Mother-to-daughter transmission of hygienic anti-parasite behaviour in mandrills.

Social animals are particularly exposed to infectious diseases. Pathogen-driven selection pressures have thus favoured the evolution of behavioural adaptations to decrease transmission risk such as the avoidance of contagious individuals. Yet, such strategies deprive individuals of valuable social interactions, generating a cost-benefit trade-off between pathogen avoidance and social opportunities. Recent studies revealed that hosts differ in these behavioural defences, but the determinants driving such inter-individual variation remain understudied. Using 6 years of behavioural and parasite data on a large natural population of mandrills (Mandrillus sphinx), we showed that, when parasite prevalence was high in the population, females avoided grooming their conspecifics' peri-anal region (PAR), where contagious gastro-intestinal parasites accumulate. Females varied, however, in their propensity to avoid this risky body region: across years, some females consistently avoided grooming it, while others did not. Interestingly, hygienic females (i.e. those avoiding the PAR) were less parasitized than non-hygienic females. Finally, age, dominance rank and grooming frequency did not influence a female's hygiene, but both mother-daughter and maternal half-sisters exhibited similar hygienic levels, whereas paternal half-sisters and non-kin dyads did not, suggesting a social transmission of this behaviour. Our study emphasizes that the social inheritance of hygiene may structure behavioural resistance to pathogens in host populations with potential consequences on the dynamics of infectious diseases.

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.

Environmental and individual determinants of fecal avoidance in semi-free ranging woolly monkeys (Lagothrix lagotricha poeppigii).

OBJECTIVES: Parasite selection pressures have driven the evolution of numerous behavioral defenses in host species, but recent studies revealed individual variation in their expression. As little is known about the factors causing heterogeneity among individuals in infection-avoidance behaviors, we investigated in woolly monkeys (Lagothrix lagotricha poeppigii) the influence of several environmental and individual characteristics on the tendency to avoid food contaminated by soil and by their own and conspecifics' feces. MATERIALS AND METHODS: We conducted feeding tests on 40 semi-free ranging individuals rescued from the pet trade. Using generalized linear mixed models, we investigated the effect of season, sex, age, dominance rank, and exposure to non-natural living conditions on feeding decisions. RESULTS: Woolly monkeys did not avoid soil-contaminated food and equally avoided food contaminated by their own and conspecifics' feces. Individuals varied greatly in their level of fecal avoidance. Only females exhibited strong avoidance of fecally contaminated food, but adapted their behavior to food availability, highlighting the trade-off between nutritional intake and parasite avoidance. Additionally, low-ranking females, less competitive over food resources, exhibited lower avoidance than dominant ones. Juveniles were more cautious than adults, possibly to compensate for a higher parasite susceptibility. Finally, we reported an unknown effect of exposure to non-natural living conditions on behavioral defenses, as animals kept as household pets for an extended period apparently lost their ability to avoid fecally contaminated food. CONCLUSION: We argue that striving to understand variation in infection-avoidance behaviors in natural populations is crucial to predict disease spread and inform conservation policies.

Unconditional care from close maternal kin in the face of parasites.

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.

Hygienic personalities in wild grey mouse lemurs vary adaptively with sex.

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.

A Comparative Study of Four Methods for the Detection of Nematode Eggs and Large Protozoan Cysts in Mandrill Faecal Material.

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.

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.

GASTROINTESTINAL PARASITES OF CAPTIVE AND FREE-LIVING LEMURS AND DOMESTIC CARNIVORES IN EASTERN MADAGASCAR.

Fecal samples from captive and free-living lemurs at Ivoloina Zoological Park (IZP) and domestic carnivores from six villages surrounding IZP were evaluated between July and August 2012. Free-living lemurs from Betampona Natural Reserve (BNR), a relatively pristine rainforest fragment 40 km away, were also evaluated in November 2013. All 33 dogs sampled (100%) and 16 of 22 cats sampled (72.7%) were parasitized, predominantly with nematodes (strongyles, ascarids, and spirurids) as well as cestodes and protozoans. Similar types of parasites were identified in the lemur populations. Identification of spirurid nematodes and protozoans in the lemur fecal samples were of concern due to previously documented morbidity and mortality in lemurs from these parasitic agents. Twelve of 13 free-living (93%) and 31 of 49 captive (63%) lemurs sampled at IZP had a higher parasite prevalence than lemurs at BNR, with 13 of 24 (54%) being parasitized. The lemurs in BNR are likely at risk of increased exposure to these parasites and, therefore, increased morbidity and mortality, as humans and their domestic animals are encroaching on this natural area.

Morbid attraction to leopard urine in Toxoplasma-infected chimpanzees.

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.

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.