The relationship between mimetic imperfection and phenotypic variation in insect colour patterns

Many hoverflies (Syrphidae) mimic wasps or bees through colour or behavioural adaptations. The relationship between phenotypic variation in colour pattern and mimetic perfection (as determined by pigeons) was investigated in three species of Müllerian mimics (Vespula spp.) and 10 Batesian hoverfly mimics, plus two non-mimetic species of flies. Four predictions were tested: (i) Batesian mimics might be imperfect because they are in the process of evolving towards perfection, hence there should be a positive relationship between variation and imperfection; (ii) some Batesian mimics are imperfect because they do not have the appropriate genetic variation to improve and have evolved to be as good as possible, hence there should be no differences between species, all displaying a low level of variation; (iii) very common hoverflies should show the highest levels of variation because they outnumber their models, resulting in high predation and a breakdown in the mimetic relationship; and (iv) social wasps (Vespula) have such a powerful defence that anything resembling a wasp, both Müllerian and perfect Batesian mimics, would be avoided, resulting in relaxed selection and high variance. Poor mimics may still evolve to resemble wasps as well as possible and display lower levels of variation. The data only provided support for the fourth prediction. The Müllerian mimics, one of the most perfect Batesian mimics, and the non-mimetic flies displayed much higher levels of variation than the other species of Batesian mimics.     

Conditioning the pecking motions of pigeons

The spatio-temporal courses of head and neck motions of pigeons while pecking at small grains are described. Single and serial pecks are distinguished but the inter- and intraindividual variability of the peck kinetics is stressed. Pigeons were then trained with instrumental conditioning procedures to speed-up their pecking. A partial reinforcement schedule where pigeons had to peck repeatedly before receiving reward led to a mild shortening of inter-peck intervals at lower reinforcement rates but surprisingly, a lengthening at higher rates. A schedule where short inter-peck intervals were differentially rewarded yielded a pronounced abbreviation of the inter-peck intervals, but this was achieved by a reduction of the movement path rather than an increase in motion velocity. A schedule whereby increased approach velocities were differentially rewarded yielded marked movement accelerations. When pigeons were rewarded for diminished approach speeds they also showed significant movement decelerations. Finally, it is shown that pigeons could learn to reliably abort their peck approach movement when a visual stimulus signalling a penalty was occasionally presented during the approach movement. The proportion of successful peck interruptions decreased as these interruption signals occurred later during the approach phase. It is concluded that the pecking of pigeons is neither an innately fixed nor a visually ballistic movement. It is instead a multiply controlled and flexibly adaptable response pattern.     

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.     

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.     

Hoverflies are imperfect mimics of wasp colouration

Many Batesian mimics are considered to be inaccurate copies of their models, including a number of hoverfly species which appear to be poor mimics of bees and wasps. This inaccuracy is surprising since more similar mimics are expected to deceive predators more frequently and therefore have greater survival. One suggested explanation is that mimics which appear inaccurate to human eyes may be perceived differently by birds, the probable agents of selection. For example, if patterns contain an ultra-violet (UV) component, this would be visible to birds but overlooked by humans. So far, indirect comparisons have been made using human and bird responses to mimetic stimuli, but direct colour measurements of mimetic hoverflies are lacking. We took spectral readings from a wide range of hoverfly and wasp patterns. They show very low reflectance in the UV range, and do not display any human-invisible colour boundaries. We modelled how the recorded spectra would be perceived by both birds and humans. While colour differences between wasps and hoverflies are slightly more distinct according to human visual abilities, bird vision is capable of discriminating the two taxa in almost all cases. We discuss a number of factors that might make the discrimination task more challenging for a predator in the field, which could explain the apparent lack of selection for accurate colour mimicry.     

A hypothesis to explain accuracy of wasp resemblances

Mimicry is one of the oldest concepts in biology, but it still presents many puzzles and continues to be widely debated. Simulation of wasps with a yellow‐black abdominal pattern by other insects (commonly called “wasp mimicry”) is traditionally considered a case of resemblance of unprofitable by profitable prey causing educated predators to avoid models and mimics to the advantage of both (Figure 1a). However, as wasps themselves are predators of insects, wasp mimicry can also be seen as a case of resemblance to one's own potential antagonist. We here propose an additional hypothesis to Batesian and Müllerian mimicry (both typically involving selection by learning vertebrate predators; cf. Table 1) that reflects another possible scenario for the evolution of multifold and in particular very accurate resemblances to wasps: an innate, visual inhibition of aggression among look‐alike wasps, based on their social organization and high abundance. We argue that wasp species resembling each other need not only be Müllerian mutualists and that other insects resembling wasps need not only be Batesian mimics, but an innate ability of wasps to recognize each other during hunting is the driver in the evolution of a distinct kind of masquerade, in which model, mimic, and selecting agent belong to one or several species (Figure  1b). Wasp mimics resemble wasps not (only) to be mistaken by educated predators but rather, or in addition, to escape attack from their wasp models. Within a given ecosystem, there will be selection pressures leading to masquerade driven by wasps and/or to mimicry driven by other predators that have to learn to avoid them. Different pressures by guilds of these two types of selective agents could explain the widely differing fidelity with respect to the models in assemblages of yellow jackets and yellow jacket look‐alikes.     

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.     

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.     

