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.     

Feature saltation and the evolution of mimicry

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

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?     

NONCONSUMPTIVE PREDATOR‐DRIVEN MORTALITY CAUSES NATURAL SELECTION ON PREY

Predators frequently exert natural selection through differential consumption of their prey. However, predators may also cause prey mortality through nonconsumptive effects, which could cause selection if different prey phenotypes are differentially susceptible to this nonconsumptive mortality. Here we present an experimental test of this hypothesis, which reveals that nonconsumptive mortality imposed by predatory dragonflies causes selection on their damselfly prey favoring increased activity levels. These results are consistent with other studies of predator‐driven selection, however, they reveal that consumption alone is not the only mechanism by which predators can exert selection on prey. Uncovering this mechanism also suggests that prey defensive traits may represent adaptations to not only avoid being consumed, but also for dealing with other sources of mortality caused by predators. Demonstrating selection through both consumptive and nonconsumptive predator mortality provides us with insight into the diverse effects of predators as an evolutionary force.     

Predator–prey naïveté, antipredator behavior,and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non‐consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non‐native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non‐native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non‐consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non‐native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter‐related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non‐native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non‐native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.     

Adaptive evolution to novel predators facilitates the evolution of damselfly species range shifts

Most species have evolved adaptations to reduce the chances of predation. In many cases, adaptations to coexist with one predator generate tradeoffs in the ability to live with other predators. Consequently, the ability to live with one predator may limit the geographic distributions of species, such that adaptive evolution to coexist with novel predators may facilitate range shifts. In a case study with Enallagma damselflies, we used a comparative phylogenetic approach to test the hypothesis that adaptive evolution to live with a novel predator facilitates range size shifts. Our results suggest that the evolution of Enallagma shifting from living in ancestral lakes with fish as top predators, to living in lakes with dragonflies as predators, may have facilitated an increase in their range sizes. This increased range size likely arose because lakes with dragonflies were widespread, but unavailable as a habitat throughout much of the evolutionary history of Enallagma because they were historically maladapted to coexist with dragonfly predators. Additionally, the traits that have evolved as defenses against dragonflies also likely enhanced damselfly dispersal abilities. While many factors underlie the evolutionary history of species ranges, these results suggest a role for the evolution of predator‐prey interactions.     

An offensive predator phenotype selects for an amplified defensive phenotype in its prey

Inducible defenses of prey and inducible offenses of predators are examples of adaptive phenotypic plasticity. Although evolutionary ecologists have paid considerable attention to the adaptive significances of these strategies, they have rarely focused on their evolutionary impacts on the interacting species. Because the functional phenotypes of predator and prey determine strength of interactions between the species, the inducible plasticity can modify selective pressure on trait distribution and, ultimately, trait evolution in the interacting species. We experimentally tested this hypothesis in a predator–prey system composed of salamander larvae (Hynobius retardatus) and frog tadpoles (Rana pirica) capable of expressing antagonistic inducible offensive or defensive traits, an enlarged gape in the salamander larvae and a bulgy body in the tadpoles, when predator–prey interactions are strong. We examined selection strength on the tadpole’s defensive trait by comparing survival rates of tadpoles with different defensive levels under predation pressure from offensive or non-offensive salamander larvae. Survival rates of more-defensive tadpoles were greater than those of less-defensive tadpoles only when the tadpoles were exposed to offensive salamander larvae; thus, the predator’s offensive phenotype could select for an amplified defensive phenotype in their prey. As the expression of inducible offenses by H. retardatus larvae depends greatly on the composition of its ecological community, the inducible defensive bulgy morph of R. pirica tadpoles might have evolved in response to the variable expression of the H. retardatus offensive larval phenotype.     

