Batesian mimics influence the evolution of conspicuousness in an aposematic salamander

Conspicuousness, or having high contrast relative to the surrounding background, is a common feature of unpalatable species. Several hypotheses have been proposed to explain the occurrence of conspicuousness, and while most involve the role of conspicuousness as a direct signal of unpalatability to potential predators, one hypothesis suggests that exaggerated conspicuousness may evolve in unpalatable species to reduce predator confusion with palatable species (potential Batesian mimics). This hypothesis of antagonistic coevolution between palatable and unpalatable species hinges on the ‘cost of conspicuousness’, in which conspicuousness increases the likelihood of predation more in palatable species than in unpalatable species. Under this mimicry scenario, four patterns are expected: (i) mimics will more closely resemble local models than models from other localities, (ii) there will be a positive relationship between mimic and model conspicuousness, (iii) models will be more conspicuous in the presence of mimics, and (iv) when models and mimics differ in conspicuousness, mimics will be less conspicuous than models. We tested these predictions in the salamander mimicry system involving Notophthalmus viridescens (model) and one colour morph of Plethodon cinereus (mimic). All predictions were supported, indicating that selection for Batesian mimicry not only influences the evolution of mimics, but also the evolution of the models they resemble. These findings indicate that mimicry plays a large role in the evolution of model warning signals, particularly influencing the evolution of conspicuousness.     

DOES THE ABUNDANCE OF HOVERFLY (SYRPHIDAE) MIMICS DEPEND ON THE NUMBERS OF THEIR HYMENOPTERAN MODELS?

We tested the prediction that, if hoverflies are Batesian mimics, this may extend to behavioral mimicry such that their numerical abundance at each hour of the day (the daily activity pattern) is related to the numbers of their hymenopteran models. After accounting for site, season, microclimatic responses, and general hoverfly abundance at three sites in northwestern England, the residual numbers of mimics were significantly correlated positively with their models nine times of 17. Sixteen of 17 relationships were positive, itself a highly significant nonrandom pattern. Several eristaline flies showed significant relationships with honeybees even though some of them mimic wasps or bumblebees, perhaps reflecting an ancestral resemblance to honeybees. There was no evidence that good and poor mimics differed in their daily activity pattern relationships with models. However, the common mimics showed significant activity pattern relationships with their models, whereas the rarer mimics did not. We conclude that many hoverflies show behavioral mimicry of their hymenopteran models.     

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.     

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.     

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.     

Natural selection in mimicry

Biological mimicry has served as a salient example of natural selection for over a century, providing us with a dazzling array of very different examples across many unrelated taxa. We provide a conceptual framework that brings together apparently disparate examples of mimicry in a single model for the purpose of comparing how natural selection affects models, mimics and signal receivers across different interactions. We first analyse how model–mimic resemblance likely affects the fitness of models, mimics and receivers across diverse examples. These include classic Batesian and Müllerian butterfly systems, nectarless orchids that mimic Hymenoptera or nectar‐producing plants, caterpillars that mimic inert objects unlikely to be perceived as food, plants that mimic abiotic objects like carrion or dung and aggressive mimicry where predators mimic food items of their own prey. From this, we construct a conceptual framework of the selective forces that form the basis of all mimetic interactions. These interactions between models, mimics and receivers may follow four possible evolutionary pathways in terms of the direction of selection resulting from model–mimic resemblance. Two of these pathways correspond to the selective pressures associated with what is widely regarded as Batesian and Müllerian mimicry. The other two pathways suggest mimetic interactions underpinned by distinct selective pressures that have largely remained unrecognized. Each pathway is characterized by theoretical differences in how model–mimic resemblance influences the direction of selection acting on mimics, models and signal receivers, and the potential for consequent (co)evolutionary relationships between these three protagonists. The final part of this review describes how selective forces generated through model–mimic resemblance can be opposed by the basic ecology of interacting organisms and how those forces may affect the symmetry, strength and likelihood of (co)evolution between the three protagonists within the confines of the four broad evolutionary possibilities. We provide a clear and pragmatic visualization of selection pressures that portrays how different mimicry types may evolve. This conceptual framework provides clarity on how different selective forces acting on mimics, models and receivers are likely to interact and ultimately shape the evolutionary pathways taken by mimetic interactions, as well as the constraints inherent within these interactions.     

