sex bias in the expression level of anti-parasite behaviours of grey mouse lemurs ( Microcebus murinus ), with only females strongly avoiding contaminated food, water and nests, and exhibiting selective defecation. Our results further suggest that individuals adapted their protective behaviours according to variation in intrinsic and ecological factors that may influence the cost–benefit balance of behavioural defences. Overall, individuals exhibited high consistency of investment in protective behaviours across behavioural contexts and time, suggesting that grey mouse lemurs exhibit different hygienic personalities. Finally, the global hygienic score was negatively correlated with faecal–orally transmitted parasite richness, suggesting that variation in behavioural defence has fitness consequences. We suggest that integrating inter-individual variation in behavioural defences in epidemiological studies should improve our ability to model disease spread within populations.

Several species mitigate relationships according to their conspecifics' parasite status. Yet, this defence strategy comes with the costs of depriving individuals from valuable social bonds. Animals therefore face a trade-off between the costs of pathogen exposure and the benefits of social relationships. According to the models of social evolution, social bonds are highly kin-biased. However, whether kinship mitigates social avoidance of contagious individuals has never been tested so far. Here, we build on previous research to demonstrate that mandrills ( Mandrillus sphinx ) modulate social avoidance of contagious individuals according to kinship: individuals do not avoid grooming their close maternal kin when contagious (parasitized with oro-faecally transmitted protozoa), although they do for more distant or non-kin. While individuals' parasite status has seldom been considered as a trait impacting social relationships in animals, this study goes a step beyond by showing that kinship balances the effect of health status on social behaviour in a non-human primate.

Coproscopical methods like sedimentation and flotation techniques are widely used in the field for studying simian gastrointestinal parasites. Four parasites of known zoonotic potential were studied in a free-ranging, non-provisioned population of mandrills (Mandrillus sphinx): 2 nematodes (Necatoramericanus/Oesophagostomum sp. complex and Strongyloides sp.) and 2 protozoan species (Balantidium coli and Entamoeba coli). Different coproscopical techniques are available but they are rarely compared to evaluate their efficiency to retrieve parasites. In this study 4 different field-friendly methods were compared. A sedimentation method and 3 different McMaster methods (using sugar, salt, and zinc sulphate solutions) were performed on 47 faecal samples collected from different individuals of both sexes and all ages. First, we show that McMaster flotation methods are appropriate to detect and thus quantify large protozoan cysts. Second, zinc sulphate McMaster flotation allows the retrieval of a higher number of parasite taxa compared to the other 3 methods. This method further shows the highest probability to detect each of the studied parasite taxa. Altogether our results show that zinc sulphate McMaster flotation appears to be the best technique to use when studying nematodes and large protozoa.

Animals have evolved a wide range of behaviours that act as barriers to decrease the risk of parasite infection. Faecal avoidance may, for example, limit contact with oro-faecally transmitted parasites, such as gastro-intestinal nematodes. When emitted in faeces, however, nematode eggs need to mature before reaching their infective stage. If strategies have evolved in hosts to specifically avoid nematodes, old faeces with infective larvae should elicit stronger avoidance behaviour than fresh faeces that contain non-infective stages. Here, we use two experiments to test the hypothesis that mandrills (Mandrillus sphinx), an Old-World primate, exhibit specific behavioural strategies to avoid nematode infection. Our results show that individuals do not avoid faeces in a non-feeding context but do avoid eating food items contaminated with faecal material, females more so than males. However, neither the presence of nematodes nor the age of faeces influenced the level of avoidance observed, suggesting that mandrills avoid faecal material in general rather than nematodes specifically when foraging.