Rapid evolution of mimicry following local model extinction

Batesian mimicry evolves when individuals of a palatable species gain the selective advantage of reduced predation because they resemble a toxic species that predators avoid. Here, we evaluated whether—and in which direction—Batesian mimicry has evolved in a natural population of mimics following extirpation of their model. We specifically asked whether the precision of coral snake mimicry has evolved among kingsnakes from a region where coral snakes recently (1960) went locally extinct. We found that these kingsnakes have evolved more precise mimicry; by contrast, no such change occurred in a sympatric non-mimetic species or in conspecifics from a region where coral snakes remain abundant. Presumably, more precise mimicry has continued to evolve after model extirpation, because relatively few predator generations have passed, and the fitness costs incurred by predators that mistook a deadly coral snake for a kingsnake were historically much greater than those incurred by predators that mistook a kingsnake for a coral snake. Indeed, these results are consistent with prior theoretical and empirical studies, which revealed that only the most precise mimics are favoured as their model becomes increasingly rare. Thus, highly noxious models can generate an ‘evolutionary momentum’ that drives the further evolution of more precise mimicry—even after models go extinct.     

Mimics without models: causes and consequences of allopatry in Batesian mimicry complexes

Batesian mimicry evolves when a palatable species (the ‘mimic’) co-opts a warning signal from a dangerous species (the ‘model’) and thereby deceives its potential predators. Longstanding theory predicts that this protection from predation should break down where the model is absent. Thus, mimics are expected to only co-occur with their model. Yet, many mimics violate this prediction and occur in areas where their model is absent. Here, we discuss the causes and consequences of such allopatric mimics. We also describe how these ‘rule-bending’ mimics provide critical insights into diverse topics ranging from how Batesian mimicry evolves to its possible role in speciation.     

Predation on snakes of Argentina: Effects of coloration and ring pattern on coral and false coral snakes

The occurrence of coral snake coloration among unrelated venomous and non‐venomous snake species has often been explained in terms of warning coloration and mimicry. In Argentina, no field tests have been conducted to confirm this mimetic association between one venomous coral species (Micrurus phyrrocryptus, Elapidae) and two non‐venomous snake species with a similar color pattern (Lystrophis pulcher and Oxyrhopus rhombifer, Colubridae). The aims of this work were to test for the possible aposematic or cryptic function of the ring pattern and coloration of coral snakes and false coral snakes from central Argentina, and to analyse whether the pattern is effective throughout the year. Predation on snakes was estimated by using non‐toxic plasticine replicas of ringed venomous and non‐venomous snakes and unbanded green snakes placed along transects in their natural habitat during the dry and rainy season. Ringed color pattern was attacked by predators despite the background color. One of the replica types was attacked more than expected during the dry season, suggesting that both shape and width of rings may influence the choice by predators. The reaction of predators towards replicas that mimic snake species with ringed patterns is independent of the geographical region, and we can conclude that mimicry characteristics are quite general when the true models are present in the area.     

Geographic variation in mimetic precision among different species of coral snake mimics

Batesian mimicry is widespread, but whether and why different species of mimics vary geographically in resemblance to their model is unclear. We characterized geographic variation in mimetic precision among four Batesian mimics of coral snakes. Each mimic occurs where its model is abundant (i.e. in ‘deep sympatry’), rare (i.e. at the sympatry/allopatry boundary or ‘edge sympatry’) and absent (i.e. in allopatry). Geographic variation in mimetic precision was qualitatively different among these mimics. In one mimic, the most precise individuals occurred in edge sympatry; in another, they occurred in deep sympatry; in the third, they occurred in allopatry; and in the fourth, precise mimics were not concentrated anywhere throughout their range. Mimicry was less precise in allopatry than in sympatry in only two mimics. We present several nonmutually exclusive hypotheses for these patterns. Generally, examining geographic variation in mimetic precision – within and among different mimics – offers novel insights into the causes and consequences of mimicry.     

