Disgust as an adaptive system for disease avoidance behaviour

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'.

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Disgust as an adaptive system for disease avoidance behaviour

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2010.0117 ◽

2011 ◽

Vol 366 (1563) ◽

pp. 389-401 ◽

Cited By ~ 262

Author(s):

Valerie Curtis ◽

Mícheál de Barra ◽

Robert Aunger

Keyword(s):

Adaptive System ◽

Learning Mechanisms ◽

Disease Avoidance ◽

Psychological Traits ◽

Hygienic Behaviour ◽

Hygiene Behaviour ◽

Pathogen Prevalence ◽

Psychological System ◽

Learning Heuristics ◽

Pathogen Avoidance

Disgust is an evolved psychological system for protecting organisms from infection through disease avoidant behaviour. This ‘behavioural immune system’, present in a diverse array of species, exhibits universal features that orchestrate hygienic behaviour in response to cues of risk of contact with pathogens. However, disgust is also a dynamic adaptive system. Individuals show variation in pathogen avoidance associated with psychological traits like having a neurotic personality, as well as a consequence of being in certain physiological states such as pregnancy or infancy. Three specialized learning mechanisms modify the disgust response: the Garcia effect, evaluative conditioning and the law of contagion. Hygiene behaviour is influenced at the group level through social learning heuristics such as ‘copy the frequent’. Finally, group hygiene is extended symbolically to cultural rules about purity and pollution, which create social separations and are enforced as manners. Cooperative hygiene endeavours such as sanitation also reduce pathogen prevalence. Our model allows us to integrate perspectives from psychology, ecology and cultural evolution with those of epidemiology and anthropology. Understanding the nature of disease avoidance psychology at all levels of human organization can inform the design of programmes to improve public health.

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

Royal Society Open Science ◽

10.1098/rsos.170968 ◽

2017 ◽

Vol 4 (11) ◽

pp. 170968 ◽

Cited By ~ 19

Author(s):

Cecile Sarabian ◽

Barthelemy Ngoubangoye ◽

Andrew J. J. MacIntosh

Keyword(s):

Experimental Evidence ◽

Pan Troglodytes ◽

Comparative Research ◽

Adaptive System ◽

Parasite Infection ◽

Avoidance Behaviour ◽

Pan Troglodytes Troglodytes ◽

Sensory Modalities ◽

Biological Contaminants ◽

Parasite Avoidance

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.

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