Model toxin level does not directly influence the evolution of mimicry in the salamander <Emphasis Type="Italic">Plethodon cinereus</Emphasis>

The resemblance between palatable mimics and unpalatable models in Batesian mimicry systems is tempered by many factors, including the toxicity of the model species. Model toxicity is thought to influence both the occurrence of mimicry and the evolution of mimetic phenotypes, such that mimicry is most likely to persist when models are particularly toxic. Additionally, model toxicity may influence the evolution of mimetic phenotype by allowing inaccurate mimicry to evolve through a mechanism termed ‘relaxed selection’. We tested these hypotheses in a salamander mimicry system between the model Notophthalmus viridescens and the mimic Plethodon cinereus, in which N. viridescens toxicity takes the form of tetrodotoxin. Surprisingly, though we discovered geographic variation in model toxin level, we found no support for the hypotheses that model toxicity directly influences either the occurrence of mimicry or the evolution of mimic phenotype. Instead, a link between N. viridescens size and toxicity may indirectly lead to relaxed selection in this mimicry system. Additionally, limitations of predator perception or variation in the rate of phenotypic evolution of models and mimics may account for the evolution of imperfect mimicry in this salamander species. Finally, variation in predator communities among localities or modern changes in environmental conditions may contribute to the patchy occurrence of mimicry in P. cinereus.     

Aggressive mimics profit from a model-signal receiver mutualism

Mimetic species have evolved to resemble other species to avoid predation (protective mimicry) or gain access to food (aggressive mimicry). Mimicry systems are frequently tripartite interactions involving a mimic, model and 'signal receiver'. Changes in the strength of the relationship between model and signal receiver, owing to shifting environmental conditions, for example, can affect the success of mimics in protective mimicry systems. Here, we show that an experimentally induced shift in the strength of the relationship between a model (bluestreak cleaner fish, Labroides dimidiatus) and a signal receiver (staghorn damselfish, Amblyglyphidodon curacao) resulted in increased foraging success for an aggressive mimic (bluestriped fangblenny, Plagiotremus rhinorhynchos). When the parasite loads of staghorn damselfish clients were experimentally increased, the attack success of bluestriped fangblenny on damselfish also increased. Enhanced mimic success appeared to be due to relaxation of vigilance by parasitized clients, which sought cleaners more eagerly and had lower overall aggression levels. Signal receivers may therefore be more tolerant of and/or more vulnerable to attacks from aggressive mimics when the net benefit of interacting with their models is high. Changes in environmental conditions that cause shifts in the net benefits accrued by models and signal receivers may have important implications for the persistence of aggressive mimicry systems.     

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.     

Why are there so many mimicry rings? Correlations between habitat,behaviour and mimicry in Heliconius butterflies

