How does mimicry support evolution

A general introduction that takes the phenomenon as whole can be found in Joron ; Ruxton, et al. As protective mimicry is an adaptation against predation, one needs to understand first how the process of predation creates a selective pressure on its prey as described by Endler As the benefit of mimetic resemblance is based on aposematism, it is also important to understand the special relationship between aposematic prey and their potential predators, which are topics covered by Rowe and Ruxton, et al.

As mimicry itself can be classified as similarity among different parties, in addition to the protective mimicry, other types of mimicry also exist that Pasteur nicely lists. Mimicry in plants is most commonly associated in gaining pollination benefits, and the plants therefore resemble some reproductive structures of those insects that pollinate them. Barrett is an early review of plant mimicry that includes, for example, orchids having both visual and olfactory mimics of a female wasp to lure males to both deposit and pick up pollen.

Barrett, Spencer C. Mimicry in plants. Scientific American — DOI: Describes mimicry in plants with many examples and suggests that it involves many ecological interactions. Mimicry in plants can be seen as a diverse phenomenon ranging from deception insect pollinators to avoidance of predators humans on weed species. Brower, Lincoln P. Mimicry and the evolutionary process. Special issue: American Naturalist S1—S Based on a symposium organized by Lincoln P.

The symposium was dedicated to E. Ford b. The whole supplement contains six great papers associated with the evolutionary process of mimicry.

Cott, Hugh B. Adaptive coloration in animals. London: Menthuen. This is a great natural history perspective on protective coloration in animals with the mechanistic explanations. Endler, John. Interactions between predators and prey. In Behavioural ecology: An evolutionary Approach. Edited by John R. Krebs and Nick B. Davies, — Cambridge, UK: Blackwell Science. Excellent description of how predators and prey interact. Describes predation as a sequence of events and gives the different mechanisms by which prey have developed defenses to avoid predation.

In cases where the different models occur in the same area and at the same time, then mimics should either center on one of the model phenotypes or some intermediate phenotype if the models themselves are similar to one another. In cases where models occur in distinct areas or at distinct times, there should be selection on mimics that use all of these areas or times to develop an intermediate phenotype.

The optimal intermediate mimic phenotype should more closely resemble the model with which the mimic spends most time, but all else being equal, the mimic should more closely resemble the less noxious and less numerous model. The analysis presented here strongly suggests that mimicry without perfect resemblance will readily evolve in systems containing a single model. Several experiments have indeed found that the relationship between model—mimic similarity and the effectiveness of the mimic is nonlinear e.

Recent work Holloway et al. Of course, one obvious question is what happens once the mimic phenotype reaches a level of similarity with the model beyond which further changes are selectively neutral with respect to predation.

At this point or even before , several additional factors may influence the evolution of the mimic phenotype. For instance, mimics may need to be recognized by mates, which might render an even closer similarity selectively disadvantageous.

Alternatively, mimic phenotype may be influenced to an extent by a need to regulate abdominal and thoracic temperature Holloway et al. As this study highlights, imperfect mimicry will be more likely to persist when the model species is costly to attack and when the mimic species is relatively rare. In support of this, Pilecki and O'Donald showed that neither poor mimics palatable mealworms nor their models experienced high attack rates when the poor mimics were relatively rare.

In contrast, other workers e. The possibility that a mimic species may have several different model species to chose from has been recognized for some time see Mallet and Joron, For example, in southern Florida where unpalatable monarchs are rare, the viceroy resembles the queen see Waldbauer, Similarly, O'Donnel and Joyce reported that the wasp Mischocyttarus mastigophorus was dimorphic and suggested that the morphs resembled two species of swarming wasp in the genus Agelaia , which were locally abundant but at predominantly different elevations.

More recently, Norman et al. The analyses in this study show how such mimetic polymorphism can arise, for instance, if one population of a mimic coexists with one model species and another population coexists with an alternative model species.

However, the analyses also indicate that when the models are similar to one another in appearance such as vespid wasps, perhaps then mimetic polymorphism is unlikely; rather, the mimetic phenotype will tend to have an intermediate form.

Such a jack-of-all-trades mimetic phenotype has only recently been considered as an explanation for imperfect mimicry Edmunds, , and the analyses presented here support the view that such a phenomenon is plausible. As this study shows, intermediate phenotypes are even more likely to arise if the models are separated in space or time, whereas the mimic is not.

Under these conditions, the intermediate mimics should more closely resemble the model with which they coexist for longer but, all else being equal, they should resemble the less noxious and less numerous model. Some of these predictions may well be amenable to experimental testing.

This study focused on quantitatively examining the validity of two important explanations for why imperfect mimicry can persist in natural populations, but there are others. Perhaps more likely, imperfect mimics such as certain species of hoverflies may not be Batesian mimics at all but may be signaling their own unprofitability e.