Field estimates of survival do not reflect ratings of mimetic similarity in wasp-mimicking hover flies

The evolution of mimicry, and particularly the persistence of undefended Batesian mimetic forms that are imperfect copies of their defended models, remains a central question in evolutionary biology. Previous work has demonstrated that variation in mimetic fidelity in artificial prey can alter survival. However, no studies have validated the assumption that detailed laboratory-based measurements of mimetic fidelity are actually reflected in survival in natural field experiments. Here, we demonstrate that, in line with previous studies, the mimetic similarity of 77 hover fly (Diptera: Syrphidae) species to the common wasp Vespula alascensis is strongly related to the number of abdominal stripes exhibited by the flies. We then produce three artificial pastry baits: (1) a “model” which is chemically defended and has two stripes, (2) a one-stripe mimic, and (3) an unstriped mimic. Based on the ratings study, we predicted that the one-stripe mimic would exhibit survival intermediate between the unstriped mimic and the model. Baits were deployed in experiments each involving 81 baits (27 of each kind), at 3 sites, with experiments replicated 10 times at each site for a total deployment of 2,430 baits. Proportional hazards models show that both one-striped and model baits survived equally well and significantly better than the unstriped baits, suggesting categorical prey identification rather than the use of stripe number as a continuous trait, as was suggested by the laboratory study. These findings suggest that, while humans and avian predators can distinguish mimics from models in the laboratory using a range of traits, behaviour in the field may not reflect this ability. This absence of a link between continuous measures of mimetic fidelity and prey selection may contribute to the maintenance of imperfect mimicry, but more studies using near-natural experimental paradigms are needed to investigate the phenomenon further.     

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.     

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.     

Mimetic gain in batesian and Müllerian mimicry

Summary Starting from field investigations and experiments on mimetic butterfly populations a model for two mimetic species is developed. The model comprises various features such as the growth rates and carrying capacities of the two species, their unpalatability to predators, the recruitment and the training of the predators and, most important, the similarity of the two mimetic species. The model ranges from pure Batesian to pure Müllerian mimicry over a spectrum of possible cases. The mimetic gain is introduced as the relative increase in equilibrium density in a mimetic situation as compared to a situation where mimicry is not present. The dependence of this quantity on parameters as growth rate, carrying capacity, unpalatability, and similarity is investigated using numerical methods.     

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.     

Playing with Black and Yellow: The Evolvability of a Batesian Mimicry

Irrespective of the selective advantage deriving from similar color pattern, the evolution of Batesian (and Müllerian) mimicry between distantly related insects groups has been perhaps facilitated by the availability to both models and mimics of similar pattern units more likely to be expressed, and to be modified in parallel ways, due to shared developmental constraints. We explore this hypothesis in a comparison of units of black-and-yellow color patterns between wasps (Vespidae) and those syrphids (Syrphidae) that are considered to be their Batesian mimics. As a proxy for evolvability we analyzed the co-occurrence of multiple color pattern within species (either as serial homologues or as expression of intraspecific variation) in 203 species of syrphids and 127 species of wasps. In both the wasps and the syrphids, the most frequent black-and-yellow patterns on the abdomen—all shared between the two insect groups—are also the most extensively linked in the networks of intraspecific co-occurrence, but are not the same in the two insect groups: in accordance with our hypothesis, this suggests positively biased evolvability.     

Balanced polymorphisms and their divergence in a Heliconius butterfly

The evolution of mimicry in similarly defended prey is well described by the Müllerian mimicry theory, which predicts the convergence of warning patterns in order to gain the most protection from predators. However, despite this prediction, we can find great diversity of color patterns among Müllerian mimics such as Heliconius butterflies in the neotropics. Furthermore, some species have evolved the ability to maintain multiple distinct warning patterns in single populations, a phenomenon known as polymorphic mimicry. The adaptive benefit of these polymorphisms is questionable since variation from the most common warning patterns is expected to be disadvantageous as novel signals are punished by predators naive to them. In this study, we use artificial butterfly models throughout Central and South America to characterize the selective pressures maintaining polymorphic mimicry in Heliconius doris. Our results highlight the complexity of positive frequency‐dependent selection, the principal selective pressure driving convergence among Müllerian mimics, and its impacts on interspecific variation of mimetic warning coloration. We further show how this selection regime can both limit and facilitate the diversification of mimetic traits.     

A protective function for aggressive mimicry?

Mimicry often involves a protective element, whereby the risk of predation on mimics is reduced owing to their resemblance to unpalatable models. However, protection from predation has so far seemed unimportant in aggressive mimicry, where mimics are usually predators rather than prey. Here, we demonstrate that bluestriped fangblennies (Plagiotremus rhinorhynchos), which are aggressive mimics of juvenile bluestreak cleaner wrasse (Labroides dimidiatus), derive significant protection benefits from their resemblance to cleaner fish. Field observations revealed that mimetic fangblennies were chased by potential victims less often than individuals of a closely related, ecologically and behaviourally similar but non-mimetic species (Plagiotremus tapeinosoma). After attacks, proximity to models protected mimics from retaliation by victims, but the effect of colour similarity was less clear. Both colour resemblance and physical proximity to models thus appear to protect cleaner-fish mimics from aggression by potential and actual victims of their attacks. Our results suggest that the mimicry types observed in nature, which are usually distinguished on the basis of the benefits accrued to mimics, may in fact overlap greatly in the benefits provided.     

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.     

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.     

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.