Understanding Mimicry – with Special Reference to Vocal Mimicry

The term mimicry was introduced to biology in 1862 by Henry Walter Bates in his evolutionary explanation of deceptive communication in nature, based on a three‐part interaction system of a mimicked organism or object (called model), a mimicking organism (called mimic), and one or more organisms as selecting agents. Bates gave two incongruous definitions of mimicry: one from the viewpoint of a natural agent that selects for, and in consequence is deceived by, the close resemblance of a toxic model's warning signal and the similar appearance of a palatable mimic, and another one from the viewpoint of a human taxonomist who under an evolutionary aspect focuses on convergent resemblance between model and mimic. Later definitions of Müllerian (F. Müller), arithmetic (A. Wallace) and social (M. Moynihan) mimicry abolish deception in the natural selecting agent, rely on the convergence criterion alone, fuse the roles of model and mimic but have to accept a mix of homologous and convergent resemblance amongst them for a functional explanation. The definition of vocal mimicry (E. Armstrong) refers to a learned resemblance between mimic and heterospecific model by character duplication (no convergence), so far without known (deceived or not deceived) natural selecting agents. It excludes Batesian vocal mimicry. The functional ethological understanding of mimicry as a tripartite communication system (W. Wickler) is consistent with Bates' concept and accepts deception as key element of Batesian mimicry beyond homologous and convergent resemblances. Deception is seen as caused by the divergence between a sign and its meaning for the natural selecting agent. This understanding covers mimicry in all behaviour domains, provides a generally applicable definition of mimic and model so far missing in any mimicry concept, and it distinguishes – still in line with Henry Bates – cultural from genetically determined model‐mimic‐resemblance; this applies to vocal mimicry in particular. Convergently evolved model‐mimic‐resemblance, not essential in Batesian mimicry but mandatory for its alternatives, marks a fundamental distinction between Batesian mimicry (including Mimesis) and all other conceptualized mimicries and accounts for the non‐existence of a unified meaning of the term mimicry. However, character convergence does not help to explain the mere existence of mimicry phenomena and is irrelevant for their permanence in nature. I therefore propose to remove the convergence argument from any mimicry definition.     

The evolution of mimicry under constraints

The resemblance between mimetic organisms and their models varies from near perfect to very crude. One possible explanation, which has received surprisingly little attention, is that evolution can improve mimicry only at some cost to the mimetic organism. In this article, an evolutionary game theory model of mimicry is presented that incorporates such constraints. The model generates novel and testable predictions. First, Batesian mimics that are very common and/or mimic very weakly defended models should evolve either inaccurate mimicry (by stabilizing selection) or mimetic polymorphism. Second, Batesian mimics that are very common and/or mimic very weakly defended models are more likely to evolve mimetic polymorphism if they encounter predators at high rates and/or are bad at evading predator attacks. The model also examines how cognitive constraints acting on signal receivers may help determine evolutionarily stable levels of mimicry. Surprisingly, improved discrimination abilities among signal receivers may sometimes select for less accurate mimicry.     

Feature saltation and the evolution of mimicry

In Batesian mimicry, a harmless prey species imitates the warning coloration of an unpalatable model species. A traditional suggestion is that mimicry evolves in a two-step process, in which a large mutation first achieves approximate similarity to the model, after which smaller changes improve the likeness. However, it is not known which aspects of predator psychology cause the initial mutant to be perceived by predators as being similar to the model, leaving open the question of how the crucial first step of mimicry evolution occurs. Using theoretical evolutionary simulations and reconstruction of examples of mimicry evolution, we show that the evolution of Batesian mimicry can be initiated by a mutation that causes prey to acquire a trait that is used by predators as a feature to categorize potential prey as unsuitable. The theory that species gain entry to mimicry through feature saltation allows us to formulate scenarios of the sequence of events during mimicry evolution and to reconstruct an initial mimetic appearance for important examples of Batesian mimicry. Because feature-based categorization by predators entails a qualitative distinction between nonmimics and passable mimics, the theory can explain the occurrence of imperfect mimicry.     