Effects of predator-specific defence on biodiversity and community complexity in two-trophic-level communities

Summary Antipredator strategies employed by prey may be specific (effective against only one type of predator) or non-specific (effective against all predators). To examine the effects of the specificity of antipredator behaviour on biodiversity and community complexity, we analyse mathematical models including both evolutionary and population dynamics of a system including multiple prey species and multiple predator species. The models assume that all predator species change in their prey choice and all prey species have evolutionary change in their antipredator effort in evolution. The traits of each species change in an adaptive manner, whose rate is proportional to the slope of their fitness function. We calculate community complexity, resource-overlap between predators, an index of biodiversity and other properties of the coevolutionarily stable community for two cases: (1) all prey species have non-specific antipredator behaviour and (2) all prey species have predator-specific defence. Predator-specificity in defence increases community complexity, resource-overlap between predators, the total abundance of predators and the ratio of predator to prey abundance. Specific defence also decreases the number of isolated subwebs within the entire foodweb.     

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.     

Prey community structure affects how predators select for Mullerian mimicry

Müllerian mimicry describes the close resemblance between aposematic prey species; it is thought to be beneficial because sharing a warning signal decreases the mortality caused by sampling by inexperienced predators learning to avoid the signal. It has been hypothesized that selection for mimicry is strongest in multi-species prey communities where predators are more prone to misidentify the prey than in simple communities. In this study, wild great tits (Parus major) foraged from either simple (few prey appearances) or complex (several prey appearances) artificial prey communities where a specific model prey was always present. Owing to slower learning, the model did suffer higher mortality in complex communities when the birds were inexperienced. However, in a subsequent generalization test to potential mimics of the model prey (a continuum of signal accuracy), only birds that had foraged from simple communities selected against inaccurate mimics. Therefore, accurate mimicry is more likely to evolve in simple communities even though predator avoidance learning is slower in complex communities. For mimicry to evolve, prey species must have a common predator; the effective community consists of the predator's diet. In diverse environments, the limited diets of specialist predators could create 'simple community pockets' where accurate mimicry is selected for.     

The long‐term impacts of predators on prey: inducible defenses,population dynamics,and indirect effects

Despite the amount of research on the inducible defenses of prey against predators, our understanding of the long‐term significance of non‐lethal predators on prey phenotypes, prey population dynamics, and community structure has rarely been explored. Our objectives were to assess the effects of predators on prey defenses, prey population dynamics, and the relative magnitude of density‐ versus trait‐mediated indirect interactions (DMIIs and TMIIs) over multiple prey generations. Using a freshwater snail and three common snail predators, we constructed a series of community treatments with pond mesocosms that manipulated trophic structure, the identity of the top predator, and whether predators were caged or uncaged. We quantified snail phenotypes, snail population size, and resource abundance over multiple snail generations. We found that snails were expressing inducible defenses in our system although the magnitude of the responses varied over time and across predator species. Despite the expression of inducible defenses, caged predators did not reduce snail population size. There also was no evidence of TMIIs throughout the experiment suggesting that TMIIs have a minimal role in the long‐term structure of our communities. The absence of TMIIs was largely driven by the lack of predator‐induced reductions in resource consumption and the lack of consistent reductions in population size with predator cues. In contrast, we detected strong DMIIs associated with lethal predators suggesting that DMIIs are the dominant long‐term mechanism influencing community structure. Our results demonstrate that although predators can have significant effects on prey phenotypes and sometimes cause short‐term TMIIs, there may be few long‐term consequences of these responses on population dynamics and indirect interactions, at least within simple food webs. Research directed towards addressing the long‐term consequences of predator–prey interactions within communities will help to reveal whether the conclusions and predictions generated from short‐term experiments are applicable over ecological and evolutionary timescales.     

Both novelty and conspicuousness influence selection by mammalian predators on the colour pattern of Plethodon cinereus (Urodela: Plethodontidae)

Predators influence the evolution of colour pattern in prey species, yet how these selective forces might differ among predators is rarely considered. In particular, prey colour patterns that indicate unpalatability to some predator species may not carry the same signal for other predators. We test several hypotheses of selection on patterning between mammal predators and the polymorphic salamander Plethodon cinereus, which, under an avian visual system appears as a mimic of the toxic newt Notophthalmus viridescens. We fit each hypothesis against field observations of mammalian attacks on salamander clay replicas. We then develop a novel analytical procedure that enables the combination of multiple non‐exclusive models in a likelihood framework. We find that mammals do not follow any single hypothesis proposed, including the hypothesis of mimicry. Instead, mammals in this system use visual cues while foraging to avoid unfamiliar, novel prey and attack conspicuous prey. We propose that mammals may help to maintain colour pattern polymorphism within populations of P. cinereus by avoiding novel, unfamiliar colour morphs. Additionally, selective pressures from multiple predators and variation in predator communities among sites may contribute to the maintenance of colour polymorphism within and among localities in this salamander species.     

