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.

Parasites either reduce or increase host vulnerability to fishing: a case study of a parasitic copepod and its salmonid host.

Parasites generally increase host vulnerability to predators via host manipulation for trophic transmission and reduction of host activities. Predators also select prey depending on the parasite infection status. Despite such parasites' roles in prey-predator interactions in wild animals, how parasites affect human hunting probability and resource consumption remains unknown. We examined the effects of the ectoparasitic copepod Salmincola cf. markewitschi on fish vulnerability to angling. We found that infected fish were less vulnerable compared with non-infected fish when the fish body condition was low, which was probably due to reduced foraging activity. On the contrary, infected fish were more vulnerable when the host body condition was high, probably due to the compensation of parasites' negative effects. A Twitter analysis also suggested that people avoided eating fish with parasites and that anglers' satisfaction decreased when captured fish were parasitized. Thus, we should consider how animal hunting is affected by parasites not only for catchability but also for avoiding parasite infection sources in many local regions.

Predation shifts coevolution toward higher host contact rate and parasite virulence.

Hosts can avoid parasites (and pathogens) by reducing social contact, but such isolation may carry costs, e.g. increased vulnerability to predators. Thus, many predator-host-parasite systems confront hosts with a trade-off between predation and parasitism. Parasites, meanwhile, evolve higher virulence in response to increased host sociality and consequently, increased multiple infections. How does predation shift coevolution of host behaviour and parasite virulence? What if predators are selective, i.e. predators disproportionately capture the sickest hosts? We answer these questions with an eco-coevolutionary model parametrized for a Trinidadian guppy-Gyrodactylus spp. system. Here, increased predation drives host coevolution of higher grouping, which selects for higher virulence. Additionally, higher predator selectivity drives the contact rate higher and virulence lower. Finally, we show how predation and selectivity can have very different impacts on host density and prevalence depending on whether hosts or parasites evolve, or both. For example, higher predator selectivity led to lower prevalence with no evolution or only parasite evolution but higher prevalence with host evolution or coevolution. These findings inform our understanding of diverse systems in which host behavioural responses to predation may lead to increased prevalence and virulence of parasites.

The influence of infection status and parasitism risk on host dispersal and susceptibility to infection in Drosophila nigrospiracula.

For many organisms, habitat avoidance provides the first line of defence against parasitic infection. Changes in infection status can shift the cost-benefit ratio of remaining in a given habitat vs dispersing. The aim of this study was to test the hypothesis that the propensity to disperse in Drosophila nigrospiracula is mediated by current parasite load and the risk of further infection by an ectoparasitic mite (Macrocheles subbadius). An activity monitor was used to assess dispersal propensity among infected and uninfected flies. The activity level of uninfected females increased threefold upon exposure to a mite, whereas the activity among uninfected males increased by 17-fold in the presence of a questing mite. Among infected flies, the risk of further infection also generated a change in activity, but the magnitude of the response was dependent on host sex. Current infection status influenced the probability of acquiring more parasites due to increased susceptibility to infection with mite load. The probability of acquiring additional mites among males increased more rapidly compared to female flies. Current infection status can potentially determine the risk of further infection, the host propensity and ability to disperse, with consequence for hosts and parasites at the individual, population and species level.

Smart carnivores think twice: Red fox delays scavenging on conspecific carcasses to reduce parasite risk.

The recent SARS-CoV-2 epidemic has highlighted the need to prevent emerging and re-emerging diseases, which means that we must approach the study of diseases from a One Health perspective. The study of pathogen transmission in wildlife is challenging, but it is unquestionably key to understand how epidemiological interactions occur at the wildlife-domestic-human interface. In this context, studying parasite avoidance behaviours may provide essential insights on parasite transmission, host-parasite coevolution, and energy flow through food-webs. However, the strategies of avoiding trophically transmitted parasites in mammalian carnivores have received little scientific attention. Here, we explore the behaviour of red foxes (Vulpes vulpes) and other mammalian carnivores at conspecific and heterospecific carnivore carcasses using videos recorded by camera traps. We aim to determine 1) the factors influencing the probability of foxes to practice cannibalism, and 2) whether the scavenging behaviour of foxes differ when facing conspecific vs. heterospecific carcasses. We found that red foxes were generally reluctant to consume mesocarnivore carrion, especially of conspecifics. When recorded, consumption by foxes was delayed several days (heterospecific carcasses) or weeks (conspecific carcasses) after carcass detection. Other mammalian scavengers showed a similar pattern. Also, meat-borne parasite transmission from wild carnivore carcasses to domestic dogs and cats was highly unlikely. Our findings challenge the widespread assumption that cannibalistic or intra-specific scavenging is a major transmission route for Trichinella spp. and other meat-borne parasites, especially for the red fox. Overall, our results suggest that the feeding decisions of scavengers are probably shaped by two main contrasting forces, namely the nutritional reward provided by carrion of phylogenetically similar species and the risk of acquiring meat-borne parasites shared with these species. This study illustrates how the detailed monitoring of carnivore behaviour is essential to assess the epidemiological role of these hosts in the maintenance and dispersion of parasites of public and animal health relevance.

