Reflexive And Learned Responses To Pathogens

Animals must adapt to their environment or suffer the consequences. Obvious examples of environmental adaptation include appropriate food-seeking and storage, as well as behaviours that facilitate thermoregulation and avoid predators [6]. Other behavioural adaptations may involve avoiding pathogens and responding in ways that minimize the effects of pathogens.

The best defence against an infection is to avoid contact with the pathogen. Thus responding to the environment in a way that minimizes contact with pathogens is an important component of behavioural defence. Avoidance behaviours can result from simple reflexes as well as learning from previous experience, and the spectrum of avoidance-related behaviours can be quite varied (e.g., nest building, foraging strategies, eliminative behaviour, food selection and grooming). We will address only a few examples. One such is the response to faeces. Faecal matter avoidance appears in the behavioural repertoire of many animals [7,8], including cattle [8], horses

[9], monkeys [10], and others [7]. In some cases, the unpleasant aroma associated with faecal matter may elicit a reflexive avoidance response without prior training or exposure, allowing the organism to avoid numerous pathogens in its environment. In addition to simply avoiding faeces, animals defecate and feed in ways suggesting faecal matter avoidance. For example, it has been observed that Howler monkeys defecate less often in areas they use predominantly for foraging than in other less foraged areas [10]. This suggests that this species both avoids faeces and defecates in a manner that will minimize contact with faeces and possible food contamination. Other animals (e.g., horses) avoid consuming foodstuffs contaminated with faeces and are known to defecate preferentially in areas where little grazing occurs [9]. Consistent with this, most humans tend to avoid eating in the bathroom.

For humans, one aspect of avoiding faeces is the disgust it invokes. Curtis and Biran suggested that faecal matter is but one of a number of stimuli that elicit a disgust response [11]. Other stimuli include (but are not limited to) other body excretions, body parts, and decaying and spoiled food. These "elicitors of disgust" were compiled after surveying people from four distinct regions (India, Africa, the Netherlands, and the United Kingdom), and in one international airport. Curtis and Biran noted that the primary stimuli that elicit disgust are potential sources of infection. A prime example is faeces, which are considered disgusting by most people, and are a major source of infections (e.g., Salmonella, Escherichia coli, Shigella, Giardia). Other objects of disgust such as vomit and saliva are also potential sources of infection. Curtis and Biran argued that the disgust response elicited by stimuli like faeces is adaptive because it produces avoidance of the potential source of a pathogen [11] (also discussed in [12]).

While faecal matter avoidance can be an effective means of pathogen avoidance it is not a universal phenomenon. Some organisms consume faeces (coprophagia) from their own species (see [7]), and less often, faeces from other species (e.g., [13]). There are a number of explanations for this. One is that faeces (or rather the cecal fluid associated with the faeces [14]) may provide animals with essential nutrients or assist them in maintaining their intestinal flora [15,16], Also, the young of some species consume the faeces of their mothers and this provides the young with appropriate intestinal microflora, and the deoxycholic acid ingested protects them against endotoxins [17], Additionally, nursing mothers of some species (including numerous rodent species) wash their young by licking them, especially in the anogenital area. Thus the mother is likely to synthesize antibodies to any pathogens ingested, which can then be transferred to the infant in breast milk [18]. Presumably, in these instances the benefits obtained by the faecal ingestion outweigh the costs associated with pathogen exposure from this material.

As indicated above, it has been shown that certain animals avoid faeces. Others have shown that animals may avoid food that is infected with pathogens. Recently, Pujol and colleagues [19] investigated the role of the toll-like receptor in avoidance of pathogens using C. elegans. Toll-like receptors are important in innate immunity because they recognize microbe-derived molecules such as LPS, and the activation of these receptors is important for the synthesis of proinflammatory cytokines [20]. Pujol and colleagues demonstrated that variants of C. elegans that express the gene tol-1, which encodes a toll-like receptor (TLR1), respond more effectively to certain bacteria in their food than organisms lacking the gene [ 19]. In particular, it was found that C. elegans mutants lacking tol-1 did not avoid the pathogen S. marcescens unlike the wild type. Thus the tol-1 receptor appears to be important for recognizing and avoiding certain pathogens and provides animals a behavioural advantage for avoiding bacteria. Based on this observation in C. elegans, it is likely that other animals also have genes (possibly for other toll-like receptors) that affect pathogen avoidance, warranting further investigation.

While we have mainly focused on the reflexive avoidance of a pathogen, other behavioural strategies also serve a defensive role. In organisms unable to avoid contact with pathogens, a second line of behavioural defence is to remove the pathogen from the body. Reflexive behaviours such as coughing, vomiting and diarrhoea expel pathogens from the body, minimizing their effects, and facilitating return to health. Other adaptive, health-promoting behaviours include activities like grooming, stomping or tail flicking to remove external pathogens from the body. For a more complete discussion of these behavioural strategies, see Hart [7].

