Experimental evidence for predator learning and Müllerian mimicry in Peruvian poison frogs (Ranitomeya,Dendrobatidae)

The evolution of mimicry is one of the most powerful examples of evolution driven by natural selection; however it is rare in non-insect taxa and thus is understudied. Ranitomeya imitator underwent a ‘mimetic radiation’ and now mimics three congeneric model species (R. fantastica, R. summersi, and two morphs of R. variabilis), creating geographically distinct populations of the species, including four allopatric mimetic morphs. These complexes are thought to represent a case of Müllerian mimicry, but no prior empirical studies on learned avoidance by predators support this claim. In this study we used young chickens (Gallus domesticus) as naïve predators to determine if a co-mimetic morph of R. imitator and R. variabilis contribute to reciprocal learned avoidance by predators—a key component of Müllerian mimicry. Chickens exposed to either stimulus species demonstrated reciprocal learned avoidance; thus our results indicate that this complex functions as a Müllerian mimicry system. This study provides novel empirical evidence supporting predictions of the Müllerian mimicry hypothesis in anurans. Our study shows no difference between learned avoidance in stimuli frogs and a ‘novel’ morph of R. imitator that differed in both color and pattern, indicating that learned avoidance by predators may be generalized in this system. Generalized learning provides a plausible mechanism for the maintenance of both polytypic mimicry and the maintenance of intrapopulation phenotypic heterogeneity.     

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.     

