Selection for evasive mimicry imposed by an arthropod predator.

It has long been hypothesized that a species that is relatively easy to catch by predators may face selection to resemble a species that is harder to catch. Several experiments using avian predators have since supported this 'evasive mimicry' hypothesis. However, the sudden movement of artificial evasive prey in each of the above experiments may have startled the predators, generating an avoidance response unrelated to difficulty of capture. Additionally in the above experiments the catchability of prey was all or nothing, while in nature predators may occasionally catch evasive prey or fail to catch slower species, which might inhibit learning. Here, using mantids as predators, we conducted an experimental test of the evasive mimicry hypothesis that circumvents these limitations, using live painted calyptrate flies with modified evasive capabilities as prey. We found that mantids readily learned to avoid pursuing the more evasive prey types. Warning signals based on evasiveness and their associated mimicry may be widespread phenomena in nature. These findings not only further support its plausibility but demonstrate that even arthropod predators can select for it.

Habitat openness and predator abundance determine predation risk of warningly colored longhorn beetles (Cerambycidae) in temperate forest.

Organisms have evolved different defense mechanisms, such as crypsis and mimicry, to avoid detection and recognition by predators. A prominent example is Batesian mimicry, where palatable species mimic unpalatable or toxic ones, such as Clytini (Coleoptera: Cerambycidae) that mimic wasps. However, scientific evidence for the effectiveness of Batesian mimicry in Cerambycids in natural habitats is scarce. We investigated predation of warningly and nonwarningly colored Cerambycids by birds in a temperate forest using beetle dummies. Dummies mimicking Tetropium castaneum, Leptura aethiops, Clytus arietis, and Leptura quadrifasciata were exposed on standing and laying deadwood and monitored predation events by birds over one season. The 20 surveyed plots differed in their structural complexity and canopy openness due to different postdisturbance logging strategies. A total of 88 predation events on warningly colored beetle dummies and 89 predation events on nonwarningly colored beetle dummies did not reveal the difference in predation risk by birds. However, predation risk increased with canopy openness, bird abundance, and exposure time, which peaked in July. This suggests that environmental factors have a higher importance in determining predation risk of warningly and nonwarningly colored Cerambycidae than the actual coloration of the beetles. Our study showed that canopy openness might be important in determining the predation risk of beetles by birds regardless of beetles' warning coloration. Different forest management strategies that often modify canopy openness may thus alter predator-prey interactions.

Climate-induced phenological shifts in a Batesian mimicry complex.

Climate-induced changes in spatial and temporal occurrence of species, as well as species traits such as body size, each have the potential to decouple symbiotic relationships. Past work has focused primarily on direct interactions, particularly those between predators and prey and between plants and pollinators, but studies have rarely demonstrated significant fitness costs to the interacting, coevolving organisms. Here, we demonstrate that changing phenological synchrony in the latter part of the 20th century has different fitness outcomes for the actors within a Batesian mimicry complex, where predators learn to differentiate harmful "model" organisms (stinging Hymenoptera) from harmless "mimics" (hoverflies, Diptera: Syrphidae). We define the mimetic relationships between 2,352 pairs of stinging Hymenoptera and their Syrphidae mimics based on a large-scale citizen science project and demonstrate that there is no relationship between the phenological shifts of models and their mimics. Using computer game-based experiments, we confirm that the fitness of models, mimics, and predators differs among phenological scenarios, creating a phenologically antagonistic system. Finally, we show that climate change is increasing the proportion of mimetic interactions in which models occur first and reducing mimic-first and random patterns of occurrence, potentially leading to complex fitness costs and benefits across all three actors. Our results provide strong evidence for an overlooked example of fitness consequences from changing phenological synchrony.

Chemical Identity of Cuticular Lipid Components in the Mimetic Swallowtail Butterfly Papilio polytes.

The swallowtail Papilio polytes shows Batesian and female-limited polymorphic mimicry. In Japan, P. polytes females have two different forms: the cyrus form is non-mimetic and resembles males, whereas the polytes form mimics Pachliopta aristolochiae and Byasa (Atrophaneura) alcinous as unpalatable models. During mating, P. polytes males use cuticular lipids to distinguish non-mimetic females from conspecific males and sympatric sister species. In this study, we investigated whether compositional differences in cuticular lipids exist between mimetic and non-mimetic females of P. polytes and between mimetic females and their model species. The mimetic and non-mimetic females had nearly identical cuticular lipid profiles, which differed from those of males. The two model species exhibited sexually dimorphic and species-specific cuticular lipid compositions, which were distinctly different from those of mimetic P. polytes females. These results strongly suggest that P. polytes females maintain the identity of cuticular lipid profiles regardless of the mimicry type, and this feature helps males recognize mimetic females as the correct mating partners.