Unlinked Mendelian inheritance of red and black pigmentation in snakes: Implications for Batesian mimicry

Identifying the genetic basis of mimetic signals is critical to understanding both the origin and dynamics of mimicry over time. For species not amenable to large laboratory breeding studies, widespread color polymorphism across natural populations offers a powerful way to assess the relative likelihood of different genetic systems given observed phenotypic frequencies. We classified color phenotype for 2175 ground snakes (Sonora semiannulata) across the continental United States to analyze morph ratios and test among competing hypotheses about the genetic architecture underlying red and black coloration in coral snake mimics. We found strong support for a two‐locus model under simple Mendelian inheritance, with red and black pigmentation being controlled by separate loci. We found no evidence of either linkage disequilibrium between loci or sex linkage. In contrast to Batesian mimicry systems such as butterflies in which all color signal components are linked into a single “supergene,” our results suggest that the mimetic signal in colubrid snakes can be disrupted through simple recombination and that color evolution is likely to involve discrete gains and losses of each signal component. Both outcomes are likely to contribute to the exponential increase in rates of color evolution seen in snake mimicry systems over insect systems.     

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.     

Predator cognition permits imperfect coral snake mimicry

Batesian mimicry is often imprecise. An underexplored explanation for imperfect mimicry is that predators might not be able to use all dimensions of prey phenotype to distinguish mimics from models and thus permit imperfect mimicry to persist. We conducted a field experiment to test whether or not predators can distinguish deadly coral snakes (Micrurus fulvius) from nonvenomous scarlet kingsnakes (Lampropeltis elapsoides). Although the two species closely resemble one another, the order of colored rings that encircle their bodies differs. Despite this imprecise mimicry, we found that L. elapsoides that match coral snakes in other respects are not under selection to match the ring order of their model. We suggest that L. elapsoides have evolved only those signals necessary to deceive predators. Generally, imperfect mimicry might suffice if it exploits limitations in predator cognitive abilities.     

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.     

The snake hiss: potential acoustic mimicry in a viper–colubrid complex

Examples of acoustic Batesian mimicry are scarce, in contrast to visual mimicry. Here we describe a potential case of acoustic mimicry of a venomous viper model by harmless viperine snakes (colubrid). Viperine snakes resemble vipers in size, shape, colour, pattern, and anti‐predatory behaviours, including head flattening, false strikes, and hissing. We sought to investigate whether hissing evolved as part of, or separately to, the viper mimic syndrome. To do this, we recorded and analysed the hissing sounds of several individual asp vipers, viperine snakes, and grass snakes (a close relative of viperine snakes that hisses but does not mimic the asp viper). Frequencies consistently ranged from 40 to 12 000 Hz across species and individuals. All vipers (100%) and most viperine snakes (84%) produced inhalation hissing sounds, in comparison to only 25% of grass snakes. Inhalation hissing sounds lasted longer in vipers than in viperine snakes. The hissing‐sound composition of grass snakes differed significantly from that of both asp vipers and viperine snakes; however, the hissing‐sound composition between viperine snakes and asp vipers was not statistically distinguishable. Whilst grass snake hissing sounds were characterized by high frequencies (5000–10 000 Hz), both vipers and viperine snake hissing sounds were dominated by low frequencies (200–400 Hz). A principal component analysis revealed no overlap between grass snakes and vipers, but important overlaps between viperine snakes and vipers, and between viperine snakes and grass snakes. The likelihood that these overlaps respectively reflect natural selection for Batesian mimicry and phylogeny constraints is discussed. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1107–1114.     

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.     

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.     

Once a Batesian mimic, not always a Batesian mimic: mimic reverts back to ancestral phenotype when the model is absent

Batesian mimics gain protection from predation through the evolution of physical similarities to a model species that possesses anti-predator defences. This protection should not be effective in the absence of the model since the predator does not identify the mimic as potentially dangerous and both the model and the mimic are highly conspicuous. Thus, Batesian mimics should probably encounter strong predation pressure outside the geographical range of the model species. There are several documented examples of Batesian mimics occurring in locations without their models, but the evolutionary responses remain largely unidentified. A mimetic species has four alternative evolutionary responses to the loss of model presence. If predation is weak, it could maintain its mimetic signal. If predation is intense, it is widely presumed the mimic will go extinct. However, the mimic could also evolve a new colour pattern to mimic another model species or it could revert back to its ancestral, less conspicuous phenotype. We used molecular phylogenetic approaches to reconstruct and test the evolution of mimicry in the North American admiral butterflies (Limenitis: Nymphalidae). We confirmed that the more cryptic white-banded form is the ancestral phenotype of North American admiral butterflies. However, one species, Limenitis arthemis, evolved the black pipevine swallowtail mimetic form but later reverted to the white-banded more cryptic ancestral form. This character reversion is strongly correlated with the geographical absence of the model species and its host plant, but not the host plant distribution of L. arthemis. Our results support the prediction that a Batesian mimic does not persist in locations without its model, but it does not go extinct either. The mimic can revert back to its ancestral, less conspicuous form and persist.     