Müllerian mimicry in aposematic spiny plants

Müllerian mimicry is common in aposematic animals but till recently, like other aspects of plant aposematism was almost unknown. Many thorny, spiny and prickly plants are considered aposematic because their sharp defensive structures are colorful and conspicuous. Many of these spiny plant species (e.g., cacti and Agave in North American deserts; Aloe, Euphorbia and acacias with white thorns in Africa; spiny plants in Ohio; and spiny members of the Asteraceae in the Mediterranean basin) have overlapping territories, and also similar patterns of conspicuous coloration, and suffer from the evolutionary pressure of grazing by the same large herbivores. I propose that many of these species form Müllerian mimicry rings.Key words: aposematic coloration, defense, evolution, herbivory, müllerian mimicry, spines, thornsAposematic (warning) coloration is a biological phenomenon in which poisonous, dangerous or otherwise unpalatable organisms visually advertise these qualities to other animals. The evolution of aposematic coloration is based on the ability of target enemies to associate the visual signal with the risk, damage or non-profitable handling, and later to avoid such organisms as prey. Typical colors of aposematic animals are yellow, orange, red, purple, black, white or brown and combinations of these.^1–5 Many thorny, spiny and prickly plant species were proposed to be aposematic because their sharp defensive structures are usually colorful (yellow, orange, red, brown, black, white) and/or associated with similar conspicuous coloration.^5–22 Animal spines also have similar conspicuous coloration and were proposed to be aposematic.^1,5,17,23Several authors have proposed that mimicry of various types helps in plant defense, e.g.,^9,24–34 More specifically, Müllerian mimicry was already proposed to exist in several defensive plant signaling systems. The first was for several spiny species with white-variegated leaves.^8,10 The second was for some tree species with red or yellow poisonous autumn leaves.³⁵ The third cases are of a mixture of Müllerian and Batesian mimicry, of thorn auto-mimicry found in many Agave species.⁸Here I propose that many species of visually aposematic spiny plants of the following taxa: (1) Cactaceae, (2) the genus Agave, (3) the genus Aloe, (4) African thorny members of the genus Euphorbia, (5) African acacias with white thorns, (6) spiny vascular plants of southeastern Ohio, (7) spiny Near Eastern plants with white variegation on their leaves, (8) Near Eastern members of the Asteraceae with yellow spines, form Müllerian mimicry rings of spiny plants.To consider the existence of Müllerian mimicry rings in aposematic organisms, two factors are needed: (1) a similar signal, and (2) an overlapping distribution in respect to the territory of predators in animals, or herbivores in plants. I will show below that for the plant taxa proposed here to form Müllerian mimicry rings, both criteria operate.The accumulating data about the common association of plant defenses by spines with visual conspicuousness, along with the fact that many such species overlap in their habitat, raises the possibility of the broad phenomenon of existence of Müllerian mimicry rings in plants. Even from the limited number of publications proposing visual aposematism in spiny plants, the operation of vegetal Müllerian mimicry rings seems to be obvious. The phenomenon can now be traced to both the Old World (Asia, Africa and Europe) and the New World (North America). The best-studied cases include Cactaceae and the genera Agave, Aloe and Euphorbia,⁶ African acacias with white thorns,^12,15 Near Eastern spiny plants with white variegation on their leaves,^7,11 aposematic spiny vascular plants of southeastern Ohio,¹⁶ and many spiny Mediterranean species of the Asteraceae with yellow spines.²²In the four spiny taxa (Cactaceae and the genera Agave, Aloe and Euphorbia) that were the first to be proposed as visually aposematic⁶ there is a very strong morphological similarity. In cacti, there are two types of conspicuousness of spines that are typical of many plant species: (1) colorful spines, and (2) white spots, or white or colorful stripes, associated with spines on the stems. These two types of aposematic coloration also dominate the spine system of Agave, Aloe and Euphorbia. The fact that many species of three of these four spiny taxa (Agave, Aloe and Euphorbia) are also poisonous^36–38 further indicates their potential to form Müllerian mimicry rings.I propose that each of these groups for itself and some of these groups (e.g., Cactaceae and the genus Agave in North America; Aloe, Euphorbia and acacias in east and south Africa) that have overlapping distribution and share at least some of the herbivores, form Müllerian mimicry rings.The first Müllerian mimicry ring is of cacti and Agave that have an overlapping distribution over large areas in North America.^37,39 The large herbivores in North America disappeared not so long ago in evolutionary time scales and seem to have shaped the spiny defense of these plant taxa.⁴⁰The second Müllerian mimicry ring is of the spiny and thorny members of the African genera Aloe, Euphorbia and certain acacias with very conspicuous white thorns, which partly overlap in distribution and share various large mammalian herbivores.^12,15,36,41The third Müllerian mimicry ring is the outcome of the common presence of aposematic coloration in spiny vascular plants of southeastern Ohio,¹⁶ with color patterns in thorns and spines similar to those of Cactaceae and the genera Agave, Aloe and Euphorbia described in Lev-Yadun.⁶The next case of potential operation of Müllerian mimicry ring of spiny plants with overlapping territories that suffer from the same large herbivores, but on a much smaller geographical scale, has recently been proposed for several spiny species with white-variegated leaves,⁷ and later for more than 20 spiny species in the flora of Israel that have white markings associated with their spines.¹¹The last case of a probable Müllerian mimicry ring was described by Ronel et al.²² who while studying the spine system of Near Eastern spiny members of the Asteraceae, found 29 spiny species with yellow spines, and additional such species are expected to occur. Since some of these species and others with yellow spines also grow in southern Europe, it is clear that the same phenomenon is also common there.I conclude that Müllerian mimicry rings seem to be very common in plants, and that it is probable that many other spiny plants that form Müllerian mimicry rings are waiting to be studied. Such defensive rings are probably also formed by poisonous plants that share similar colors or odors.     

Batesian, quasi-Batesian or Müllerian mimicry? Theory and data in mimicry Research

In this paper I argue that the nature of mimetic relationships remains contentious because there are insufficient data to enable full evaluation of theoretical models. There is, however, a growing appreciation of the need to draw together empirical studies to provide foundations for theoretical work. I review some recent data that considers the responses of predators to changing numbers of defended prey items and the nature of mimicry along a palatability spectrum. A simple model of predator behaviour is constructed which combines assumptions from Pavlovian learning studies with traditional ‘number dependent’ learning models. This model has two important properties. First it shows that Pavlovian assumptions can be represented in a simple model which generates interesting predictions. Second it indicates some areas that still need detailed empirical study – most importantly perhaps is the way that predators respond to prey with different levels of edibility. This revised version was published online in July 2006 with corrections to the Cover Date.     