Coping with Danger and Deception: Lessons from Signal Detection Theory.

AbstractSignal detection theory (SDT) has been used to model optimal stimulus discrimination for more than four decades in evolutionary ecology. A popular standard model that maximizes payoff per encounter was recently criticized for being too simplistic, leading to erroneous predictions. We review a number of SDT models that have received less attention but have explicitly taken repeated encounters into account, focusing on prey choice, mate search, aggressive mimicry, and the aiding of kin. We show how these models can be seen as variants of a second standard model that can be analyzed in a unified framework. In contrast to the simpler model, in this second model a higher probability of an undesirable or dangerous event occurring may either decrease or increase the receiver's acceptance rates. In each instance, the latter outcome requires undesirable events to be undesirable in a relative rather than an absolute sense. Increasing the abundance of desirable signalers or the payoff from accepting them may also either raise or reduce acceptance rates. Our synthesis highlights fundamental similarities among models previously studied on a case-by-case basis and challenges some long-held beliefs. For example, some classic predictions of Batesian mimicry can be reversed when model prey are protected by low profitability rather than harmful defense.

Mimicry in motion and morphology: do information limitation, trade-offs or compensation relax selection for mimetic accuracy?

Many animals mimic dangerous or undesirable prey as a defence from predators. We would expect predators to reliably avoid animals that closely resemble dangerous prey, yet imperfect mimics are common across a wide taxonomic range. There have been many hypotheses suggested to explain imperfect mimicry, but comparative tests across multiple mimicry systems are needed to determine which are applicable, and which-if any-represent general principles governing imperfect mimicry. We tested four hypotheses on Australian ant mimics and found support for only one of them: the information limitation hypothesis. A predator with incomplete information will be unable to discriminate some poor mimics from their models. We further present a simple model to show that predators are likely to operate with incomplete information because they forage and make decisions while they are learning, so might never learn to properly discriminate poor mimics from their models. We found no evidence that one accurate mimetic trait can compensate for, or constrain, another, or that rapid movement reduces selection pressure for good mimicry. We argue that information limitation may be a general principle behind imperfect mimicry of complex traits, while interactions between components of mimicry are unlikely to provide a general explanation for imperfect mimicry.

The evolution and genetics of sexually dimorphic 'dual' mimicry in the butterfly Elymnias hypermnestra.

Sexual dimorphism is a major component of morphological variation across the tree of life, but the mechanisms underlying phenotypic differences between sexes of a single species are poorly understood. We examined the population genomics and biogeography of the common palmfly Elymnias hypermnestra, a dual mimic in which female wing colour patterns are either dark brown (melanic) or bright orange, mimicking toxic Euploea and Danaus species, respectively. As males always have a melanic wing colour pattern, this makes E. hypermnestra a fascinating model organism in which populations vary in sexual dimorphism. Population structure analysis revealed that there were three genetically distinct E. hypermnestra populations, which we further validated by creating a phylogenomic species tree and inferring historical barriers to gene flow. This species tree demonstrated that multiple lineages with orange females do not form a monophyletic group, and the same is true of clades with melanic females. We identified two single nucleotide polymorphisms (SNPs) near the colour patterning gene WntA that were significantly associated with the female colour pattern polymorphism, suggesting that this gene affects sexual dimorphism. Given WntA's role in colour patterning across Nymphalidae, E. hypermnestra females demonstrate the repeatability of the evolution of sexual dimorphism.

Increased speed of movement reduced identification of Batesian ant-mimicking spiders by surrogate predators.

In Batesian mimicry, the mimic gains protection from predators by imitating a noxious model. Some myrmecomorphic species use ants as models as ants have strong defensive capabilities. Ants are highly mobile models, and besides colour, shape, and size, mimics also imitate their movement. Yet, former studies focused mainly on static traits. Here, I tested the hypothesis that artificially increased speed of movement reduces the probability of the mimic being identified. First, images of 14 myrmecomorphic spider species and their models were used for humans to rank their mimetic accuracy. Humans were used as surrogate predators to obtain scores for each mimetic pair. In the second experiment, the effect of movement playback speed on the probability of identification was investigated, again using humans. Videos of mimics were played at different speeds, and the identification probability was recorded. While ants were correctly identified at any playback speed, the identification of myrmecomorphic spiders declined with increasing playback speed. In other words, the latency to correct identification increased with playback speed. Overall, mimics with higher accuracy scores were more difficult to identify while moving. The natural speed of movement of accurate mimics was similar to that of inaccurate ones. Movement is thus an important trait for myrmecomorphic species.

Looking for Mimicry in a Snake Assemblage Using Deep Learning.