In the new world tropics there is an extravagant array of sympatric butterfly mimicry rings. This is puzzling under strictly coevolutionary (Müllerian) mimicry: all unpalatable species should converge as ‘co-mimics' to the same pattern. If mimicry has usually evolved in unpalatable species by one-sided (Batesian) evolution, however, it is easy to see that mimicry rings centred on different models could remain distinct. If mimicry rings were also segregated by habitat, a diversity of mimicry rings could be stabilized. In this paper we report correlations between behaviour and mimicry of nine unpalatable Heliconius species. It is already known that co-mimics fly in similar habitats, and non-mimics fly in different habitats, although there is much overlap. Contrary to a previous report, we find little difference in flight heights of heliconiine mimicry rings; all species fly from ground level to the canopy. However, co-mimics roost at night in similar habitats and at similar heights above the ground, but in different habitats and at different heights from species in other mimicry rings. Heliconius (especially the erato taxonomic group) are renowned for roosting gregariously; and co-mimics roost gregariously with each other more often than with non-mimics. Gregarious roosting is therefore common between species, as well as within species. There are thus strong links between mimicry and behavioural ecology in Heliconius. The paradoxical correlation between nocturnal roosting and visual mimicry is presumably explained by bird predation at dusk when roosts are forming, or at dawn before they have disbanded. Direct evidence of predation is lacking, but there are high rates of disturbance by birds at these times. These results, together with knowledge of the phylogeny of Heliconius, suggest that species from the melpomene-group of Heliconius have radiated to occupy mimetic niches protected by model species in the Ithomiinae and the erato-group of Heliconius. A variety of sympatric mimicry rings is apparently maintained because key models fail to converge, while more rapidly-evolving unpalatable mimics evolve towards the colour patterns of the models. The maintenance of mimetic diversity would be aided by the habitat and behavioural differences between mimicry rings revealed here, provided that different predators are found in different habitats. This explanation for the maintenance of multiple mimicry rings is more plausible for Heliconius mimicry than alternatives based on visual mating constraints, thermal ecology, or camouflage.     

Similar yet different: differential response of a praying mantis to ant‐mimicking spiders

Batesian mimics typically dupe visual predators by resembling noxious or deadly model species. Ants are unpalatable and dangerous to many arthropod taxa, and are popular invertebrate models in mimicry studies. Ant mimicry by spiders, especially jumping spiders, has been studied and researchers have examined whether visual predators can distinguish between the ant model, spider mimic and spider non‐mimics. Tropical habitats harbour a diverse community of ants, their mimics and predators. In one such tripartite mimicry system, we investigated the response of an invertebrate visual predator, the ant‐mimicking praying mantis (Euantissa pulchra), to two related ant‐mimicking spider prey of the genus Myrmarachne, each closely mimicking its model ant species. We found that weaver ants (Oecophylla smaragdina) were much more aggressive than carpenter ants (Camponotus sericeus) towards the mantis. Additionally, mantids exhibited the same aversive response towards ants and their mimics. More importantly, mantids approached carpenter ant‐mimicking spiders significantly more than often that they approached weaver ant‐mimicking spiders. Thus, in this study, we show that an invertebrate predator, the praying mantis, can indeed discriminate between two closely related mimetic prey. The exact mechanism of the discrimination remains to be tested, but it is likely to depend on the level of mimetic accuracy by the spiders and on the aggressiveness of the ant model organism.     

Frequency-dependent variation in mimetic fidelity in an intraspecific mimicry system

Contemporary theory predicts that the degree of mimetic similarity of mimics towards their model should increase as the mimic/model ratio increases. Thus, when the mimic/model ratio is high, then the mimic has to resemble the model very closely to still gain protection from the signal receiver. To date, empirical evidence of this effect is limited to a single example where mimicry occurs between species. Here, for the first time, we test whether mimetic fidelity varies with mimic/model ratios in an intraspecific mimicry system, in which signal receivers are the same species as the mimics and models. To this end, we studied a polymorphic damselfly with a single male phenotype and two female morphs, in which one morph resembles the male phenotype while the other does not. Phenotypic similarity of males to both female morphs was quantified using morphometric data for multiple populations with varying mimic/model ratios repeated over a 3 year period. Our results demonstrate that male-like females were overall closer in size to males than the other female morph. Furthermore, the extent of morphological similarity between male-like females and males, measured as Mahalanobis distances, was frequency-dependent in the direction predicted. Hence, this study provides direct quantitative support for the prediction that the mimetic similarity of mimics to their models increases as the mimic/model ratio increases. We suggest that the phenomenon may be widespread in a range of mimicry systems.     