Spatial mosaic and interfacial dynamics in a Müllerian mimicry system

Uncovering why spatial mosaics of mimetic morphs are maintained in a Müllerian mimicry system has been a challenging issue in evolutionary biology. In this article, we analyze the reaction diffusion system that describes two-species Müllerian mimicry in one- and two-dimensional habitats. Due to positive frequency-dependent selection, a local population first approaches the state where one of the comimicking patterns predominates, which is followed by slow movement of boundaries where different patterns meet. We then analyze the interfacial dynamics of the boundaries to find whether a stable cline is maintained and to obtain the wave speed if the cline is unstable. The results are: (1) In a spatially uniform habitat the morph with greater base fitness spreads both in one and two species system. (2) The strength of cross-species interaction determines whether the mimetic morph clines of model and mimic species coalesce into the same geographical region or pass through each other. The joint wave speed of clines decreases by increasing the number of comimicking species in the mimicry ring. (3) In spatial heterogeneous habitats, stable clines can be maintained due to the balance between the base fitness gradient and the biased gene flow by negative curvature of boundary. This allows the persistence of a spatial mosaic even if one of the morphs is in every place advantageous over the other. A balanced cline is also maintained if there is a gradient in the population density. (4) A new advantageous morph occurring at a local region is doomed to go to extinction in a finite time if the "radius" of initial distribution is below a threshold. Possible applications to the heliconiine butterfly mimicry ring, heterozygous disadvantage systems of chromosomal rearrangement and hybrid zone, the third phase of Wright's Shifting Balance theory, and cytoplasmic incompatibility are discussed.     

The importance of pattern similarity between Müllerian mimics in predator avoidance learning

Müllerian mimicry, where unpalatable prey share common warning patterns, has long fascinated evolutionary biologists. It is commonly assumed that Müllerian mimics benefit by sharing the costs of predator education, thus reducing per capita mortality, although there has been no direct test of this assumption. Here, we specifically measure the selection pressure exerted by avian predators on unpalatable prey with different degrees of visual similarity in their warning patterns. Using wild-caught birds foraging on novel patterned prey in the laboratory, we unexpectedly found that pattern similarity did not increase the speed of avoidance learning, and even dissimilar mimics shared the education of naive predators. This was a consistent finding across two different densities of unpalatable prey, although mortalities were lower at the higher density as expected. Interestingly, the mortalities of Müllerian mimics were affected by pattern similarity in the predicted way by the end of our experiment, although the result was not quite significant. This suggests that the benefits to Müllerian mimics may emerge only later in the learning process, and that predator experience of the patterns may affect the degree to which pattern similarity is important. This highlights the need to measure the behaviour of real predators if we are to understand fully the evolution of mimicry systems.     

Causes and Consequences of a Lack of Coevolution in Müllerian mimicry

Müllerian mimicry, in which both partners are unpalatable to predators, is often used as an example of a coevolved mutualism. However, it is theoretically possible that some Müllerian mimics are parasitic if a weakly defended mimic benefits at the expense of a more highly defended model, a phenomenon known as ‘quasi-Batesian mimicry’. The theory expounded by Müller and extended here for unequal unpalatability, on the other hand, suggests that quasi-Batesian mimicry should be rare in comparison with classical, or mutualistic Müllerian mimicry. Evolutionarily, quasi-Batesian mimicry has consequences similar to classical Batesian mimicry, including unilateral ‘advergence’ of the mimic to the model, and diversifying frequency-dependent selection on the mimic which may lead to mimetic polymorphism. In this paper, theory and empirical evidence for mutual benefit and coevolution in Müllerian mimicry are reviewed. I use examples from well-known insect Müllerian mimicry complexes: the Limenitis–Danaus (Nymphalidae) system in North America, the Bombus–Psithyrus (Apidae) system in the north temperate zone, and the Heliconius–Laparus (Nymphalidae) system in tropical America. These give abundant evidence for unilateral advergence, and no convincing evidence, to my knowledge, for coevolved mutual convergence. Furthermore, mimetic polymorphisms are not uncommon. Yet classical mutualistic Müllerian mimicry, coupled with spatial (and possibly temporal) variation in model abundances convincingly explain these apparent anomalies without recourse to a quasi-Batesian explanation. Nevertheless, the case against classical Müllerian mimicry is not totally disproved, and should be investigated further. I hope that this tentative analysis of actual mimicry rings may encourage others to look for evidence of coevolution and quasi-Batesian effects in a variety of other Müllerian mimicry systems. This revised version was published online in July 2006 with corrections to the Cover Date.     