This is an interesting theory, but it should be noted that some species of hoverflies also engage in behavioral mimicry, for instance by waving their legs to resemble Hymenopteran antennae see Golding and Edmunds, ; Waldbauer, Perhaps more likely, the higher flight speeds of hoverflies might reduce their mean profitability on pusuit b.

Lower b will allow a greater density of mimics at equilibrium and generate a broader range of selectively neutral phenotypes. Alternative explanations for imperfect mimicry that were not identified in Edmunds short summary include the possibility that resemblance does not have to be close when the mimic is so mobile that predators are rarely given a clear view and that there are phylogenetic constraints on optimization that restrict closer resemblance see Gould, Although earlier researchers rightly recognized imperfect mimics as a neglected problem of Batesian mimicry Dittrich et al.

I sincerely thank Professor Malcolm Edmunds for comments on an earlier draft of this paper. Mimicry profiles are affected by human-induced habitat changes. Proc R Soc Lond B : Brower JVZ, Experimental studies of mimicry. The reactions of starlings to different proportions of models and mimics. Am Nat 94 : Mimicry and the eye of the beholder. Imperfect mimicry: a pigeon's perspective. Continuous and quantal theories of sensory discrimination.

Sensory discrimination and its role in the evolution of Batesian mimicry. Behaviour 24 : Edmunds M, Why are there good mimics and poor mimics?

Biol J Linn Soc 70 : Emlen JM, Batesian mimicry: a preliminary theoretical investigation of quantitative aspects. Am Nat : Strategy for a predator encountering a model-mimic system. Fisher RA, The genetical theory of natural selection.

Oxford: Clarendon Press. Getty T, Discriminability and the sigmoid functional response: how optimal foragers could stabilize model-mimic complexes. Crypsis, mimicry, and switching: the basic similarity of superficially different analyses. Golding YC, Edmunds M, Behavioural mimicry of honeybees Apis mellifera by droneflies Diptera: Syrphidae: Eristalis spp.

Proc R Soc B Lond : Goodale MA, Sneddon I, The effect of distastefulness of the model on the predation of artificial Batesian mimics. Anim Behav 25 : Gould SJ, The panda's thumb.

New York: Penguin Books. Greenwood JJD, Crypsis, mimicry, and switching by optimal foragers. The relationship between mimetic imperfection and phenotypic variation in insect colour patterns. Phenotypic plasticity in hoverflies: the relationship between colour pattern and season in Episyrphus balteatus and other Syrphidae.

Ecol Entomol 22 : Dynamics of mimicry evolution. Biol J Linn Soc 66 : Satyric mimicry: the evolution of apparent imperfection. Huheey JE, Studies of warning coloration and mimicry. Examples of cue mimicry in protective mimicry. The body shape of the ant Oecophylla smaragdina A is mimicked by the spider Myrmaplata plataleoides B.

Note that this instance of cue mimicry may not be considered as such under the informational approach Table 1. In addition to signal mimicry, the gait of the beetle Anthia thoracica C is mimicked by the juvenile lizard Heliobolus lugubris D.

Protective mimicry, when a species benefits from reduced predation by mimicking another unprofitable species, is one of the most celebrated examples of evolution by natural selection Bates, ; Cott, ; Quicke, Species engaged in protective mimicry are traditionally defined as mimetic or model species, with the former being the species benefiting the most from mimicry Cott, ; Ruxton et al.

Communication between prey and predators determines the evolution of protective mimicry but, surprisingly, little attention has been given to the evolutionary implication of cues in protective mimicry. In the case of cue mimicry, the same phenotypic trait is a signaling trait in the mimetic species, and a cue in the model species Jamie, In a recent review paper, Jamie proposed a conceptual framework considering the distinction between cues and signals to contrast and order all mimetic resemblances protective mimicry, aggressive mimicry, rewarding mimicry.

We then discuss the evolutionary consequences of this defensive strategy for the evolution of mimetic signals. In nature, protective mimicry is often characterized by some forms of cue mimicry. One of its most striking examples is eyespots mimicry found in a wide variety of insects Stevens, Eyespots usually take the form of a large dark central spot surrounded by a white border, and look like the eyes of large size vertebrates that are predators of the small birds attacking insects.

The evolution of eyespots is determined by differential predation rate in insect mimetic species De Bona et al. As such, eyespots mimicry can be defined as cue mimicry. Another common example of cue mimicry is seen in the mimicry of ants. Ants are involved in many mimetic systems, especially with spiders as mimics, and yet rarely display conspicuous colorations Huang et al. Most ant species can defend themselves mandible, formic acid , making them unprofitable to most predators.

Mimetic species with the same body shape, gait and colorations than the ants benefit from reduced predation Figures 1A,B ; McIver and Stonedahl, ; Nelson and Card, In the ant models, the evolution of these traits is mainly determined by environment and developmental constraints except aposematic conspicuous coloration in some ant species , while it is determined by predator selective pressures in their mimics.