Batesian mimicry is a canonical example of evolution by natural selection, popularized by highly colorful species resembling unrelated models with astonishing precision. However, Batesian mimicry could also occur in inconspicuous species and rely on subtle resemblance. Although potentially widespread, such instances have been rarely investigated, such that the real frequency of Batesian mimicry has remained largely unknown. To fill this gap, we developed a new approach using deep learning to quantify the visual resemblance between putative mimics and models from photographs. We applied this method to Western Palearctic snakes. Potential nonvenomous mimics were revealed by an excess of resemblance to sympatric venomous snakes compared with random expectations. We found that 8% of the nonvenomous species were potential mimics, although they resembled their models imperfectly. This study is the first to quantify the frequency of Batesian mimicry in a whole community of vertebrates, and it shows that even concealed species can act as potential models. Our approach should prove useful for detecting mimicry in other communities, and more generally it highlights the benefits of deep learning for quantitative studies of phenotypic resemblance.

Transformational Mimicry in a Myrmecomorphic Spider.

Species that are Batesian mimics during postembryonic development shift between mimetic models as they grow in size. However, it has not yet been tested whether these successive mimetic phenotypes are similarly protected from predators. Early-instar phenotypes could represent an inaccurate phenotype or an accurate phenotype because of selection from different predators. Here, we tested the hypotheses of transformational Batesian mimicry in the ant-mimicking jumping spider Leptochestes berolinensis. We quantified the mimetic accuracy of different ontogenetic stages to potential ant models by using a multitrait approach. We measured movement, body profile, body size, and coloration. Analysis revealed adults to be more accurate mimics than juveniles. Adults were similar to smaller morphs of Camponotus or Lasius ants, whereas juveniles were more similar to Lasius and Colobopsis ants. We tested whether predators, mantises, and Pisaura spiders were deceived by mimics after having experience with ant models. These predators never captured any ant or a mimic but always captured the nonmyrmecomorphic spider. We conclude that L. berolinensis is a Batesian mimic of ants undergoing transformational mimicry, with all stages being accurate mimics.

State-Dependent Decision-Making by Predators and Its Consequences for Mimicry.

AbstractThe mimicry of one species by another provides one of the most celebrated examples of evolution by natural selection. Edible Batesian mimics deceive predators into believing they may be defended, whereas defended Müllerian mimics have evolved a shared warning signal, more rapidly educating predators to avoid them. However, it may benefit hungry predators to attack defended prey, while the benefits of learning about unfamiliar prey depends on the future value of this information. Previous energetic state-dependent models of predator foraging behavior have assumed complete knowledge, while informational state-dependent models have assumed fixed levels of hunger. Here, we identify the optimal decision rules of predators accounting for both energetic and informational states. We show that the nature of mimicry is qualitatively and quantitatively affected by both sources of state dependence. Associative learning weakens the extent of parasitic mimicry by edible prey because naive predators often attack defended models. More importantly, mimicry among equally highly defended prey may be parasitic or mutualistic depending on the ecological context (e.g., the source of mimics and the abundance of alternative prey). Finally, mimicry by prey with intermediate defenses corresponds to Batesian or Müllerian mimicry depending on whether the mimic is profitable to attack by hungry predators, but it is not a special case of mimicry.

Mimicry diversification in Papilio dardanus via a genomic inversion in the regulatory region of engrailed-invected.

Polymorphic Batesian mimics exhibit multiple protective morphs that each mimic a different noxious model. Here, we study the genomic transitions leading to the evolution of different mimetic wing patterns in the polymorphic Mocker Swallowtail Papilio dardanus. We generated a draft genome (231 Mb over 30 chromosomes) and re-sequenced individuals of three morphs. Genome-wide single nucleotide polymorphism (SNP) analysis revealed elevated linkage disequilibrium and divergence between morphs in the regulatory region of engrailed, a developmental gene previously implicated in the mimicry switch. The diverged region exhibits a discrete chromosomal inversion (of 40 kb) relative to the ancestral orientation that is associated with the cenea morph, but not with the bottom-recessive hippocoonides morph or with non-mimetic allopatric populations. The functional role of this inversion in the expression of the novel phenotype is currently unknown, but by preventing recombination, it allows the stable inheritance of divergent alleles enabling geographic spread and local coexistence of multiple adaptive morphs.

How do predators generalize warning signals in simple and complex prey communities? Insights from a videogame.

