If the mechanism allowing automimics to persist is optimal diet selection by predators, then we can make certain predictions about the ecological circumstances in which automimics can flourish. They can exist at ecologically relevant frequencies if their potential predators have alternative prey that is abundant, if the time to evaluate whether an individual is defended or not is long, or if automimics take a long time to assess or otherwise handle and/or are of low energetic value, relative to alternative prey types. Clearly, all species will be under selection pressure to make themselves uneconomical to potential predators, hence the interesting variable here is the time taken to evaluate whether an individual is defended or not. This produces selection on automimics to resemble defended individuals as accurately as possible. Conversely, since there is likely to be a cost to being sampled even if this leads to rejection, defended individuals will be under selection pressure to allow differentiation to occur as quickly as possible in a predation sequence. This can lead to evolutionary pressure for reliable, self-advertising physical defences such as spines that can be seen at a distance and hence are very difficult or impossible for undefended individuals to successfully mimic. Even for toxic defences, automimicry should lead to evolutionary pressure for the predator to detect these defences as early in the predation process as possible. Toxins should, therefore, be very close to (if not on) the surface of the animal itself, concentrated in areas that predators first come into contact with, and of such a chemical nature that they can be detected as easily as possible (cf. Poulton 1890
In our simple model of predator selection, we assumed that the predator must avoid defended prey at all costs. There may be situations where the level of defence of defended individuals might be more moderate, such that predators would prefer to avoid them if possible, but occasional ingestion can be tolerated (Kokko et al. 2003
; Sherratt et al. 2004
). This could lead to an increased behavioural repertoire being open to the predator. Instead of ignoring all individuals, or sampling carefully to weed out defended individuals, it could simply ingest all individuals of the automimicked population that it encounters. This would not be an attractive strategy if automimics are rare, but if automimics are plentiful then this may become an attractive strategy (if unselective processing allows a time and/or energy saving that compensates for occasional consumption of defended individuals). Under such circumstances, both defended and undefended individuals would suffer similar predation costs, and so—assuming defences are costly—automimics would rise to fixation. Hence, in order to avoid this outcome, defended prey must invest in defences of sufficient potency that unselective ingestion is not an attractive option to predators. We might, therefore, expect to see adaptive automimicry occur only in species where the defences adopted by some individuals in the population are of high potency to potential predators.
A key assumption of scenarios 2 and 3 is that defence is costly. If there is no cost to defence in these two scenarios then the defended morph always has higher fitness and we would not expect to find automimicry persisting in such systems. However, there is now growing empirical evidence that defences are costly in a wide variety of, though not necessarily all, circumstances (Ruxton et al. 2004
, pp. 59–63).
We also demonstrate that a variable predation pressure can provide a theoretical mechanism by which both defended and undefended types can co-exist in the long term, even if defence is costly and predators can differentiate and preferentially consume undefended individuals. Temporal fluctuation in per-capita rate of attack can be driven by variation in the numbers of either the focal species, the predator population or the availability of alternative prey types. These fluctuations could be driven by either intrinsically unstable population dynamics, by external factors such as weather patterns and by migration. In the earliest theoretical paper on automimicry, Brower et al. (1970)
argued that for the monarch, Danaus plexippus
, predation pressure is likely to be highly variable because of migratory change, writing:
in most of North America [the number of prey per predator] is small during the northward migration in the spring. By late summer successive generations have increased the size of the butterfly populations all over North America and [the number of prey per predator] is large.
Furthermore, both defended and undefended phenotypes could be maintained if there is no temporal variation in predator number, but spatial variation combined with migration such that there is mixing of prey individuals between areas where defended individuals have an advantage and areas where undefended individuals have the advantage.
It is important to note that fluctuation itself is not a sufficient condition for retention of both phenotypes in the population: the fluctuation must be such that predation pressure repeatedly moves from one side of the critical value of attack rate to the other; switches must also be sufficiently frequent that neither type is able to rise to fixation before selection changes to favour the other type. Further, if reproduction is synchronized, then switches must not be so frequent that although switches occur the average frequency of attacks over the course of a generation is always on one side of the critical value or the other.
(a) What range of chemical defences might show automimicry?
In the literature, automimicry is usually associated with constitutive defences that are not controlled responsively by the individual animal (e.g. a toxin stored in a butterfly's cuticle that is continually present within an individual). However, the scope of automimicry may be wider than this. In many arthropod species, constitutive chemical defences can be used responsively by defensive secretion (e.g. when a ladybird carries out costly reflex bleeding, Whitman et al. 1990
; Grill & Moore 1998
). This leads to the potential for automimicry in the sense that animals may be able to choose whether or not to ‘fire off’ for a given level of predatory threat, in which case we hypothesize that there may be automimics that tend to reserve their toxins and automodels that more readily deplete them and pay the costs of restoring them subsequently. Although, the data are to our knowledge currently lacking, it is an interesting possibility that prey that utilize their toxins responsively may contain a proportion of such automimics. Should this be the case, then models like those described here may apply (albeit in a modified form).
