Automimicry

In one form, first described by Lincoln Brower in 1967, weakly-defended members of a species with warning coloration are parasitic on more strongly-defended members of their species, mimicking them to provide the negative reinforcement learning required for warning signals to function. The mechanism, analogous to Batesian mimicry, is found in insects such as the monarch butterfly.

In another form, first noted by Edward B. Poulton in 1890, a less vulnerable part of an animal's body resembles a more vulnerable part, for example with deceptive eyespots or a false head that deflects attacks away from the real head, providing an immediate selective advantage. The mechanism is found in both vertebrates such as fishes and snakes, and insects such as hairstreak butterflies.

Automimicry has sometimes been put to military use. The A-10 Thunderbolt II often had a false canopy painted on its underside to confuse enemies, while the armoured recovery vehicle variant of the Churchill tank had a dummy gun, imitating an armed variant of the same tank.

Mimicry of distasteful members of the same species

Automimicry was first reported by the ecologist Lincoln Brower and colleagues, who found that monarch butterflies reared on cabbage were palatable to blue jays. However, monarchs raised on their natural host plant, milkweed, were noxious to jays - in fact, jays that ingested them vomited. Subsequently, Brower proposed the hypothesis of automimicry involving a polymorphism or spectrum of palatability: some individuals might be defended, and others palatable.

It turns out that many species of insects are toxic or distasteful when they have fed on plants that contain chemicals of particular classes, but not when they have fed on plants that lack those chemicals. For instance, some milkweed butterflies feed on milkweeds (Asclepias) which contain the cardiac glycoside oleandrin; this makes them poisonous to most predators. These insects are often aposematically coloured and patterned. When feeding on innocuous plants, they are harmless and nutritious, but a bird that has sampled a toxic specimen even once is unlikely to risk tasting harmless specimens with the same aposematic coloration. Such acquired toxicity is not limited to insects: many groups of animals have since been shown to obtain toxic compounds through their diets, making automimicry potentially widespread. Even if toxic compounds are produced by metabolic processes with an animal, there may still be variability in the amount that animals invest in them, so scope for automimicry remains even when dietary plasticity is not involved. Whatever the mechanism, palatability may vary with age, sex, or how recently they used their supply of toxin.

The existence of automimicry in the form of non-toxic mimics of toxic members of the same species (analogous to Batesian mimicry) poses two challenges to evolutionary theory: how can automimicry be maintained, and how can it evolve? For the first question, as long as prey of the species are, on average, unprofitable for predators to attack, automimicry can persist. If this condition is not met, then the population of the species rapidly crashes. The second question is more difficult, and can also be rephrased as being about the mechanisms that keep warning signals honest. If signals were not honest, they would not be evolutionarily stable. If costs of using toxins for defence affects members of a species, then cheats might always have higher fitness than honest signallers defended by costly toxins. A variety of hypotheses have been put forth to explain signal honesty in aposematic species. First, toxins may not be costly. There is evidence that in some cases there is no cost, and that toxic compounds may actually be beneficial for purposes other than defence. If so, then automimics may simply be unlucky enough not to have gathered enough toxins from their environment. A second hypothesis for signal honesty is that there may be frequency-dependent advantages to automimicry. If predators switch between host plants that provide toxins and plants that do not, depending on the abundance of larvae on each type, then automimicry of toxic larvae by non-toxic larvae may be maintained in a balanced polymorphism. A third hypothesis is that automimics are more likely to die or to be injured by a predator's attack. If predators carefully sample their prey and spit out any that taste bad before doing significant damage ("go-slow" behaviour), then honest signallers would have an advantage over automimics that cheat.