Müllerian mimicry is a type of biological mimicry in which two or more well-defended species, often foul-tasting and sharing common predators, converge in appearance to mimic each other's honest warning signals. This convergence of appearance achieves the following benefit to species that undergo it: predators need only experience a single unpleasant encounter with any member of a set of Müllerian mimics in order to thereafter avoid all creatures of similar appearance, whether or not it is the same species as the initial encounter. A ring of distinct species is thereby protected from their mutual predators by attempted predation upon any one of its members. The phenomenon is named after the German-Brazilian naturalist Fritz Müller, who proposed the concept in 1878, supporting his theory with a mathematical model of frequency-dependent selection, one of the first such models to be deployed in biology.
Müllerian mimicry was first identified in tropical butterflies that shared colourful wing patterns, but it is found in many groups of insects such as bumblebees, as well as in other animals such as poison frogs and coral snakes. The mimicry need not be restricted to that detected by vision—many snakes share auditory warning signals. Similarly, the defences involved are not limited to toxicity—anything that tends to deter predators, such as foul taste, sharp spines, or defensive behaviour can make a species unprofitable enough to predators to allow Müllerian mimicry to develop.
Once a pair of Müllerian mimics has formed other mimics may join them by advergent evolution (one species changing to conform to the appearance of the pair, rather than mutual convergence), forming mimicry rings. Large rings are found among the several thousand species of velvet ants (which are all, in fact, types of wasp). Because the frequency of mimics in a given environment is positively correlated with an individual mimic's survival, the rarer mimics come to resemble the commoner models, favouring both advergence and ever-larger rings of Müllerian mimicry. Where Müllerian mimics are not strongly protected by venom or other defences, honest Müllerian mimicry transforms incrementally into the better-known bluffing of Batesian mimicry.
History
Origins
Müllerian mimicry was proposed by Fritz Müller (1821–1897). An early proponent of evolution, Müller offered the first explanation for resemblance between certain butterflies that had puzzled the English naturalist Henry Walter Bates in 1862. Bates, like Müller, spent a significant fraction of his life in Brazil, which Bates described in his book The Naturalist on the River Amazons. Bates conjectured that these abundant and distasteful butterflies might have been caused to resemble each other by their physical environment. Müller had also seen these butterflies first hand and, like Bates, had collected specimens. Müller proposed a variety of other explanations. One was sexual selection—that individuals would choose to mate with partners with frequently-seen coloration, such as those resembling other species. However, if as is usual, females are the choosers, then mimicry would be seen in males, but in sexually dimorphic species, females are more often mimetic. Another was, as Müller wrote in 1878, that "defended species may evolve a similar appearance so as to share the costs of predator education."
Müller's mathematical model
Müller's 1879 account was the earliest use of a mathematical model in evolutionary ecology, and the first exact model of frequency-dependent selection. Mallet calls Müller's mathematical assumption behind the model "beguilingly simple". Müller presumed that the predators had to attack n unprofitable prey in a summer to experience and learn their warning coloration. Calling a1 and a2 the total numbers of two unprofitable prey species, Müller then argued that, if the species are completely unalike they each lose n individuals. However, if they resemble each other,
then species 1 loses individuals, and species 2 loses individuals.
Species 1 therefore gains
and species 2 similarly gains in absolute numbers of individuals not killed.
The proportional gain compared to the total population of species 1 is
and similarly for species 2 , giving the per head fitness gain of the mimicry when the predators have been fully educated.
Hence, Müller concluded, the proportion g1:g2 was , which equals , and the rarer species gains far more than the commoner one.
The model is an approximation, and assumes the species are equally unprofitable. Later models are more complex. If one is more distasteful than the other, then the relative gains differ further, the less distasteful species benefiting more (as a square of the relative distastefulness) from the protection afforded by mimicry. Some have argued that some "Müllerian" mimicry may be "quasi-Batesian", or parasitic, rather than mutualistic. In "quasi-Batesian" mimicry, a weakly unpalatable species is proposed to gain protection from mimicry, while the strongly protected "model" species it mimics suffers greater predation as a result of the weakening of the average distastefulness of the mimetic pair. The assumption of a fixed number n to be attacked is a useful first step, but unlikely to perfectly reflect the effect of predators' memories. Müller also effectively assumed a step function, when a gradual change (a functional response) is more plausible.
Non-deceitful mimicry
Biologists have not always viewed the Müllerian mechanism as mimicry, both because the term was strongly associated with Batesian mimicry, and because no deception was involved—unlike the situation in Batesian mimicry, the aposematic signals given by Müllerian mimics are (unconsciously) honest. Earlier terms, no longer in use, for Müllerian mimicry included "homotypy", "nondeceitful homotypy" and "arithmetic homotypy".