Furthermore, even if all capable prey always use their defensive secretion when attacked, there will still be some level of automimicry if the defensive act quickly depletes the defensive store, leaving recently disturbed individuals as effectively undefended automimics for a refractory period (e.g. Holloway et al. 1991
). In this case, automimicry is a constraint of a particular defensive system and it does not need the treatments described here to explain it. However, if attacks were frequent (relative to the time required to recover defences) and predators could costlessly discriminate defended from undefended-depleted individuals, the entire system of defensive secretion would be unstable and some alternative defence would be necessary. Hence, prohibitive handling costs for predators, like those described in the first model of this paper, reduce the predatory burden on such transient obligate automimics, thereby rendering the overall strategy of defensive secretion (and a subsequent refactory period of vulnerability) profitable and stable. In other cases where the defence is truly inducible (i.e. a toxin is not present in an animal until it is induced by a predatory cue), other modelling schemes apply (Clark & Harvell 1992
; Tollrian & Harvell 1999
(b) How best might the assumptions and predictions of this theory be tested?
This paper was prompted by Gamberale-Stille & Guilford's (2004)
demonstration that chicks can differentially consume undefended artificial prey, while rejecting very similar looking defended individuals. Since, all our theory rests on this behaviour, the most important empirical task is to explore its generality and fine detail. Thus, it would be useful to explore whether similar selective behaviour is found in experiments that are closer to ecologically relevant conditions. Particularly, interesting would be experiments that utilized natural prey. Specifically, if it where possible to assay individuals of a prey species for strength of defence prior to offering them to predators, then one could test whether less defended individuals were preferentially consumed. This may be possible with prey species such as ladybirds that defend themselves by releasing chemically loaded reflex blood, a process than can be induced by experimenters, allowing the blood to be analysed for level of defence without destroying the prey (Holloway et al. 1991
). A further benefit to such an experiment is that one could explore whether predators can differentiate between two non-zero levels of defence: Gamberale-Stille & Guilford's birds differentiated between defended and entirely undefended prey.
The key assumption of the first mechanism described in this paper is that careful sampling and discrimination of prey individuals is expensive (in time spent) for predators. It should be possible to test this assumption with, for example, similar chick experiments to those of Gamberale-Stille & Guilford (2004)
by adding a control manipulation where only undefended prey are offered to the birds and no discrimination is required. One theoretical prediction from our first model that should be particularly amenable to testing is the prediction in equation (2.3)
for when a prey type featuring automimicry should or should not be included in a predator's diet. All of the parameters of this equation could be controlled in laboratory experiments allowing predictions as to whether predators would exploit a given prey type that features automimicry: these predictions then being tested by observation of real predators. More challenging to organize, but still within the bounds of possibility would be to use equation (2.3)
combined with empirically derived estimates of the necessary parameter values for a natural system, then compare the actual level of automimicry found in real prey populations with than predicted by equation (2.3)
Testing the mechanism that relates temporal variation in predation pressure to the existence of automimicry may be more challenging because obtaining quantitative predictions from the models would involve obtaining an estimate of the cost of defence. Measurements of the cost of defence are often technically challenging, although there have been notable successes (reviewed in Ruxton et al. 2004
). However, a useful first step would be to measure temporal variation in predation pressure on a natural prey species that features automimicry, then equation (3.1)
can be used to estimate low large the cost of defence would have to be for temporal variation in predation pressure to explain the maintenance of automimicry in this prey species. The plausibility of this estimated cost could then be evaluated in terms of our understanding of the physiology and life history of the species, and further could inform the design of experiments aimed at quantifying the cost empirically. Similarly, an important first step in exploring the importance of our third mechanism would be to use either natural variation in subpopulations in level of automimicry, or controlled variation in artificial-prey experiments to explore whether there is any evidence that predators do increase their attack rate on populations that have higher levels of automimicry.
Particularly with reference to our final non-adaptive explanation for within-population variance in level of defence, it would be valuable to empirically explore whether an example of naturally occurring automimicry appears to be adaptive. Specifically, this requires exploring whether ecological circumstances can vary (either naturally or by experimental manipulation) such that either high or low defence is selectively favoured in the manner predicted by the first three explanations of this paper. This could be done by for example, experimentally reducing predation pressure on an prey populations that feature automimics. If automimicry is driven by an adaptive explanation such as the first three given in this paper, then we would expect that this should lead to an increase in the frequency of automimics within the population. Such experiments could be carried out in laboratory colonies or in the wild using predator-excluding enclosures.