Individual behavioral variation in predator–prey models

The role of individual behavioral variation in community dynamics was studied. Behavioral variation in this study does not refer to differences in average responses (e.g., average response between presence and absence of antipredator behavior). Rather it refers to the variation around the average response that is not explained by trivial experimental treatments. First, the effect of behavioral variation was examined based on Jensen’s inequality. In cases of commonly used modeling framework with type II functional response, neglecting behavioral variation (a component of encounter rate) causes overestimation of predation effects. The effect of this bias on community processes was examined by incorporating the behavioral variation in a commonly used consumer-resource model (Rosenzweig–MacArthur model). How such a consideration affects a model prediction (paradox of enrichment) was examined. The inclusion of behavioral variation can both quantitatively and qualitatively alter the model characteristics. Behavioral variation can substantially increase the stability of the community with respect to enrichment.     

Testing Müllerian mimicry: an experiment with wild birds

Experiments with wild birds feeding on pastry 'prey' were performed to test competing theories of Müllerian mimicry Conventional theories predict that all resemblances between defended prey will be mutually advantageous and, hence, Müllerian. In contrast, unconventional theories predict that, if there are inequalities in defences between mimetic species, the less well-defended prey may dilute the protection of the better defended species in a quasi-Batesian manner. This unconventional prediction follows from an assumption that birds learn about the edibilities of prey using rules of Pavlovian learning. We report on two experiments, each lasting 40 days, which showed that a moderately defended prey can dilute the protection of a better defended mimic in a quasi-Batesian fashion, but can add protection to a mimic which has the same moderate levels of defence. These results match predictions of unconventional theories of mimicry and go some way to resolving the long-running arguments over the nature of Müllerian mimicry.     

Heterogeneity in predator micro-habitat use and the maintenance of Müllerian mimetic diversity

Müllerian mimicry, where groups of chemically defended species display a common warning color pattern and thereby share the cost of educating predators, is one of the most striking examples of ecological adaptation. Classic models of Müllerian mimicry predict that all unpalatable species of a similar size and form within a community should converge on a single mimetic pattern, but instead communities of unpalatable species often display a remarkable diversity of mimetic patterns (e.g. neotropical ithomiine butterflies). It has been suggested that this apparent paradox may be explained if different suites of predators and species belonging to different mimicry groups utilize different micro-habitats within the community. We developed a stochastic individual-based model for a community of unpalatable mimetic prey species and their predators to evaluate this hypothesis and to examine the effect of predator heterogeneity on prey micro-habitat use. We found that community-level mimetic diversity was higher in simulations with heterogeneous predator micro-habitat use than in simulations with homogeneous predator micro-habitat use. Regardless of the form of predation, mimicry pattern-based assortative mating caused community-level mimetic diversity to persist. Heterogeneity in predator micro-habitat use led to an increased association between mimicry pattern and prey micro-habitat use relative to homogeneous predator micro-habitat use. This increased association was driven, at least in part, by evolutionary convergence of prey micro-habitat use when predators displayed heterogeneous micro-habitat use. These findings provide a theoretical explanation for an important question in evolutionary biology: how is community-level Müllerian mimetic diversity maintained in the face of selection against rare phenotypes?     

Spatial mosaic formation through frequency-dependent selection in Müllerian mimicry complexes

Although contemporary models of Müllerian mimicry have considered the movement of interfacial boundaries between two distinct mimetic forms, and even the possibility of polymorphisms in two patch systems, no model has considered how multiple forms of Müllerian mimics might evolve and be maintained over large geographical areas. A spatially explicit individual-based model for the evolution of Müllerian mimicry is presented, in which two unpalatable species are distributed over discrete cells within a regular lattice. Populations in each cell are capable of genetic drift and experience localized dispersal as well as frequency-dependent selection by predators. When each unpalatable prey species was introduced into a random cell and allowed to spread, then mimicry evolved throughout the system in the form of a spatial mosaic of phenotypes, separated by narrow "hybrid zones". The primary mechanism generating phenotypic diversity was the occasional establishment of new mutant forms in unoccupied cells and their subsequent maintenance (and spread) through frequency-dependent selection. The mean number of discrete clusters of the same morph that formed in the lattice was higher the higher the intensity of predation, and higher the lower the dispersal rate of unpalatable prey. Under certain conditions the hybrid zones moved, in a direction dependent on the curvature of their interfacial boundaries. However, the mimetic mosaics were highly stable when the intensity of predation was high and the rate of prey dispersal was low. Overall, this model highlights how a stable mosaic of different mimetic forms can evolve from a range of starting conditions through a combination of chance effects and localized frequency-dependent selection.     