Evidence of weaker phenotypic plasticity by prey to novel cues from non‐native predators

A central question in evolutionary biology is how coevolutionary history between predator and prey influences their interactions. Contemporary global change and range expansion of exotic organisms impose a great challenge for prey species, which are increasingly exposed to invading non‐native predators, with which they share no evolutionary history. Here, we complete a comprehensive survey of empirical studies of coevolved and naive predator?prey interactions to assess whether a shared evolutionary history with predators influences the magnitude of predator‐induced defenses mounted by prey. Using marine bivalves and gastropods as model prey, we found that coevolved prey and predator‐naive prey showed large discrepancies in magnitude of predator‐induced phenotypic plasticity. Although naive prey, predominantly among bivalve species, did exhibit some level of plasticity – prey exposed to native predators showed significantly larger amounts of phenotypic plasticity. We discuss these results and the implications they may have for native communities and ecosystems.     

Evolutionary implications of the form of predator generalization for aposematic signals and mimicry in prey

Generalization is at the heart of many aspects of behavioral ecology; for foragers it can be seen as an essential feature of learning about potential prey, because natural populations of prey are unlikely to be perfectly homogenous. Aposematic signals are considered to aid predators in learning to avoid a class of defended prey. Predators do this by generalizing between the appearance of prey they have previously sampled and the appearance of prey they subsequently encounter. Mimicry arises when such generalization occurs between individuals of different species. Our aim here is to explore whether the specific shape of the generalization curve can be expected to be important for theoretical predictions relating to the evolution of aposematism and mimicry. We do this by a reanalysis and development of the models provided in two recent papers. We argue that the shape of the generalization curve, in combination with the nature of genetic and phenotypic variation in prey traits, can have evolutionary significance under certain delineated circumstances. We also demonstrate that the process of gradual evolution of Müllerian mimicry proposed by Fisher is particularly efficient in populations with a rich supply of standing genetic variation in mimetic traits.     

Fitness minimization and dynamic instability as a consequence of predator–prey coevolution

We analyse dynamic models of the coevolution of continuous traits that determine the capture rate of a prey species by a predator. The goal of the analysis is to determine conditions when the coevolutionary dynamics will be unstable and will generate population cycles. We use a simplified model of the evolutionary dynamics of quantitative traits in which the rate of change of the mean trait value is proportional to the rate of increase of individual fitness with trait value. Traits that increase ability in the predatory interaction are assumed to have negative effects on another component of fitness. We concentrate on the role of equilibrial fitness minima in producing cycles. In this case, the mean trait of a rapidly evolving species minimizes its fitness and it is chased around this equilibrium by adaptive evolution in the other species. Such cases appear to be most likely if the capture rate of prey by predators is maximal when predator and prey phenotypes match each other. They are possible, but less likely when traits in each species determine a one-dimensional axis of ability related to the interaction. Population dynamics often increase the range of parameter values for which cycles occur, relative to purely evolutionary models, although strong prey self-regulation may stabilize an evolutionarily unstable subsystem.     

Fitness minimization and dynamic instability as a consequence of predator-prey coevolution

Summary We analyse dynamic models of the coevolution of continuous traits that determine the capture rate of a prey species by a predator. The goal of the analysis is to determine conditions when the coevolutionary dynamics will be unstable and will generate population cycles. We use a simplified model of the evolutionary dynamics of quantitative traits in which the rate of change of the mean trait value is proportional to the rate of increase of individual fitness with trait value. Traits that increase ability in the predatory interaction are assumed to have negative effects on another component of fitness. We concentrate on the role of equilibrial fitness minima in producing cycles. In this case, the mean trait of a rapidly evolving species minimizes its fitness and it is chased around this equilibrium by adaptive evolution in the other species. Such cases appear to be most likely if the capture rate of prey by predators is maximal when predator and prey phenotypes match each other. They are possible, but less likely when traits in each species determine a one-dimensional axis of ability related to the interaction. Population dynamics often increase the range of parameter values for which cycles occur, relative to purely evolutionary models, although strong prey self-regulation may stabilize an evolutionarily unstable subsystem.     