An animal cannot always reflexively avoid or remove pathogens. Thus learning to avoid stimuli previously associated with pathogen exposure or illness is an important line of defence. An important example of this, conditioned taste aversion, was first studied by Garcia and colleagues [21] and is often referred to as the 'Garcia effect.' In a typical taste aversion experiment, thirsty animals are given the opportunity to drink a novel, highly palatable solution (the conditioned stimulus, CS). Following consumption, animals are exposed to an illness-inducing agent (the unconditioned stimulus, US); early experiments used radiation exposure to induce illness, but numerous other treatments (e.g., lithium chloride) have been used for this purpose. Once the association between the illness and the novel tasting solution has been made, animals avoid the solution. A taste aversion can be produced with a single flavour-illness pairing, and even if there is a lengthy delay (e.g., many hours) between the taste and the illness. More recent work has demonstrated that if animals are exposed to an agent such as LPS that induces an acute phase response, a conditioned taste aversion can be induced [22]. Tumour growth may also induce a taste aversion for novel food consumed [23,24], presumably because the tumour serves as the illness-inducing US and the novel tasting food as the CS. In these and other demonstrations, animals learned to associate a flavour with an illness-inducing event and subsequently avoid that flavour.

Although laboratory work has paired specific flavours with distinct illness-inducing agents, conditioned taste aversions occur naturally where the flavour and the illness-inducing agent are often part of the same stimulus complex. For example, a poisonous mushroom may possess a specific novel taste and also delivers a toxin to the animal that consumes it. The animal will learn to associate the effect of the toxin with the taste of the mushroom and will subsequently avoid it. Such taste aversions are highly adaptive; an animal that does not learn to avoid a flavour associated with sickness is at risk of poisoning and death. Thus avoidance of an illness-inducing flavour is an effective behavioural defence.

Conditioned taste aversions may have efficacy beyond inducing flavour avoidance/aversion; they may also condition the immune system. It has been shown that a taste stimulus that precedes inhibition of the immune system will, upon re-exposure, produce a similar inhibition of the immune system [25]. If the conditioned stimuli (taste or otherwise) were to elicit immune system enhancement, an individual re-exposed to these stimuli would be aided by the activity of the immune system. Some work has shown conditioned immunoenhancing responses. For example, Ramirez-Amaya and Bermudez-Rattoni have recently shown that rats can exhibit increased antibody responses when exposed to a stimulus associated with antigen exposure [26]. They paired either a novel taste or a novel odour with a hen egg lysozyme (HEL) antigen. Re-exposure to the taste or odour was associated with enhanced HEL IgG antibody production in conditioned animals. In humans, Stockhorst and colleagues showed that patients undergoing chemotherapy have higher levels of natural killer cells and IFNy when tested in the hospital setting than when tested at home [27]. Although they did not manipulate the exposure to chemotherapy, they argued that the hospital was a conditioned environment (CS) because of its association with the immune-enhancing effect of chemotherapy (US), and would be expected to induce immune responses not present in the home.

In a conditioned taste aversion paradigm, taste avoidance results from exposure to pathogens or illness-inducing agents. It is also possible that taste avoidance, and presumably pathogen avoidance, can be learned by observation. Much work by Galef and others (for reviews, see [28,29]) has clearly demonstrated that dietary choice and food preference can be passed from one member of the species to others. In a typical procedure, a "demonstrator" animal, for example a rat, is given access to food with a distinct odour and is then allowed to interact with an "observer" rat. The observer rat, though never having had access to this food, will subsequently demonstrate a preference for the food the demonstrator ate over another, novel food. In humans, food preferences may be dependent upon social learning, so that children acquire taste preferences by observing their parents and peers eating and enjoying particular foods [30,31]. The extent to which dietary preference is related to immunocompetence has not been investigated specifically. However, young animals learn from other members of the species which foods are safe to eat, and this can protect the animal against future illness. If the young learn about dietary selection by observation, they enjoy the benefits of the experience of others and avoid the risks, and possible pathogens, associated with the consumption of novel foods.

As can be seen from the examples listed above, animals have a number of behavioural strategies to facilitate pathogen avoidance: avoiding stimuli that may be infected with pathogens, avoiding stimuli that have previously made you sick, and learning to distinguish healthy from unhealthy foods. We have not described the entirety of reflexes and learned behaviours that animals make in response to pathogens, but have merely emphasized the importance of both reflexive and learned behaviours in avoiding and minimizing the effects of pathogens, as part of behavioural defence [7]. Below we shall consider what happens to organisms when such avoidance is not immediately successful.

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