Tasting the difference: do multiple defence chemicals interact in Müllerian mimicry?

Müllerian mimicry, where two unpalatable species share a warning pattern, is classically believed to be a form of mutualism, where the species involved share the cost of predator education. The evolutionary dynamics of Müllerian mimicry have recently become a controversial subject, after mathematical models have shown that if minor alterations are made to assumptions about the way in which predators learn and forget about unpalatable prey, this textbook case of mutualism may not be mutualistic at all. An underlying assumption of these models is that Müllerian mimics possess the same defence chemical. However, some Müllerian mimics are known to possess different defence chemicals. Using domestic chicks as predators and coloured crumbs flavoured with either the same or different unpalatable chemicals as prey, we provide evidence that two defence chemicals can interact to enhance predator learning and memory. This indicates that Müllerian mimics that possess different defence chemicals are better protected than those that share a single defence chemical. These data provide insight into how multiple defence chemicals are perceived by birds,and how they influence the way birds learn and remember warningly coloured prey. They highlight the importance of considering how different toxins in mimicry rings can interact in the evolution and maintenance of Müllerian mimicry and could help to explain the remarkable variation in chemical defences found within and between species.     

Convergent evolution in the genetic basis of Müllerian mimicry in heliconius butterflies

The neotropical butterflies Heliconius melpomene and H. erato are Müllerian mimics that display the same warningly colored wing patterns in local populations, yet pattern diversity between geographic regions. Linkage mapping has previously shown convergent red wing phenotypes in these species are controlled by loci on homologous chromosomes. Here, AFLP bulk segregant analysis using H. melpomene crosses identified genetic markers tightly linked to two red wing-patterning loci. These markers were used to screen a H. melpomene BAC library and a tile path was assembled spanning one locus completely and part of the second. Concurrently, a similar strategy was used to identify a BAC clone tightly linked to the locus controlling the mimetic red wing phenotypes in H. erato. A methionine rich storage protein (MRSP) gene was identified within this BAC clone, and comparative genetic mapping shows red wing color loci are in homologous regions of the genome of H. erato and H. melpomene. Subtle differences in these convergent phenotypes imply they evolved independently using somewhat different developmental routes, but are nonetheless regulated by the same switch locus. Genetic mapping of MRSP in a third related species, the “tiger” patterned H. numata, has no association with wing patterning and shows no evidence for genomic translocation of wing-patterning loci.     

Selection of aphid prey by a generalist predator: do prey chemical defences matter?

1. For predators, prey selection should maximise nutrition and minimise fitness costs. In the present study, it was investigated whether a generalist predator [Chrysoperla carnea (Stephens) lacewing larvae] rejected harmful, chemically‐defended prey [Brevicoryne brassicae (Linnaeus) aphids] when non‐defended prey [Myzus persicae (Sulzer) aphids] were available. 2. It was tested: (i) whether consuming different prey species affects predator mortality; (ii) whether naïve predators reject chemically‐defended prey while foraging when non‐defended prey are available; (iii) whether the relative abundance of each prey affects the predator's prey choice; and (iv) whether predators learn to avoid consuming chemically‐defended prey after exposure to both prey species. 3. Consumption of B. brassicae yielded greater C. carnea mortality than M. persicae consumption, but naïve C. carnea did not reject B. brassicae in favour of M. persicae during foraging. When presented at unequal abundances, naïve predators generally consumed each aphid species according to their initial relative abundance, although, predation of non‐defended prey was less than expected when defended prey were initially more abundant, indicating a high consumption of B. brassicae impeded M. persicae consumption. With experience, C. carnea maintained predation of both aphid species but consumed more M. persicae than B. brassicae, indicating a change in behaviour. 4. Although prey choice by C. carnea may change with experience of available prey, prey chemical defences do not appear to influence prey choice by naïve predators. This inability to avoid harmful prey could facilitate wider, indirect interactions. Myzus persicae may benefit where high consumption of B. brassicae hinders predators in the short term, and in the long term, increases predator mortality.     