Evolution
Aposematism, camouflage, and mimicry
Müllerian mimicry relies on aposematism, or warning signals. Dangerous organisms with these honest signals are avoided by predators, which quickly learn after a bad experience not to pursue the same unprofitable prey again. Learning is not actually necessary for animals which instinctively avoid certain prey; however, learning from experience is more common. The underlying concept with predators that learn is that the warning signal makes the harmful organism easier to remember than if it remained as well camouflaged as possible. Aposematism and camouflage are in this way opposing concepts, but this does not mean they are mutually exclusive. Many animals remain inconspicuous until threatened, then suddenly employ warning signals, such as startling eyespots, bright colours on their undersides or loud vocalizations. In this way, they enjoy the best of both strategies. These strategies may also be employed differentially throughout development. For instance, large white butterflies are aposematic as larvae, but are Müllerian mimics once they emerge from development as adult butterflies.
Selective advantage
Many different prey of the same predator could all employ their own warning signals, but this would make no sense for any party. If they could all agree on a common warning signal, the predator would have fewer detrimental experiences, and the prey would lose fewer individuals educating it. No such conference needs to take place, as a prey species that just so happens to look a little like an unprofitable species will be safer than its conspecifics, enabling natural selection to drive the prey species toward a single warning language. This can lead to the evolution of both Batesian and Müllerian mimicry, depending on whether the mimic is itself unprofitable to its predators, or just a free-rider. Multiple species can join the protective cooperative, expanding the mimicry ring. Müller thus provided an explanation for Bates' paradox; the mimicry was not, in his view, a case of exploitation by one species, but rather a mutualistic arrangement, though his mathematical model indicated a pronounced asymmetry.
Relationship to Batesian mimicry
The Müllerian strategy is usually contrasted with Batesian mimicry, in which one harmless species adopts the appearance of an unprofitable species to gain the advantage of predators' avoidance; Batesian mimicry is thus in a sense parasitic on the model's defences, whereas Müllerian is to mutual benefit. However, because comimics may have differing degrees of protection, the distinction between Müllerian and Batesian mimicry is not absolute, and there can be said to be a spectrum between the two forms.
Viceroy butterflies and monarchs (types of admiral butterfly) are both poisonous Müllerian mimics, though they were long thought to be Batesian. Mitochondrial DNA analysis of admiral butterflies shows that the viceroy is sister to two western sister species in North America. The variation in wing patterns appears to have preceded the evolution of toxicity, while other species remain non-toxic, refuting the hypothesis that the toxicity of these butterflies is a conserved characteristic from a common ancestor.
Non-visual mimicry
Müllerian mimicry need not involve visual mimicry; it may employ any of the senses. For example, many snakes share the same auditory warning signals, forming an auditory Müllerian mimicry ring. More than one signal may be shared: snakes can make use of both auditory signals and warning coloration.
Negative frequency-dependent selection
There is a negative correlation between the frequency of mimics and the "survivability" of both species involved. This implies that it is reproductively beneficial for both species if the models outnumber the mimics; this increases the negative interactions between predator and prey.
Genetics
Some insight into the evolution of mimetic color mimicry in Lepidoptera in particular can be seen through the study of the Optix gene. The Optix gene is responsible for the Heliconius butterflies' signature red wing patterns that help it signal to predators that it is toxic. By sharing this coloration with other poisonous red winged butterflies the predator may have pursued previously, the Heliconius butterfly increases its chance of survival through association. By mapping the genome of many related species of Heliconius butterflies "show[s] that the cis-regulatory evolution of a single transcription factor can repeatedly drive the convergent evolution of complex color patterns in distantly related species…". This suggests that the evolution of a non-coding piece of DNA that regulates the transcription of nearby genes can be the reason behind similar phenotypic coloration between distant species, making it hard to determine if the trait is homologous or simply the result of convergent evolution.
Two step evolution
One proposed mechanism for Müllerian mimicry is the "two step hypothesis". This states that a large mutational leap initially establishes an approximate resemblance of the mimic to the model, both species already being aposematic. In a second step, smaller changes establish a closer resemblance. This is only likely to work, however, when a trait is governed by a single gene, and many coloration patterns are certainly controlled by multiple genes.
Advergence versus mutualism
The mimic poison frog Ranitomeya (Dendrobates) imitator is polymorphic, with a striped morph that imitates the black and yellow striped morph of Ranitomeya variabilis, a spotted morph that imitates the largely blue-green highland spotted morph also of R. variabilis, and a banded morph that imitates the red and black banded Ranitomeya summersi.
R. imitator has thus apparently evolved in separate populations to resemble different targets, i.e. it has changed to resemble (adverged on) those target species, rather than both R. imitator and the other species mutually converging in the way that Müller supposed for tropical butterflies.