Diversity of warning signal and social interaction influences the evolution of imperfect mimicry

Mimicry, the resemblance of one species by another, is a complex phenomenon where the mimic (Batesian mimicry) or the model and the mimic (Mullerian mimicry) gain an advantage from this phenotypic convergence. Despite the expectation that mimics should closely resemble their models, many mimetic species appear to be poor mimics. This is particularly apparent in some systems in which there are multiple available models. However, the influence of model pattern diversity on the evolution of mimetic systems remains poorly understood. We tested whether the number of model patterns a predator learns to associate with a negative consequence affects their willingness to try imperfect, novel patterns. We exposed week‐old chickens to coral snake (Micrurus) color patterns representative of three South American areas that differ in model pattern richness, and then tested their response to the putative imperfect mimetic pattern of a widespread species of harmless colubrid snake (Oxyrhopus rhombifer) in different social contexts. Our results indicate that chicks have a great hesitation to attack when individually exposed to high model pattern diversity and a greater hesitation to attack when exposed as a group to low model pattern diversity. Individuals with a fast growth trajectory (measured by morphological traits) were also less reluctant to attack. We suggest that the evolution of new patterns could be favored by social learning in areas of low pattern diversity, while individual learning can reduce predation pressure on recently evolved mimics in areas of high model diversity. Our results could aid the development of ecological predictions about the evolution of imperfect mimicry and mimicry in general.     

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.     

Dynamics of the evolution of Batesian mimicry: molecular phylogenetic analysis of ant-mimicking Myrmarachne (Araneae: Salticidae) species and their ant models

Batesian mimicry is seen as an example of evolution by natural selection, with predation as the main driving force. The mimic is under selective pressure to resemble its model, whereas it is disadvantageous for the model to be associated with the palatable mimic. In consequence one might expect there to be an evolutionary arms race, similar to the one involving host-parasite coevolution. In this study, the evolutionary dynamics of a Batesian mimicry system of model ants and ant-mimicking salticids is investigated by comparing the phylogenies of the two groups. Although Batesian mimics are expected to coevolve with their models, we found the phylogenetic patterns of the models and the mimics to be indicative of adaptive radiation by the mimic rather than co-speciation between the mimic and the model. This shows that there is strong selection pressure on Myrmarachne, leading to a high degree of polymorphism. There is also evidence of sympatric speciation in Myrmarachne, the reproductive isolation possibly driven by female mate choice in polymorphic species.     

Batesian mimics influence mimicry ring evolution

Mathematical models of mimicry typically involve artificial prey species with fixed colorations or appearances; this enables a comparison of predation rates to demonstrate the level of protection a mimic might be afforded. Fruitful theoretical results have been produced using this method, but it is also useful to examine the possible evolutionary consequences of mimicry. To that end, we present individual-based evolutionary simulation models where prey colorations are free to evolve. We use the models to examine the effect of Batesian mimics on Müllerian mimics and mimicry rings. Results show that Batesian mimics can potentially incite Müllerian mimicry relationships and encourage mimicry ring convergence.     

The effects of floral mimics and models on each others' fitness

Plants that lack floral rewards may nevertheless attract pollinators by mimicking the flowers of rewarding plants. It has been suggested that both mimics and models should suffer reduced fitness when mimics are abundant relative to their models. By manipulating the relative densities of an orchid mimic Disa nivea and its rewarding model Zaluzianskya microsiphon in small experimental patches within a larger population we demonstrated that the mimic does indeed suffer reduced pollination success when locally common relative to its model. Behavioural experiments suggest that this phenomenon results from the tendency of the long-proboscid fly pollinator to avoid visits to neighbouring plants when encountering the mimic. No negative effect of the mimic on the pollination success of the model was detected. We propose that changes in pollinator flight behaviour, rather than pollinator conditioning, are likely to account for negative frequency-dependent reproductive success in deceptive orchids.     