Finally, cue mimicry is also found in plants. Several plant species produce a white trichome that is highly similar to a spider web, and thereby benefit from reduced herbivory Yamazaki and Lev-Yadun, In spider model species, however, the web here recognized as a component of the extended phenotype has evolved through other evolutionary forces than predator avoidance.

Another example of cue mimicry in plants is seen in species emitting the alarm pheromones of their aphid herbivore, thereby reducing herbivory by aphids Gibson and Pickett, In aphids, releasing alarm pheromones does not reduce any death rate caused by other aphid individuals, making this adaptive ressemblance a case of cue mimicry.

Cue mimicry also exists between plant species. Australian mistletoe species benefit from reduced herbivory by mimicking the foliage of their host-tree Barlow and Wiens, ; Burns, Similarly, a vine, Boquila trifoliolata , has the same leave shape as its supporting plant Gianoli and Carrasco-Urra, In both examples, the supporting species is considered as the model because they are little palatable. Here again, the foliage shape of models is probably determined by environment and developmental constraints, rather than herbivory.

All these examples demonstrate that cue mimicry is not anecdotal and may be taxonomically widespread. Cue mimicry can be associated with signal mimicry in the same mimetic system. This is especially the case when model and mimic belong to different guilds and have very different ecology.

For instance, in southern Africa, juveniles of the Heliobolus lugubris lizard species mimic a sympatric and noxious beetle species Figures 1C,D ; Huey and Pianka, The two species have a similar conspicuous coloration, a black coloration with white spots, but the lizard also has the same gait as the beetle, thereby increasing mimetic resemblance. Likewise, some hoverfly species wave their darkened front legs, thereby mimicking the presence and movement of long antennae that are cues in conspicuously colored wasp models Waldbauer, Cue mimicry can also be associated with signal mimicry when model and mimic belong to the same guild.

For instance, some aposematic species of Dilophotes beetles have different conspicuous mimetic signals shared with different model species depending on their sex Motyka et al. In these species, males are smaller than females, and this sexual size dimorphism may have favored the evolution of sexual mimetic dimorphism. In model species, size is probably a cue, the evolution of which is primarily determined by developmental constraints.

In the mimetic Dilophotes species, however, sexual size dimorphism strongly affects predator avoidance and has determined the evolution of different conspicuous mimetic signals in females and males.

This example reveals how model's cues can potentially influence the signaling traits of the mimic, and thus demonstrates the importance of accounting for cues in theories on mimicry evolution. Accounting for cue mimicry may shed light on puzzling patterns observed in mimetic systems. Imperfect mimicry is found in many taxa Vereecken and Schiestl, ; Penney et al. Several hypotheses may explain this paradox Kikuchi and Pfennig, Among those hypotheses, the backup signal hypothesis suggests that a weak resemblance between mimic and model can be compensated by additional backup signals, thereby maintaining imperfect mimicry on other signaling traits Johnstone, Following this backup signal hypothesis, cue mimicry may evolve as a backup to imperfect signal mimicry.

In particular, if mimetic and model species belong to different guilds and show strong phenotypic differences, perfect mimicry may be difficult to evolve and cue mimicry is likely to evolve as a backup to imperfect signal mimicry. Overall, even in mimetic systems involving species from the same guild e. Several hypotheses may explain this phenomenon, like local adaptation Mallet and Gilbert, or heterogeneity in micro-habitat use among species Willmott et al.

Predators use both signaling traits and cues to recognize their prey, so that mimicry based on signaling traits alone may not necessarily deceive predators. Contrary to signaling traits, selective pressure imposed by predation does not favor the evolution of shared cues in the model species.

Such a situation is illustrated by the case of Dilophotes beetles, the evolution of which is compelled by the size of their models Motyka et al. This hypothesis remains to be investigated theoretically, and has received little empirical support so far, probably because of the oversight of cues in the literature on protective mimicry. The literature on aposematism and mimicry has mainly focused on conspicuous signaling traits.

While such focus has allowed for rapid advancement of the field, we may have minimized the implication of cues for the evolution of mimicry.

As illustrated above, protective mimicry can occur without any form of conspicuous signal and, by focusing on conspicuous coloration, we may underestimate the predominance of protective mimicry in natural communities. A rigorous framework should be employed to detect such mimicry based on non-conspicuous traits see de Jager and Anderson, The evolution of mimetic signals involves a wide variety of selective pressures, but also a large variety of traits Rojas et al.

We highlighted here that the same phenotypic trait can be shaped by different selective forces in the different species involved in mimicry. Such distinction could help to disentangle the selective forces shaping the complex evolution of mimicry and may improve our comprehension of this defensive strategy.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We are grateful to P. Crochet and T. Sherratt for comments on earlier versions of the manuscript.

We also thank P. Lev-Yadun, and D. Pfennig for suggestions that improved the paper.