Taste rejection of potential food items is commonly observed in the natural world: the consumer will sample a prey item orally before rejecting it. It is generally assumed that such prey are chemically defended with toxins, and that these toxins are signalled to potential consumers by an aversive taste (e.g. Bowers 1980; Jarvi, Sillen-Tullberg & Wiklund 1981; Wiklund & Jarvi 1982; Sillen-Tullberg 1985). This linkage between defence and a chemical advertisement is considered advantageous to both parties. The prey benefits from advertising its toxicity because the consumer is warned early in the predation sequence before it has irretrievably injured the prey. The predator benefits if the aversive taste reliably informs it of the danger of ingesting something dangerous and/or costly. But, how reliable is aversive taste as a signal that a potential meal is truly toxic? Evolutionary ecologists often implicitly believe in this reliability, and ‘bitter’ or ‘aversive’ are often taken as synonyms for ‘toxically defended’ (e.g. Fisher 1930; Cott 1940; Edmunds 1974; Alatalo & Mappes 1996; Tullberg & Hunter 1996; Tulberg, Leimar & Gamberale-Stille 2000; Ruxton, Speed & Sherratt 2004). However, there is no strong evidence in support of this belief, and we argue that distasteful nontoxic prey items may be widespread, and that further consideration and experimental testing of the link between toxic defence and aversive taste is required.

Some compounds would be dangerous if consumed. One of the functions of an animal's taste sensory system is to detect such compounds. However, as there are very many potentially toxic compounds, it is not practical for an animal to have dedicated taste receptors specific to each potential threat. Such a system would be physically impossible to accommodate and would be unfeasibly expensive to maintain. Hence, some degree of compromise is required; this compromise may be open to exploitation by prey.

If some toxic compounds are highly unlikely to be encountered, then there is no need to carry the ability to detect such compounds. Further, as developing and maintaining taste receptors, and the means to process information from them, are likely to incur some costs, we would expect redundant receptors to be selected out. However, this solution would leave the consumer vulnerable to the emergence of a novel toxin in their prey, with this toxin being consumed without warning, until such times as an appropriate receptor or behavioural avoidance evolves.

Another solution for consumers is to have receptors that are not specific to a single chemical compound but rather are triggered by a range of compounds. This solution requires a trade-off between specificity and generality. Generality is made more attractive by the fact that the consumer generally does not gain a fitness benefit from identifying a specific toxic compound, it may be sufficient merely to identify potential prey as dangerous to eat or not. If a particular receptor is too general in the compounds that trigger it, then it will be triggered by nontoxins as well as toxins and the consumer will mistakenly taste-reject benign and nutritious meals. However, if the receptors are too specific then either an unfeasible number of different receptors would be required, or the consumer would have to run the risk of being unable to detect some toxins.

For a specific consumer, we would expect the number and specificity of taste receptors to be shaped by evolution to trade-off the risk of failing to taste-detect toxins, and the risk of mistakenly rejecting undefended food items. The best solutions to this trade-off will differ between species, but the trade-off will always exist, and so no perfect cheat-proof taste detection of toxins will have evolved. The potential is there for consumers to be fooled into finding harmless compounds aversive.

Do we expect selection pressure on potential prey to adopt unpalatable but otherwise benign compounds instead of truly toxic ones? Toxins are generally expensive either to synthesize or sequester (see review in chapter 5 in Ruxton et al. 2004), but the same could be true of aversive nontoxins. Further, it is not clear that one category of chemicals would be more or less expensive to manufacture or collect than the other. However, toxins are expensive in another way: the physiology of the bearer of the toxins has to be modified so as to avoid the animal itself being poisoned by the toxins. These modifications will likely have fitness costs (see Tollrian & Harvell 1999). These costs could be saved by instead storing a nontoxic compound that is aversive.

There is evidence that compounds that fool taste receptors exist. Some fruiting plants produce hyper-sweet peptides that are cheaper to produce than the sugars that they mimic (Bassoli 2004); a major industrial pursuit of humans is to manufacture metabolically useless but very sweet-tasting compounds such as aspartame and saccharine (Henin 2001). Similarly, and highly relevant to our interests, children can be dissuaded from nail-biting by the application of compounds that are nontoxic but highly unpleasant to taste, such as denatonium benzoate (Bitrex). Peppers are aversive to most mammals but not birds, and this is said to aid the plant's distribution of seeds (Tewksbury & Nabhan 2001): but frugivorous mammals are being fooled by their taste receptors: the peppers may be aversant but they contain no compounds that would actually harm them, and would provide nutritional benefits.

Potential prey exploit weaknesses in other sensory systems of their consumers. Myriad examples exist of undefended prey that mimic the appearance of defended individuals (Batesian mimicry; see Ruxton et al. 2004) or whose appearance produces the optical illusion of physical defences such as spines where no such defences actually exist (Lev-Yadun 2003). Burrowing owls mimic the sound of venomous snakes so as to discourage potential predators from entering their burrows (Rowe, Cross & Owings 1986). These is no reason to think that taste has special properties that would protect it from such exploitation.

If potential prey do carry aversive nontoxins then what would be the consequences of this for evolutionary ecologists? Another layer of complexity that must be added to the potential taste mimicry of toxins is visual mimicry of aversive species by nonaversive species. Mimicry has been a fertile testbed for evolutionary thinking from Darwin and Wallace right up to the present day (Ruxton et al. 2004). Traditionally, if scientists observe individuals of both species being aversive to predators then the mimicry complex has been considered mutualistic and is termed Mullerian mimicry. Whereas, if during the learning process only individuals of one species are aversive to predators, then the relationship is considered parasitic (with the nonaversive species benefiting at the expense of the aversive one), and is termed Batesian mimicry. We now suggest that one or more of the species involved in a mimicry complex could be aversive but not toxic. How does this change our understanding of mimicry systems? In one sense, it may promote Mullerian mimicry. If nontoxic aversants are cheaper than toxins, then this may allow individuals to carry higher concentrations of these substances, making them even more aversive and speeding the aversion learning of the predators that is at the heart of Mullerian mimicry. Similarly, removing the risk of autotoxicity may allow greater variation in the types of aversants carried and indeed may allow a single individual to carry multiple aversants. As heterogeneity of aversive stimuli speeds aversive learning (Skelhorn & Rowe 2005), this too should strengthen Mullerian mimicry. However, when nontoxic aversants are used by the prey, there will be selection pressure on predators to see through this deception, and start to consume individuals that utilize this compound. Such selection would be retarded by visual mimicry between a species with a nontoxic aversant and a species with a genuine toxin: causing a switch in the mimetic relationship to a parasitic Batesian one. Even in the absence of mimicry, we have a classic ‘red queen’ coevolutionary situation where neither predators nor prey can afford to stand still. A predator that does not constantly adapt its taste sensory system will find itself being exploited by potential prey items that it mistakenly excludes from its diet on the basis of possession of nontoxic aversants. However, this very process puts evolutionary pressure on predators to develop their taste receptors so as to combat this ruse, and so potential prey may need to shift from one nontoxic aversant to another, or between nontoxic aversants and genuine toxins.

In summary, we argue that a bad taste does not necessarily indicate danger. The compromises inherent in any sensory system will leave open an opportunity for the evolution of taste deception by prey animals (and plants), and consequently also in a failure of some predators (or herbivores) to exploit potential resources. A challenge to the dogma that aversive responses are always reliable and useful is clearly warranted.


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