Imperfect Batesian mimicry—the effects of the frequency and the distastefulness of the model

Batesian mimicry is the resemblance between unpalatable models and palatable mimics. The widely accepted idea is that the frequency and the unprofitability of the model are crucial for the introduction of a Batesian mimic into the prey population. However, experimental evidence is limited and furthermore, previous studies have considered mainly perfect mimicry (automimicry). We investigated imperfect Batesian mimicry by varying the frequency of an aposematic model at two levels of distastefulness. The predator encountered prey in a random order, one prey item at a time. The prey were thus presented realistically in a sequential way. Great tits (Parus major) were used as predators. This experiment, with a novel signal, supports the idea that Batesian mimics gain most when the models outnumber them. The mortalities of the mimics as well as the models were significantly dependent on the frequency of the model. Both prey types survived better the fewer mimics there were confusing the predator. There were also indications that the degree of distastefulness of the model had an effect on the survival of the Batesian mimic: the models survived significantly better the more distasteful they were. The experiment supports the most classical predictions in the theories of the origin and maintenance of Batesian mimicry.     

Alternative prey can change model–mimic dynamics between parasitism and mutualism

Classical (conventional) Müllerian mimicry theory predicts that two (or more) defended prey sharing the same signal always benefit each other despite the fact that one species can be more toxic than the other. The quasi‐Batesian (unconventional) mimicry theory, instead, predicts that the less defended partner of the mimetic relationship may act as a parasite of the signal, causing a fitness loss to the model. Here we clarify the conditions for parasitic or mutualistic relationships between aposematic prey, and build a model to examine the hypothesis that the availability of alternative prey is crucial to Müllerian and quasi‐Batesian mimicry. Our model is based on optimal behaviour of the predator. We ask if and when it is in the interest of the predator to learn to avoid certain species as prey when there is alternative (cryptic) prey available. Our model clearly shows that the role of alternative prey must be taken into consideration when studying model–mimic dynamics. When food is scarce it pays for the predator to test the models and mimics, whereas if food is abundant predators should leave the mimics and models untouched even if the mimics are quite edible. Dynamics of the mimicry tend to be classically Müllerian if mimics are well defended, while quasi‐Batesian dynamics are more likely when they are relatively edible. However, there is significant overlap: in extreme cases mimics can be harmful to models (a quasi‐Batesian case) even if the species are equally toxic. A crucial parameter explaining this overlap is the search efficiency with which indiscriminating vs. discriminating predators find cryptic prey. Quasi‐Batesian mimicry becomes much more likely if discrimination increases the efficiency with which the specialized predator finds cryptic prey, while the opposite case tends to predict Müllerian mimicry. Our model shows that both mutualistic and parasitic relationship between model and mimic are possible and the availability of alternative prey can easily alter this relationship.     

A test of fundamental questions in mimicry theory using long‐term datasets

Since the phenomenon of mimicry was first described by Bates in 1862 it has become one of the foundational examples of adaptive evolution. Numerous subcategories of mimicry and dozens of hypotheses pertaining to its evolution and maintenance have been proposed. Many of these hypotheses, however, are difficult to test in experimental settings, and data from natural observations are often inadequate. Here we use data from a long‐term survey of butterfly presence and abundance to test several hypotheses pertaining to Batesian and female‐limited polymorphic mimicry (FPM; a special case of Batesian mimicry). We found strong evidence that models outnumber mimics in both mimicry systems, but no evidence for an increase in relative abundance of FPM mimics to their Batesian counterparts. Tests of the early‐emergence/model first hypothesis showed strong evidence that the Batesian mimic routinely emerges after the model, while emergence timing in the FPM system was site specific, suggesting that other ecological factors are at play. These results demonstrate the importance of long‐term field observations for testing evolutionary and ecological hypotheses.     