Negative density-dependent parasitism in a group-living carnivore.

Animals living at high population densities commonly experience greater exposure to disease, leading to increased parasite burdens. However, social animals can benefit immunologically and hygienically from cooperation, and individuals may alter their socio-spatial behaviour in response to infection, both of which could counteract density-related increases in exposure. Consequently, the costs and benefits of sociality for disease are often uncertain. Here, we use a long-term study of a wild European badger population (Meles meles) to investigate how within-population variation in host density determines infection with multiple parasites. Four out of five parasite taxa exhibited consistent spatial hotspots of infection, which peaked among badgers living in areas of low local population density. Combined movement, survival, spatial and social network analyses revealed that parasite avoidance was the likely cause of this negative density dependence, with possible roles for localized mortality, encounter-dilution effects, and micronutrient-enhanced immunity. These findings demonstrate that animals can organize their societies in space to minimize parasite infection, with important implications for badger behavioural ecology and for the control of badger-associated diseases.

Low host specificity and lack of parasite avoidance by immature ticks in Brazilian birds.

Ticks are ectoparasites that feed on blood of a broad taxonomic range of terrestrial and flying vertebrates and are distributed across a wide range of environmental conditions. Here, we explore the biotic and abiotic factors on infestation probability of ticks of the genus Amblyomma and assess the degree of host specificity based on analysis of 1028 birds surveyed across Brazil. We show that tick infestation rates exhibited considerable variation across the 235 avian species analyzed and that the probability of an individual bird being parasitized by immature ticks (larvae and nymphs) increased with annual precipitation. Host phylogeny and two host ecological traits known to promote tick exposure (body mass and foraging behavior) did not predict infestation probability. Moreover, immature ticks displayed a low degree of host specificity at the family level. Lastly, tick occurrence in birds carrying infection with avian malaria and related parasites did not differ from those free of these haemosporidian parasites, indicating a lack of parasite avoidance by immature ticks. Our findings demonstrate that tick occurrence in birds across Brazilian biomes responds to environmental factors rather than ecological and evolutionary host attributes.

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.

Proximity to parasites reduces host fitness independent of infection in a Drosophila-Macrocheles system.

Parasites are known to have direct negative effects on host fitness; however, the indirect effects of parasitism on host fitness sans infection are less well understood. Hosts undergo behavioural and physiological changes when in proximity to parasites. Yet, there is little experimental evidence showing that these changes lead to long-term decreases in host fitness. We aimed to determine if parasite exposure affects host fitness independent of contact, because current approaches to parasite ecology may underestimate the effect of parasites on host populations. We assayed the longevity and reproductive output of Drosophila nigrospiracula exposed or not exposed to ectoparasitic Macrocheles subbadius. In order to preclude contact and infection, mites and flies were permanently separated with a mesh screen. Exposed flies had shorter lives and lower fecundity relative to unexposed flies. Recent work in parasite ecology has argued that parasite-host systems show similar processes as predator-prey systems. Our findings mirror the non-consumptive effects observed in predator-prey systems, in which prey species suffer reduced fitness even if they never come into direct contact with predators. Our results support the perspective that there are analogous effects in parasite-host systems, and suggest new directions for research in both parasite ecology and the ecology of fear.

Parasite and predator risk assessment: nuanced use of olfactory cues.

Foraging herbivores face twin threats of predation and parasite infection, but the risk of predation has received much more attention. We evaluated, experimentally, the role of olfactory cues in predator and parasite risk assessment on the foraging behaviour of a population of marked, free-ranging, red-necked wallabies (Macropus rufogriseus). The wallabies adjusted their behaviour according to these olfactory cues. They foraged less, were more vigilant and spent less time at feeders placed in the vicinity of faeces from dogs that had consumed wallaby or kangaroo meat compared with that of dogs feeding on sheep, rabbit or possum meat. Wallabies also showed a species-specific faecal aversion by consuming less food from feeders contaminated with wallaby faeces compared with sympatric kangaroo faeces, whose gastrointestinal parasite fauna differs from that of the wallabies. Combining both parasite and predation cues in a single field experiment revealed that these risks had an additive effect, rather than the wallabies compromising their response to one risk at the expense of the other.

Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques.

