Müllerian mimicry

The Heliconius butterflies from the tropics of the Western Hemisphere are classic Müllerian mimics.^[1]

Müllerian mimicry is a natural phenomenon in which two or more distasteful species, that may or may not be closely related and share one or more common predators, have come to mimic each other's warning signals. It is named after the German naturalist Fritz Müller, who first proposed the concept in 1878.^[2]^[3]

The phenomenon can be understood by imagining two distasteful species that do not resemble one another and are also prey to a common predator. Occasionally, individuals of the predatory third species will encounter one or the other type of noxious prey, and thereafter avoid it. Predators that avoid only one of the harmful species provide no benefit to individuals of the other species. Therefore, it would be advantageous if the appearances of the two prey species were more similar. This is because a predator that learns to avoid either species in a pair of species exhibiting Müllerian mimicry learns, in effect, to avoid both.

Background

Fritz Müller

The viceroy butterfly (top) appears very similar to the noxious-tasting monarch butterfly (bottom). Although it was for a long time purported to be an example of Batesian mimicry, the viceroy has recently been discovered to be actually just as unpalatable as the monarch, making this a case of Müllerian mimicry.^[4]

Müllerian mimicry was proposed by the German zoologist and naturalist Johann Friedrich Theodor Müller (1821–1897), always known as Fritz. An early proponent of evolution, Müller offered the first explanation for resemblance between certain butterflies that had puzzled the English naturalist Henry Walter Bates, who, like Müller, spent a significant part of his life in Brazil. Müller had also seen these butterflies first hand, and collected specimens like Bates.

Understanding Müllerian mimicry is impossible without first understanding aposematism, or warning signals. Dangerous organisms with these honest signals are avoided by predators, who quickly learn after a bad experience not to pursue the same prey again. Learning is not actually necessary for animals which instinctively avoid certain prey;^[5] however, learning from experience is much more common.^[6] The underlying concept with predators that learn is that the warning signal makes the harmful organism easier to remember than if it remained as cryptic as possible (e.g. being still and silent, providing no scent, and being well camouflaged). Aposematism and crypsis 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 colors on their undersides or loud vocalizations. In this way, they enjoy the best of both strategies. These strategies may also be employed differentially throughout stages of development. For instance, large white butterflies are aposematic as larvae, but are Müllerian mimics once they emerge from the final stages of development as butterflies.^[7]

Many different prey of the same predator may employ separate warning colors, but this makes no sense for any party. Surely if they could all get together and agree on a common warning signal, the predator would have fewer detrimental experiences, and the prey would lose fewer individuals educating it. But no such conference needs to take place, as a prey species that just so happens to look a little like a harmful species will be safer than its conspecifics, leading to a tendency toward a single warning language. This can lead to the evolution of both Batesian and Müllerian mimicry, depending on whether the prey is harmful, as well, or just a free-rider. Multiple species can join this protective cooperative, expanding the mimicry ring.

Müller thus provided an explanation for 'Bates' paradox'; the mimicry was not a case of exploitation by one species, but rather a mutualistic arrangement.

Mechanism

The Müllerian strategy is usually contrasted with Batesian mimicry, in which one harmless species adopts the appearance of another, harmful species to gain the advantage of predators' avoidance. 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.^[8] Additionally, a species may be a Batesian mimic to one predator and a Müllerian mimic to another. Viceroy butterflies and monarchs (admiral butterflies) have often been called Batesian mimics; however, this is not the case as both are poisonous which makes them Müllerian mimics. Extensive mitochondrial DNA analysis of admiral butterflies has led to the discovery that the viceroy is the basal lineage of two western sister species in North America. The variation in the wing patterns are thought to precede the evolution of toxicity therefore challenging the hypothesis that the toxicity of the admiral butterflies is a conserved characteristic from a common ancestor.^[9] This explanation suggests that because some of the species of admiral butterflies that evolved after the node split from the viceroy lineage are not poisonous but look similar to their ancestor, the propensity for chemical defense is an analogous adaptation (an example of convergent evolution) that evolved separately after the species developed different phenotypic wing patterns. While Batesian and Müllerian mimicry are commonly given examples of mimicry, there is often little or no mention of other forms.^[10] There are many other types of mimicry however, some very similar in principle, others far separated. For example in aggressive mimicry a predator mimics the food of its prey, luring them towards it and improving its foraging success.

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 common signal may show convergences by the parties. While model and mimic are often closely related species, Müllerian mimicry between very distantly related taxa also occurs. And according to recent research, there may be more than just taste and population size that affect Müllerian mimetic relationships. For example: co-mimicry, a mutualistic relationship that occurs when the mimicking population is polymorphic and resembles more than one model. This keeps the ratio of mimic to model individuals for any particular coloration low, increasing overall fitness for both parties.^[11] There is a negative correlation between the frequency of mimics and the "survivability" of both species involved.^[11] This suggests that it is reproductively beneficial for both species if the models outnumber the mimics; this increases the negative interactions between predator and prey.

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…”.^[12] 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.

It is commonly believed that males would be more likely to co-mimic than females (generally being the choosier sex) but in the case of sexually dimorphic species, females are the ones that tend to be mimetic.^[13]

A plausible explanation for Müllerian mimicry is given by the "two step hypothesis". This states that first, a large mutational leap establishes an approximate resemblance of one species to another species (the "model"). For this to be part of a Müllerian mimicry model, the mimic and model must each cause an unfavorable reaction in their shared predator. Once this leap has occurred, the mimic gradually evolves greater similarity to the model, which must already be aposematic. Both species then share in the benefits of a superior defense mechanism by way of patterning changes. The likelihood that a species will be mimicked is considerably higher when there is only one key heritable trait involved in a predator's generalization of undesirability. In time, implying many generations, the trait should eventually become fixated. In contrast, "non-feature traits" do not affect the predator's selection of the mimic. Because individuals with mutated non-feature traits do not share a significant resemblance to the model in a way that is distinctive to the predator, the mimic containing this type of mutation is more likely to be eaten than mutants containing feature-trait resembling mutations. Therefore, the genetic mutation for the non-feature trait will likely not be passed on even if it confers some evolutionary advantage unrelated to predator selection. The greatest selective pressure in the system is the propensity of the predators to avoid certain recognized patterns. This selective pressure should continue until the mimicry trait spreads throughout the population.^[14]