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 evolution of multicomponent mimicry

The relative sizes of phenotypic mutations contributing to evolutionary change has long been the subject of debate. We describe how mimicry research can shed light on this debate, and frame mimicry studies within the general context of macromutationism and micromutationism, and punctuated versus gradual evolution. Balogh and Leimar [Müllerian mimicry: an examination of Fisher's theory of gradual evolutionary change. Proc. Roy. Soc. Lond. B Biol. Sci. 272, 2269-2275] have recently used a model to readdress the question of whether or not mimicry evolves gradually along a single dimension. We extend their approach, and present the first model to consider the effect of predator generalization along multiple components on the evolution of mimicry. We find that the gradual evolution of mimicry becomes increasingly less likely as the number of signal components increases, unless predators generalize widely over all components. However, we show that the contemporary two-step hypothesis (punctuated evolution followed by gradual refinement) can explain the evolution of Müllerian mimicry under all tested conditions. Thus, although the gradual evolution of mimicry is possible, the two-step hypothesis appears more generally applicable.     

Multi-trait mimicry and the relative salience of individual traits

Mimicry occurs when one species gains protection from predators by resembling an unprofitable model species. The degree of mimic–model similarity is variable in nature and is closely related to the number of traits that the mimic shares with its model. Here, we experimentally test the hypothesis that the relative salience of traits, as perceived by a predator, is an important determinant of the degree of mimic–model similarity required for successful mimicry. We manipulated the relative salience of the traits of a two-trait artificial model prey, and subsequently tested the survival of mimics of the different traits. The unrewarded model prey had two colour traits, black and blue, and the rewarded prey had two combinations of green, brown and grey shades. Blue tits were used as predators. We found that the birds perceived the black and blue traits to be similarly salient in one treatment, and mimic–model similarity in both traits was then required for high mimic success. In a second treatment, the blue trait was the most salient trait, and mimic–model similarity in this trait alone achieved high success. Our results thus support the idea that similar salience of model traits can explain the occurrence of multi-trait mimicry.     

The molecular basis of venom resistance in a rattlesnake‐squirrel predator‐prey system

Understanding how interspecific interactions mould the molecular basis of adaptations in coevolving species is a long‐sought goal of evolutionary biology. Venom in predators and venom resistance proteins in prey are coevolving molecular phenotypes, and while venoms are highly complex mixtures it is unclear if prey respond with equally complex resistance traits. Here, we use a novel molecular methodology based on protein affinity columns to capture and identify candidate blood serum resistance proteins (“venom interactive proteins” [VIPs]) in California Ground Squirrels (Otospermophilus beecheyi) that interact with venom proteins from their main predator, Northern Pacific Rattlesnakes (Crotalus o. oreganus). This assay showed that serum‐based resistance is both population‐ and species‐specific, with serum proteins from ground squirrels showing higher binding affinities for venom proteins of local snakes compared to allopatric individuals. Venom protein specificity assays identified numerous and diverse candidate prey resistance VIPs but also potential targets of venom in prey tissues. Many specific VIPs bind to multiple snake venom proteins and, conversely, single venom proteins bind multiple VIPs, demonstrating that a portion of the squirrel blood serum “resistome” involves broad‐based inhibition of nonself proteins and suggests that resistance involves a toxin scavenging mechanism. Analyses of rates of evolution of VIP protein homologues in related mammals show that most of these proteins evolve under purifying selection possibly due to molecular constraints that limit the evolutionary responses of prey to rapidly evolving snake venom proteins. Our method represents a general approach to identify specific proteins involved in co‐evolutionary interactions between species at the molecular level.