Parasites are ubiquitous in nature and can be costly to animal fitness, so hosts have evolved behavioural counter-strategies to mitigate infection risk. We investigated feeding-related infection-avoidance strategies in Japanese macaques via field-experimentation and observation. We first examined risk sensitivity during foraging tasks involving faecally contaminated or debris-covered food items, and then investigated individual tendencies to manipulate food items during natural foraging bouts. We concurrently monitored geohelminth infection in all subjects. We ran a principal component analysis on the observational/experimental data to generate a hygienic index across individuals and found that hygienic tendencies towards faeces avoidance and food manipulation correlated negatively with geohelminth infection. Females scored higher in hygienic tendencies than males, which might contribute to the common vertebrate pattern of male-biased infection. The behavioural tendencies observed may reflect a general form of hygiene, providing a mechanism of behavioural immunity against parasites with implications for the evolution and diversification of health maintenance strategies in humans.

Fatal attraction: vegetation responses to nutrient inputs attract herbivores to infectious anthrax carcass sites.

Parasites can shape the foraging behaviour of their hosts through cues indicating risk of infection. When cues for risk co-occur with desired traits such as forage quality, individuals face a trade-off between nutrient acquisition and parasite exposure. We evaluated how this trade-off may influence disease transmission in a 3-year experimental study of anthrax in a guild of mammalian herbivores in Etosha National Park, Namibia. At plains zebra (Equus quagga) carcass sites we assessed (i) carcass nutrient effects on soils and grasses, (ii) concentrations of Bacillus anthracis (BA) on grasses and in soils, and (iii) herbivore grazing behaviour, compared with control sites, using motion-sensing camera traps. We found that carcass-mediated nutrient pulses improved soil and vegetation, and that BA is found on grasses up to 2 years after death. Host foraging responses to carcass sites shifted from avoidance to attraction, and ultimately to no preference, with the strength and duration of these behavioural responses varying among herbivore species. Our results demonstrate that animal carcasses alter the environment and attract grazing hosts to parasite aggregations. This attraction may enhance transmission rates, suggesting that hosts are limited in their ability to trade off nutrient intake with parasite avoidance when relying on indirect cues.

Integrating concepts of physiological and behavioral resistance to parasites.

Conceptual parallels between physiological and behavioral forms of resistance to parasites have led to the development of terminology like "the behavioral immune system" to refer to behaviors that combat parasites. I extend this metaphor by applying findings from research on physiological resistance to generate predictions for the ecology and evolution of behavioral resistance (here, synonymous with avoidance). In certain cases, behavioral resistance may follow similar evolutionary dynamics to physiological resistance. However, more research on the nature of the costs of behavioral resistance is needed, including how parasite transmission mode may be a key determinant of these costs. In addition, "acquiring" behavioral resistance may require specific mechanisms separate from classical forms of conditioning, due to constraints on timing of host learning processes and parasite incubation periods. Given existing literature, behavioral resistance to infectious disease seems more likely to be innate than acquired within the lifetime of an individual, raising new questions about how individual experience could shape anti-parasite behaviors. This review provides a framework for using existing literature on physiological resistance to generate predictions for behavioral resistance, and highlights several important directions for future research based on this comparison.

Divergent strategies in faeces avoidance between two cercopithecoid primates.

Parasites constitute a major selective pressure which has shaped animal behaviour through evolutionary time. One adaption to parasites consists of recognizing and avoiding substrates or cues that indicate their presence. Among substrates harbouring infectious agents, faeces are known to elicit avoidance behaviour in numerous animal species. However, the function and mechanisms of faeces avoidance in non-human primates has been largely overlooked by scientists. In this study, we used an experimental approach to investigate whether aversion to faeces in a foraging context is mediated by visual and olfactory cues in two cercopithecoid primates: mandrills (Mandrillus sphinx) and long-tailed macaques (Macaca fascicularis). Visual and olfactory cues of faeces elicited lower food consumption rates in mandrills and higher food manipulation rates in long-tailed macaques. Both results support the infection-avoidance hypothesis and confirm similar tendencies observed in other primate species. More studies are now needed to investigate the divergence of avoidance strategies observed in non-human primates regarding food contamination.

Extending the ecology of fear: Parasite-mediated sexual selection drives host response to parasites.