Testing the adaptive hypothesis of Batesian mimicry among hybridizing North American admiral butterflies

Batesian mimicry is characterized by phenotypic convergence between an unpalatable model and a palatable mimic. However, because convergent evolution may arise via alternative evolutionary mechanisms, putative examples of Batesian mimicry must be rigorously tested. Here, we used artificial butterfly facsimiles (N = 4000) to test the prediction that (1) palatable Limenitis lorquini butterflies should experience reduced predation when in sympatry with their putative model, Adelpha californica, (2) protection from predation on L. lorquini should erode outside of the geographical range of the model, and (3) mimetic color pattern traits are more variable in allopatry, consistent with relaxed selection for mimicry. We find support for these predictions, implying that this convergence is the result of selection for Batesian mimicry. Additionally, we conducted mark–recapture studies to examine the effect of mimicry and found that mimics survive significantly longer at sites where the model is abundant. Finally, in contrast to theoretical predictions, we found evidence that the Batesian model (A. californica) is protected from predation outside of its geographic range. We discuss these results considering the ongoing hybridization between L. lorquini and its sister species, L. weidemeyerii, and growing evidence that selection for mimicry predictably leads to a reduction in gene flow between nascent species.     

The effect of alternative prey on the dynamics of imperfect Batesian and Müllerian mimicries

Both Batesian and Müllerian mimicries are considered classical evidence of natural selection where predation pressure has, at times, created a striking similarity between unrelated prey species. Batesian mimicry, in which palatable mimics resemble unpalatable aposematic species, is parasitic and only beneficial to the mimics. By contrast, in classical Müllerian mimicry the cost of predators' avoidance learning is shared between similar unpalatable co-mimics, and therefore mimicry benefits all parties. Recent studies using mathematical modeling have questioned the dynamics of Müllerian mimicry, suggesting that fitness benefits should be calculated in a way similar to Batesian mimicry; that is, according to the relative unpalatability difference between co-mimics. Batesian mimicry is very sensitive to the availability of alternative prey, but the effects of alternative prey for Müllerian dynamics are not known and experiments are rare. We designed two experiments to test the effect of alternative prey on imperfect Batesian and Müllerian mimicry complexes. When alternative prey were scarce, imperfect Batesian mimics were selected out from the population, but abundantly available alternative prey relaxed selection against imperfect mimics. Birds learned to avoid both Müllerian models and mimics irrespective of the availability of alternative prey. However, the rate of avoidance learning of models increased when alternative prey were abundant. This experiment suggests that the availability of alternative prey affects the dynamics of both Müllerian and Batesian mimicry, but in different ways.     

PREDATOR PERCEPTION OF BATESIAN MIMICRY AND CONSPICUOUSNESS IN A SALAMANDER

In Batesian mimicry a palatable mimic deceives predators by resembling an unpalatable model. The evolution of Batesian mimicry relies on the visual capabilities of the potential predators, as prey detection provides the selective force driving evolutionary change. We compared the visual capabilities of several potential predators to test predictions stemming from the hypothesis of Batesian mimicry between two salamanders: the model species Notophthalmus viridescens, and polymorphic mimic, Plethodon cinereus. First, we found mimicry to be restricted to coloration, but not brightness. Second, only bird predators appeared able to discriminate between the colors of models and nonmimic P. cinereus. Third, estimates of salamander conspicuousness were background dependent, corresponding to predictions only for backgrounds against which salamanders are most active. These results support the hypothesis that birds influence the evolution of Batesian mimicry in P. cinereus, as they are the only group examined capable of differentiating N. viridescens and nonmimetic P. cinereus. Additionally, patterns of conspicuousness suggest that selection from predators may drive the evolution of conspicuousness in this system. This study confirms the expectation that the visual abilities of predators may influence the evolution of Batesian mimicry, but the role of conspicuousness may be more complex than previously thought.     

Distance-dependent costs and benefits of aggressive mimicry in a cleaning symbiosis

In aggressive mimicry, a 'predatory' species resembles a model that is harmless or beneficial to a third species, the 'dupe'. We tested critical predictions of Batesian mimicry models, i.e. that benefits of mimicry to mimics and costs of mimicry to models should be experienced only when model and mimic co-occur, in an aggressive mimicry system involving juvenile bluestreaked cleaner wrasse (Labroides dimidiatus) as models and bluestriped fangblennies (Plagiotremus rhinorhynchos) as mimics. Cleanerfish mimics encountered nearly twice as many potential victims and had higher striking rates when in proximity to than when away from the model. Conversely, in the presence of mimics, juvenile cleaner wrasses were visited by fewer clients and spent significantly less time foraging. The benefits to mimic and costs to model thus depend on a close spatial association between model and mimic. Batesian mimicry theory may therefore provide a useful initial framework to understand aggressive mimicry.     