Disruptive ecological selection on a mating cue

Adaptation to divergent ecological niches can result in speciation. Traits subject to disruptive selection that also contribute to non-random mating will facilitate speciation with gene flow. Such ‘magic’ or ‘multiple-effect’ traits may be widespread and important for generating biodiversity, but strong empirical evidence is still lacking. Although there is evidence that putative ecological traits are indeed involved in assortative mating, evidence that these same traits are under divergent selection is considerably weaker. Heliconius butterfly wing patterns are subject to positive frequency-dependent selection by predators, owing to aposematism and Müllerian mimicry, and divergent colour patterns are used by closely related species to recognize potential mates. The amenability of colour patterns to experimental manipulation, independent of other traits, presents an excellent opportunity to test their role during speciation. We conducted field experiments with artificial butterflies, designed to match natural butterflies with respect to avian vision. These were complemented with enclosure trials with live birds and real butterflies. Our experiments showed that hybrid colour-pattern phenotypes are attacked more frequently than parental forms. For the first time, we demonstrate disruptive ecological selection on a trait that also acts as a mating cue.     

DIFFERENTIAL AVOIDANCE OF CORAL SNAKE BANDED PATTERNS BY FREE-RANGING AVIAN PREDATORS IN COSTA RICA

Empirical studies of mimicry have rarely been conducted under natural conditions. Field investigations of some lepidopteran systems have provided a bridge between experiments examining artificial situations and the mimicry process in nature, but these systems do not include all types of mimicry. The presence of dangerous or deadly models is thought to alter the usual rules for mimicry complexes. In particular, a deadly model is expected to protect a wide variety of mimics. Avoidance of different types of mimics should vary according to how closely they resemble the model. Coral snake mimicry complexes in the neotropics may provide natural systems in which these ideas can be examined, but there is no direct evidence that the patterns of venomous coral snakes or potential mimics are avoided in the wild. Plasticine replicas of snakes were used to assess the frequency of avian predation attempts as a function of color pattern. Avian predators left identifiable marks on the replicas, the position of which indicated that replicas were perceived as potentially dangerous prey items by birds. The number of attacks on unmarked brown replicas was greater than that on tricolor coral snake banded replicas. This result was true whether replicas were placed on natural or plain white backgrounds, suggesting that coral snake banded patterns function aposematically. In a separate experiment, replicas representing all six patterns of proposed coral mimics at the study site were attacked less often than unmarked brown replicas. Within these six banded patterns, some were attacked significantly more often than others. This study provides direct field evidence that coral snake banded patterns are avoided by free-ranging avian predators and supports theoretical predictions about mimicry systems involving deadly models.     

Behaviour before beauty: Signal weighting during mate selection in the butterfly Papilio polytes

Mating displays often contain multiple signals. Different combinations of these signals may be equally successful at attracting a mate, as environment and signal combination may influence relative signal weighting by choosy individuals. This variation in signal weighting among choosy individuals may facilitate the maintenance of polymorphic displays and signalling behaviour. One group of animals known for their polymorphic patterning are Batesian mimetic butterflies, where the interaction of sexual selection and predation pressures is hypothesized to influence the maintenance of polymorphic wing patterning and behaviour. Males in the female‐limited polymorphic Batesian mimetic butterfly Papilio polytes use female wing pattern and female activity levels when determining whom to court. They court stationary females with mimetic wing patterns more often than stationary females with non‐mimetic, male‐like wing patterns and active females more often than inactive females. It is unclear whether females modify their behaviour to increase (or decrease) their likelihood of receiving male courtship, or whether non‐mimetic females spend more time in cryptic environments than mimetic females, to compensate for their lack of mimicry‐driven predation protection (at the cost of decreased visibility to males). In addition, relative signal weighting of female wing pattern and activity to male mate selection is unknown. To address these questions, we conducted a series of observational studies of a polymorphic P. polytes population in a large butterfly enclosure. We found that males exclusively courted active females, irrespective of female wing pattern. However, males did court active non‐mimetic females significantly more often than expected given their relative abundance in the population. Females exhibited similar activity levels, and selected similar resting environments, irrespective of wing pattern. Our results suggest that male preference for non‐mimetic females may play an active role in the maintenance of the non‐mimetic female form in natural populations, where males are likely to be in the presence of active, as well as inactive, mimetic and non‐mimetic females.     

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.     

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.     

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.     

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.     

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.