The effect of habitat-specific sampling on biological assessment of water quality using a predictive model

1. Detection of impairment in macroinvertebrate communities using rapid biological assessment depends on the ability to compare sites, with confidence that differences obtained result from water quality. However, collections from more than one habitat type may introduce variation that can potentially mask water quality differences among sites. Data were collected from the riffle, edge, pool-rock and macrophyte habitats at reference (minimally disturbed) and test (disturbed) stream sites throughout the Australian Capital Territory. The effect of habitat-specific sampling on predictive models for detecting impairment in macroinvertebrate communities was determined. Four models were used: riffle only, edge only, each habitat as an individual object, and all habitats sampled at a site considered as a composite sample. 2. Macroinvertebrates from individual habitats generally clustered into separate groups because collections from the same habitat at different sites were more similar than collections from different habitats within a site. Thus, in the habitats as individual objects model, the taxa predicted to occur at a test site may be an indication of habitat type rather than water quality. The outputs of the composite habitats and riffle and edge models were similar. However, the variable number of habitats included at each site in the composite model may confound the detection of biological impairment because of unequal sampling effort. The riffle and edge models were the most robust because they were less confounded by inter-habitat variation and were based on comparisons made between equivalent environmental units. 3. Comparison of observed/expected taxa ratios for test sites showed that each model could detect biological impairment, indicating considerable data redundancy was introduced by sampling several habitats. In particular, the pool-rock and macrophyte habitats contributed no information with regard to macroinvertebrate taxon occurrence or detection of biological impairment that could not be obtained from either the riffle or edge habitats within the study area.     

Evidence of a geographically variable competitive mimicry relationship in coral reef fishes

In Kimbe Bay, Papua New Guinea, juvenile surgeonfish Acanthurus pyroferus have been shown to gain access to food resources defended by the damselfish Plectroglyphidodon lacrymatus by mimicking a pygmy angelfish, Centropyge vrolikii , that does not compete with the damsel for food. I tested whether A. pyroferus juveniles gain the same competitive advantage from mimicking a different pygmy angelfish, Centropyge flavissima , in Moorea, French Polynesia. Through abundance and substrate surveys, behavioral observations and stomach content analyses, I demonstrate that in Moorea, mimicry of Ce. flavissima does not provide A. pyroferus with access to damselfish Stegastes nigricans territories; Ce. flavissima models are always attacked upon territory entry and A. pyroferus mimics avoid damsel territories. Damselfish aggression toward the model angelfish cannot be attributed to overabundance of the deceptive mimic; instead, aggression can best be explained by the fact that Ce. flavissima competes with damsels in Moorea by consuming their algal turfs, making them inappropriate models for competitive mimics. Juveniles of many Indo-Pacific surgeonfishes appear to mimic pygmy angelfishes; I suggest that these mimics' success in gaining access to damselfish territories is geographically variable and may be determined by the extent to which mimics, models and receivers overlap in resource use at a given site. This mimicry complex may thus present an excellent illustration of the geographic mosaic model of coevolution.     

Mimicry between unequally defended prey can be parasitic: evidence for quasi-Batesian mimicry

The nature of signal mimicry between defended prey (known as Müllerian mimicry) is controversial. Some authors assert that it is always mutualistic and beneficial, whilst others speculate that less well defended prey may be parasitic and degrade the protection of their better defended co-mimics (quasi-Batesian mimicry). Using great tits (Parus major) as predators of artificial prey, we show that mimicry between unequally defended co-mimics is not mutualistic, and can be parasitic and quasi-Batesian. We presented a fixed abundance of a highly defended model and a moderately defended dimorphic (mimic and distinct non-mimetic) species, and varied the relative frequency of the two forms of the moderately defended prey. As the mimic form increased in abundance, per capita predation on the model-mimic pair increased. Furthermore, when mimics were rare they gained protection from predation but imposed no co-evolutionary pressure on models. We found that the feeding decisions of the birds were affected by their individual toxic burdens, consistent with the idea that predators make foraging decisions which trade-off toxicity and nutrition. This result suggests that many prey species that are currently assumed to be in a simple mutualistic mimetic relationship with their co-mimic species may actually be engaged in an antagonistic co-evolutionary process.