Is inaccurate mimicry ancestral to accurate in myrmecomorphic spiders (Araneae)?

Batesian mimicry, in which a palatable organism resembles an unpalatable model, is widespread among taxa. Batesian mimics can be classified based on their level of accuracy (inaccurate or accurate). Using data on defensive strategies in more than 1000 species of spiders I investigated whether inaccurate myrmecomorphy is ancestral to accurate myrmecomorphy. I classified 233 myrmecomorphic species into four accuracy levels based on morphology, from poor inaccurate mimics to very accurate ones. I found that myrmecomorphy has evolved independently in 16 families and 85 genera. On the family‐level phylogeny, the occurrence of myrmecomorphy is confined mainly to families branching later on the tree, from the RTA clade. On the generic‐level phylogenies in Corinnidae and Salticidae, myrmecomorphy is not only of derived origin. Estimated ancestral state was non‐mimetic in Salticidae and poor inaccurate myrmecomorphy in Corinnidae. Thus, inaccurate myrmecomorphic spider mimics seem rather ancestral to accurate but additional analysis on species‐level phylogenies is needed to support this conclusion. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 97–111.     

Dorsal Forewing White Spots of Male <Emphasis Type="Italic">Papilio polytes</Emphasis>(Lepidoptera: Papilionidae) not Maintained by Female Mate Choice

Palatable animals sometimes mimic the color patterns of noxious animals to gain protection from predators. This phenomenon, known as Batesian mimicry, is seen in many butterflies of the genus Papilio, and in some species the mimicry is limited to females. Although female-limited Batesian mimicry has been hypothesized to be caused by females preferring to mate with non-mimetic males, this hypothesis is rarely tested. In this study, we tested whether female mate choice is driving female-limited Batesian mimicry in Papilio polytes. Males have white spots on the dorsal forewings, which are absent in mimetic female sand in the toxic model, Pachliopta aristolochiae. Hence, we conducted mate choice experiments to examine whether these white spots are important to females. We offered females a choice of males with intact dorsal forewing white spots and males with artificially blackened dorsal forewings, resembling the model. Females did not show a preference for males with the white spots, suggesting that they are not being maintained by female mate choice. Future studies should investigate the presence of female mate choice on other parts of males’ wings to further understand the role of female mate choice, as well as explore other factors driving female-limited mimicry in these butterflies.     

Batesian mimicry promotes pre‐ and postmating isolation in a snake mimicry complex

We evaluated whether Batesian mimicry promotes early‐stage reproductive isolation. Many Batesian mimics occur not only in sympatry with their model (as expected), but also in allopatry. As a consequence of local adaptation within both sympatry (where mimetic traits are favored) and allopatry (where nonmimetic traits are favored), divergent, predator‐mediated natural selection should disfavor immigrants between these selective environments as well as any between‐environment hybrids. This selection might form the basis for both pre‐ and postmating isolation, respectively. We tested for such selection in a snake mimicry complex by placing clay replicas of sympatric, allopatric, or hybrid phenotypes in both sympatry and allopatry and measuring predation attempts. As predicted, replicas with immigrant phenotypes were disfavored in both selective environments. Replicas with hybrid phenotypes were also disfavored, but only in a region of sympatry where previous studies have detected strong selection favoring precise mimicry. By fostering immigrant inviability and ecologically dependent selection against hybrids (at least in some habitats), Batesian mimicry might therefore promote reproductive isolation. Thus, although Batesian mimicry has long been viewed as a mechanism for convergent evolution, it might play an underappreciated role in fueling divergent evolution and possibly even the evolution of reproductive isolation and speciation.     