The 'ecology of fear' describes the negative effects natural enemies have on potential victims even when those victims are not consumed or infected. Although recent work has demonstrated parasites have non-consumptive effects (NCE) on potential hosts, how these effects vary within host populations is not well understood. We investigated how NCE vary based on host risk of infection and relative cost of infection by measuring the metabolic rate (MR) of naive Drosophila nigrospiracula exposed to an ectoparasite, Macrocheles subbadius. We tested two mutually exclusive hypotheses: 1) asymmetrical costs of infection drive adaptions for stronger responses to parasite exposure; or 2) asymmetrical risks of infection drive adaptions for stronger responses to parasite exposure. In this system, male flies have higher costs of infection relative to female flies due to parasite-mediated sexual selection; similarly, virgin females experience higher costs of infection relative to mated females. Risk of infection also varies among flies because mites preferentially infect female flies over males, and mites preferentially infect mated females over virgin females. Our results were compatible with the hypothesis that costs of infection drive the strength of response to mite risk. Female flies responded to parasite exposure with a 15.1% increase in MR, while exposed males showed a stronger response with a 31.3% increase in MR. Mated females increased their MR by 34.8% during mite exposure whereas virgin females experienced an increase of 61.2%. Our findings suggest that NCE of parasites can vary based on state-dependent costs of infection.

Evolution of pathogen and parasite avoidance behaviours.

All free-living animals are subject to intense selection pressure from parasites and pathogens resulting in behavioural adaptations that can help potential hosts to avoid falling prey to parasites. This special issue on the evolution of parasite avoidance behaviour was compiled following a Royal Society meeting in 2017. Here we have assembled contributions from a wide range of disciplines including genetics, ecology, parasitology, behavioural science, ecology, psychology and epidemiology on the disease avoidance behaviour of a wide range of species. Taking an interdisciplinary and cross-species perspective allows us to sketch out the strategies, mechanisms and consequences of parasite avoidance and to identify gaps and further questions. Parasite avoidance strategies must include avoiding parasites themselves and cues to their presence in conspecifics, heterospecifics, foods and habitat. Further, parasite avoidance behaviour can be directed at constructing parasite-retardant niches. Mechanisms of parasite avoidance behaviour are generally less well characterized, though nematodes, rodents and human studies are beginning to elucidate the genetic, hormonal and neural architecture that allows animals to recognize and respond to cues of parasite threat. While the consequences of infection are well characterized in humans, we still have much to learn about the epidemiology of parasites of other species, as well as the trade-offs that hosts make in parasite defence versus other beneficial investments like mating and foraging. Finally, in this overview we conclude that it is legitimate to use the word 'disgust' to describe parasite avoidance systems, in the same way that 'fear' is used to describe animal predator avoidance systems. Understanding disgust across species offers an excellent system for investigating the strategies, mechanisms and consequences of behaviour and could be a vital contribution towards the understanding and conservation of our planet's ecosystems.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Avoidance of biological contaminants through sight, smell and touch in chimpanzees.

Avoiding biological contaminants is a well-known manifestation of the adaptive system of disgust. In theory, animals evolved with such a system to prevent pathogen and parasite infection. Bodily products are human-universal disgust elicitors, but whether they also elicit avoidance behaviour in non-human primates has yet to be tested. Here, we report experimental evidence that potential exposure to biological contaminants (faeces, blood, semen), as perceived via multiple sensory modalities (visual, olfactory, tactile), might influence feeding decisions in chimpanzees (Pan troglodytes troglodytes)-our closest phylogenetic relatives. Although somewhat mixed, our results do show increased latencies to feed, tendencies to maintain greater distances from contaminants and/or outright refusals to consume food in test versus control conditions. Overall, these findings are consistent with the parasite avoidance theory of disgust, although the presence of biological contaminants did not preclude feeding entirely. The avoidance behaviours observed hint at the origins of disgust in humans, and further comparative research is now needed.

Vertebrate defense against parasites: Interactions between avoidance, resistance, and tolerance.

Hosts can utilize different types of defense against the effects of parasitism, including avoidance, resistance, and tolerance. Typically, there is tremendous heterogeneity among hosts in these defense mechanisms that may be rooted in the costs associated with defense and lead to trade-offs with other life-history traits. Trade-offs may also exist between the defense mechanisms, but the relationships between avoidance, resistance, and tolerance have rarely been studied. Here, we assessed these three defense traits under common garden conditions in a natural host-parasite system, the trematode eye-fluke Diplostomum pseudospathaceum and its second intermediate fish host. We looked at host individuals originating from four genetically distinct populations of two closely related salmonid species (Atlantic salmon, Salmo salar and sea trout, Salmo trutta trutta) to estimate the magnitude of variation in these defense traits and the relationships among them. We show species-specific variation in resistance and tolerance and population-specific variation in resistance. Further, we demonstrate evidence for a trade-off between resistance and tolerance. Our results suggest that the variation in host defense can at least partly result from a compromise between different interacting defense traits, the relative importance of which is likely to be shaped by environmental components. Overall, this study emphasizes the importance of considering different components of the host defense system when making predictions on the outcome of host-parasite interactions.