Phylogenetic evidence for colour pattern convergence in toxic pitohuis: Müllerian mimicry in birds?

Bird species in the genus Pitohui are chemically defended by a potent neurotoxic alkaloid in their skin and feathers. The two most toxic pitohui species, the hooded pitohui (Pitohui dichrous) and the variable pitohui (Pitohui kirhocephalus), are sometimes strikingly patterned and, in certain portions of their geographical ranges, both species share a nearly identical colour pattern, whereas in other areas they do not. Müllerian mimicry (the mutual resemblance of two chemically defended prey species) is common in some other animal groups and Pitohui birds have been suggested as one of the most likely cases in birds. Here, we examine pitohui plumage evolution in the context of a well-supported molecular phylogeny and use a maximum likelihood approach to test for convergent evolution in coloration. We show that the 'mimetic' phenotype is ancestral to both species and that the resemblance in most races is better explained by a shared ancestry. One large clade of P. kirhocephalus lost this mimetic phenotype early in their evolution and one race nested deep within this clade appears to have re-evolved this phenotype. These latter findings are consistent with the hypothesis that Müllerian mimicry is driving the evolution for a similar colour pattern between P. dichrous, but only in this one clade of P. kirhocephalus     

The wave speed of intergradation zone in two-species lattice Müllerian mimicry model

A spatially explicit model is studied to analyse the movement of coupled clines in two-species Müllerian mimicry system as exemplified by the comimicking helicoiine butterflies in Central-South America Heliconius erato and Heliconius melpomene. In this system, a pair of comimicking wing patterns of two species (mimicry ring) is found in a geographical region but another pair of wing patterns is found in a different geographical region. The distribution of mimicry rings thus forms a spatial mosaic in a large geographical scale, and the mechanism responsible for their stable maintenance has been a long-standing question in evolutionary biology. We here examine the speed of the movement of boundaries that divide the regions inhabited by different mimetic morphs in each comimicking species, by assuming coupled two-state stochastic cellular automatons where the flipping rate of the site occupied by a mimetic morph depends on the local density of the same morph and of the comimicking morph in the other species. The speed of cline movement shows a complex dependence on the coupling parameter between mimetic species--greater coupling of comimicking morphs between species slows down the cline movement only when the reduction in predation rate exhibits diminishing return to the increase of local mimetic morph density. The analytical predictions are confirmed by the results of Monte Carlo simulations. The speed of advance is quite different from that predicted from the conventional reaction-diffusion model, indicating that demographic stochasticity plays a critical role in determining the speed of cline movement. We also examine if the spatial heterogeneity in migration rate can stably maintain clines.     

Conservative coevolution of Müllerian mimicry in a group of rift lake catfish

Biological mimicry has long been viewed as a powerful example of natural selection's ability to drive phenotypic evolution, although continuing debates surround the mechanisms leading to its development and the nature of these mimetic relationships. Müllerian mimicry, in which unpalatable species derive a mutual selective benefit through evolved phenotypic similarity, has alternatively been proposed to evolve through either a two-step process initiated by a large mutational change, or through continuous gradual evolution toward a common aposematic phenotype. I exposed a model predatory fish species to two species of endemic Lake Tanganyikan Synodontis to provide evidence for aposematism and the presence of Müllerian mimicry in these species. Predators quickly became conditioned to avoid the venomous catfish and did not discriminate between the two species when they were switched, supporting a hypothesis of functional Müllerian mimicry in this group of similarly colored fish. Ancestral state reconstructions and statistical comparisons of color pattern divergence in Tanganyikan Synodontis indicate that Müllerian mimicry in these catfish has developed through diversification of an aposematic common ancestor with subsequent conservative mutualistic coevolution among its daughter lineages, rather than advergent evolution of a mimic toward a nonrelated model, as assumed by widely accepted models of Müllerian mimicry evolution.     