Population genetic structure and evolution of Batesian mimicry in Papilio polytes from the Ryukyu Islands,Japan, analyzed by genotyping‐by‐sequencing

Batesian mimicry is a striking example of Darwinian evolution, in which a mimetic species resembles toxic or unpalatable model species, thereby receiving protection from predators. In some species exhibiting Batesian mimicry, nonmimetic individuals coexist as polymorphism in the same population despite the benefits of mimicry. In a previous study, we proposed that the abundance of mimics is limited by that of the models, leading to polymorphic Batesian mimicry in the swallowtail butterfly, Papilio polytes, on the Ryukyu Islands in Japan. We found that their mimic ratios (MRs), which varied among the Islands, were explained by the model abundance of each habitat, rather than isolation by distance or phylogenetic constraint based on the mitochondrial DNA (mtDNA) analysis. In the present study, this possibility was reexamined based on hundreds of nuclear single nucleotide polymorphisms (SNPs) of 93 P. polytes individuals from five Islands of the Ryukyus. We found that the population genetic and phylogenetic structures of P. polytes largely corresponded to the geographic arrangement of the habitat Islands, and the genetic distances among island populations show significant correlation with the geographic distances, which was not evident by the mtDNA‐based analysis. A partial Mantel test controlling for the present SNP‐based genetic distances revealed that the MRs of P. polytes were strongly correlated with the model abundance of each island, implying that negative frequency‐dependent selection interacting with model species shaped and maintained the mimetic polymorphism. Taken together, our results support the possibility that predation pressure, not isolation by distance or other neutral factors, is a major driving force of evolution of the Batesian mimicry in P. polytes from the Ryukyus.     

A single origin of Batesian mimicry among hybridizing populations of admiral butterflies (Limenitis arthemis) rejects an evolutionary reversion to the ancestral phenotype

Batesian mimicry is a fundamental example of adaptive phenotypic evolution driven by strong natural selection. Given the potentially dramatic impacts of selection on individual fitness, it is important to understand the conditions under which mimicry is maintained versus lost. Although much empirical and theoretical work has been devoted to the maintenance of Batesian mimicry, there are no conclusive examples of its loss in natural populations. Recently, it has been proposed that non-mimetic populations of the polytypic Limenitis arthemis species complex represent an evolutionary loss of Batesian mimicry, and a reversion to the ancestral phenotype. Here, we evaluate this conclusion using segregating amplified fragment length polymorphism markers to investigate the history and fate of mimicry among forms of the L. arthemis complex and closely related Nearctic Limenitis species. In contrast to the previous finding, our results support a single origin of mimicry within the L. arthemis complex and the retention of the ancestral white-banded form in non-mimetic populations. Our finding is based on a genome-wide sampling approach to phylogeny reconstruction that highlights the challenges associated with inferring the evolutionary relationships among recently diverged species or populations (i.e. incomplete lineage sorting, introgressive hybridization and/or selection).     

New case of true mimicry in cockroaches (Blattodea)

True mimicry is an extremely rare phenomenon in cockroaches, with beetles as their favorite models. So far, only very few Pseudophyllodromiinae could be identified that conform to all requirements for Batesian mimicry and similarly exist only isolated reports on Müllerian mimicry. The vast majority, however, of the so‐called beetle‐mimicking cockroaches only shows a high degree of generalized convergence regarding their outer appearance. Specific models or counterparts, respectively, are lacking. Here we report on a last instar nymph of an undescribed Blattinae (Blattodea: Blattidae) that accurately mimics a truly harmful, sympatric carabid beetle. Although no indications for inedibility of this cockroach became evident, thus making Batesian mimicry likely, Müllerian mimicry can not be excluded with certainty. At any rate, this represents both the first case of mimicry in Blattidae and the first case with a ground beetle (Carabidae) as model for a cockroach mimic.     

Evasive mimicry: when (if ever) could mimicry based on difficulty of capture evolve?

We elucidate the conditions under which an easy-to-catch edible prey species may evolve to resemble another edible species that is much more difficult to capture ('evasive Batesian mimicry'), and the conditions under which two or more edible but hard-to-catch species evolve a common resemblance ('evasive Mullerian mimicry'). Using two complementary mathematical models, we argue that both phenomena are logically possible but that several factors will limit the prevalence of these forms of mimicry in nature. Evasive Batesian mimicry is most likely to arise when it is costly in time or energy for the predator species to pursue evasive prey, when mimics are encountered less frequently than evasive models and where there are abundant alternative prey. Evasive Mullerian mimicry, by contrast, is most likely to arise when evasive prey species differ in abundance, predators are slow to learn to avoid evasive prey and evading capture is costly to the prey. Unequivocal evidence for evasive Batesian or Mullerian mimicry has not yet been demonstrated in the field, and we argue that more empirical work is needed to test whether putative examples are indeed a result of selection to signal difficulty of capture.     

Ecological and Evolutionary Processes Drive the Origin and Maintenance of Imperfect Mimicry

Although the forces behind the evolution of imperfect mimicry remain poorly studied, recent hypotheses suggest that relaxed selection on small-bodied individuals leads to imperfect mimicry. While evolutionary history undoubtedly affects the development of imperfect mimicry, ecological community context has largely been ignored and may be an important driver of imperfect mimicry. Here we investigate how evolutionary and ecological contexts might influence mimetic fidelity in Müllerian and Batesian mimicry systems. In Batesian hoverfly systems we find that body size is not a strong predictor of mimetic fidelity. However, in Müllerian velvet ants we find a weak positive relationship between body size and mimetic fidelity when evolutionary context is controlled for and a much stronger relationship between community diversity and mimetic fidelity. These results suggest that reduced selection on small-bodied individuals may not be a major driver of the evolution of imperfect mimicry and that other factors, such as ecological community context, should be considered when studying the evolution of imperfect mimicry.     

Multitrait aposematic signal in Batesian mimicry

Batesian mimics can parasitize Müllerian mimicry rings mimicking the warning color signal. The evolutionary success of Batesian mimics can increase adding complexity to the signal by behavioral and locomotor mimicry. We investigated three fundamental morphological and locomotor traits in a Neotropical mimicry ring based on Ithomiini butterflies and parasitized by Polythoridae damselflies: wing color, wing shape, and flight style. The study species have wings with a subapical white patch, considered the aposematic signal, and a more apical black patch. The main predators are VS‐birds, visually more sensitive to violet than to ultraviolet wavelengths (UVS‐birds). The white patches, compared to the black patches, were closer in the bird color space, with higher overlap for VS‐birds than for UVS‐birds. Using a discriminability index for bird vision, the white patches were more similar between the mimics and the model than the black patches. The wing shape of the mimics was closer to the model in the morphospace, compared to other outgroup damselflies. The wing‐beat frequency was similar among mimics and the model, and different from another outgroup damselfly. Multitrait aposematic signals involving morphology and locomotion may favor the evolution of mimicry rings and the success of Batesian mimics by improving signal effectiveness toward predators.     

Newly emerged Batesian mimicry protects only unfamiliar prey

The evolution of Batesian mimicry was tested experimentally using avian predators. We investigated the effect of a search image on the protection effectiveness of a newly emerged Batesian mimic. The two groups of predators (adult great tits, Parus major) differed in prior experience with prey from which the mimic evolved. The Guyana spotted roach (Blaptica dubia) was used as a palatable prey from which the mimic emerged, and red firebug (Pyrrhocoris apterus) was used as a model. Optical signalization of the insect prey was modified by a paper sticker placed on its back. The cockroaches with the firebug pattern sticker were significantly better protected against tits with no prior experience with cockroaches. The protection of the firebug sticker was equally effective on cockroaches as it was on firebugs. The cockroaches with firebug stickers were not protected against attacks of tits, which were familiar with unmodified cockroaches better than cockroaches with a cockroach sticker. We suppose that pre-trained tits acquired the search image of a cockroach, which helped them to reveal the “fake” Batesian mimic. Such a constraint of Batesian mimicry effectiveness could substantially decrease the probability of evolution of pure Batesian mimic systems.