Müllerian mimicry: an examination of Fisher's theory of gradual evolutionary change

In 1927, Fisher suggested that Müllerian mimicry evolution could be gradual and driven by predator generalization. A competing possibility is the so-called two-step hypothesis, entailing that Müllerian mimicry evolves through major mutational leaps of a less-protected species towards a better-protected, which sets the stage for coevolutionary fine-tuning of mimicry. At present, this hypothesis seems to be more widely accepted than Fisher's suggestion. We conducted individual-based simulations of communities with predators and two prey types to assess the possibility of Fisher's process leading to a common prey appearance. We found that Fisher's process worked for initially relatively similar appearances. Moreover, by introducing a predator spectrum consisting of several predator types with different ranges of generalization, we found that gradual evolution towards mimicry occurred also for large initial differences in prey appearance. We suggest that Fisher's process together with a predator spectrum is a realistic alternative to the two-step hypothesis and, furthermore, it has fewer problems with purifying selection. We also examined the factors influencing gradual evolution towards mimicry and found that not only the relative benefits from mimicry but also the mutational schemes of the prey types matter.     

Müllerian mimicry among bees and wasps: a review of current knowledge and future avenues of research

Many bees and stinging wasps, or aculeates, exhibit striking colour patterns or conspicuous coloration, such as black and yellow stripes. Such coloration is often interpreted as an aposematic signal advertising aculeate defences: the venomous sting. Aposematism can lead to Müllerian mimicry, the convergence of signals among different species unpalatable to predators. Müllerian mimicry has been extensively studied, notably on Neotropical butterflies and poison frogs. However, although a very high number of aculeate species harbour putative aposematic signals, aculeates are under-represented in mimicry studies. Here, we review the literature on mimicry rings that include bee and stinging wasp species. We report over a hundred described mimicry rings, involving a thousand species that belong to 19 aculeate families. These mimicry rings are found all throughout the world. Most importantly, we identify remaining knowledge gaps and unanswered questions related to the study of Müllerian mimicry in aculeates. Some of these questions are specific to aculeate models, such as the impact of sociality and of sexual dimorphism in defence levels on mimicry dynamics. Our review shows that aculeates may be one of the most diverse groups of organisms engaging in Müllerian mimicry and that the diversity of aculeate Müllerian mimetic interactions is currently under-explored. Thus, aculeates represent a new and major model system to study the evolution of Müllerian mimicry. Finally, aculeates are important pollinators and the global decline of pollinating insects raises considerable concern. In this context, a better understanding of the impact of Müllerian mimicry on aculeate communities may help design strategies for pollinator conservation, thereby providing future directions for evolutionary research.     

Reciprocity in predator–prey interactions: exposure to defended prey and predation risk affects intermediate predator life history and morphology

A vast body of literature exists documenting the morphological, behavioural and life history changes that predators induce in prey. However, little attention has been paid to how these induced changes feed back and affect the predators’ life history and morphology. Larvae of the phantom midge Chaoborus flavicans are intermediate predators in a food web with Daphnia pulex as the basal resource and planktivorous fish as the top predator. C. flavicans prey on D. pulex and are themselves prey for fish; as D. pulex induce morphological defences in the presence of C. flavicans this is an ideal system in which to evaluate the effects of defended prey and top predators on an intermediate consumer. We assessed the impact on C. flavicans life history and morphology of foraging on defended prey while also being exposed to the non-lethal presence of a top fish predator. We tested the basic hypothesis that the effects of defended prey will depend on the presence or absence of top predator predation risk. Feeding rate was significantly reduced and time to pupation was significantly increased by defended morph prey. Gut size, development time, fecundity, egg size and reproductive effort respond to fish chemical cues directly or significantly alter the relationship between a trait and body size. We found no significant interactions between prey morph and the non-lethal presence of a top predator, suggesting that the effects of these two biological factors were additive or singularly independent. Overall it appears that C. flavicans is able to substantially modify several aspects of its biology, and while some changes appear mere consequences of resource limitation others appear facultative in nature.