The persistence of distinct warning signals within and between sympatric mimetic communities is a puzzling evolutionary question because selection favours convergence of colour patterns among toxic species. Such convergence is partly shaped by predators' reaction to similar but not identical stimulus (i.e. generalization behaviour), and generalization by predators is likely to be shaped by the diversity of local prey. However, studying generalization behaviour is generally limited to simple variations of prey colour patterns. Here, we used a computer game played by humans as surrogate predators to investigate generalization behaviours in simple (4 morphs) and complex (10 morphs) communities of unprofitable (associated with a penalty) and profitable butterflies. Colour patterns used in the game are observed in the natural populations of unprofitable butterfly species such as Heliconius numata. Analyses of 449 game participants' behaviours show that players avoided unprofitable prey more readily in simple than in complex communities. However, generalization was observed only in players that faced complex communities, enhancing the protection of profitable prey that looked similar to at least one unprofitable morph. Additionally, similarity among unprofitable prey also reduced attack rates only in complex communities. These results are consistent with previous studies using avian predators but artificial colour patterns and suggest that mimicry is more likely to evolve in complex communities where increases in similarity are more likely to be advantageous.

Multiple models generate a geographical mosaic of resemblance in a Batesian mimicry complex.

Batesian mimics-benign species that receive protection from predation by resembling a dangerous species-often occur with multiple model species. Here, we examine whether geographical variation in the number of local models generates geographical variation in mimic-model resemblance. In areas with multiple models, selection might be relaxed or even favour imprecise mimicry relative to areas with only one model. We test the prediction that model-mimic match should vary with the number of other model species in a broadly distributed snake mimicry complex where a mimic and a model co-occur both with and without other model species. We found that the mimic resembled its model more closely when they were exclusively sympatric than when they were sympatric with other model species. Moreover, in regions with multiple models, mimic-model resemblance was positively correlated with the resemblance between the model and other model species. However, contrary to predictions, free-ranging natural predators did not attack artificial replicas of imprecise mimics more often when only a single model was present. Taken together, our results suggest that multiple models might generate a geographical mosaic in the degree of phenotype matching between Batesian mimics and their models.

Frequency dependence shapes the adaptive landscape of imperfect Batesian mimicry.

Despite more than a century of biological research on the evolution and maintenance of mimetic signals, the relative frequencies of models and mimics necessary to establish and maintain Batesian mimicry in natural populations remain understudied. Here we investigate the frequency-dependent dynamics of imperfect Batesian mimicry, using predation experiments involving artificial butterfly models. We use two geographically distinct populations of Adelpha butterflies that vary in their relative frequencies of a putatively defended model (Adelpha iphiclus) and Batesian mimic (Adelpha serpa). We found that in Costa Rica, where both species share similar abundances, Batesian mimicry breaks down, and predators more readily attack artificial butterfly models of the presumed mimic, A. serpa By contrast, in Ecuador, where A. iphiclus (model) is significantly more abundant than A. serpa (mimic), both species are equally protected from predation. Our results provide compelling experimental evidence that imperfect Batesian mimicry is frequency-dependent on the relative abundance of models and mimics in natural populations, and contribute to the growing body of evidence that complex dynamics, such as seasonality or the availability of alternative prey, influence the evolution of mimetic traits.

Reciprocal mimicry: kin selection can drive defended prey to resemble their Batesian mimics.

Established mimicry theory predicts that Batesian mimics are selected to resemble their defended models, while models are selected to become dissimilar from their mimics. However, this theory has mainly considered individual selection acting on solitary organisms such as adult butterflies. Although Batesian mimicry of social insects is common, the few existing applications of kin selection theory to mimicry have emphasized relatedness among mimics rather than among models. Here, we present a signal detection model of Batesian mimicry in which the population of defended model prey is kin structured. Our analysis shows for most of parameter space that increased average dissimilarity from mimics has a twofold group-level cost for the model prey: it attracts more predators and these adopt more aggressive attack strategies. When mimetic resemblance and local relatedness are sufficiently high, such costs acting in the local neighbourhood may outweigh the individual benefits of dissimilarity, causing kin selection to drive the models to resemble their mimics. This requires model prey to be more common than mimics and/or well-defended, the conditions under which Batesian mimicry is thought most successful. Local relatedness makes defended prey easier targets for Batesian mimicry and is likely to stabilize the mimetic relationship over time.

Moving like a model: mimicry of hymenopteran flight trajectories by clearwing moths of Southeast Asian rainforests.

Clearwing moths are known for their physical resemblance to hymenopterans, but the extent of their behavioural mimicry is unknown. We describe zigzag flights of sesiid bee mimics that are nearly indistinguishable from those of sympatric bees, whereas sesiid wasp mimics display faster, straighter flights more akin to those of wasps. In particular, the flight of the sesiids Heterosphecia pahangensis, Aschistophleps argentifasciata and Pyrophleps cruentata resembles both Tetragonilla collina and T. atripes stingless bees and, to a lesser extent, dwarf honeybees Apis andreniformis, whereas the sesiid Pyrophleps sp. resembles Tachysphex sp. wasps. These findings represent the first experimental evidence for behavioural mimicry in clearwing moths.

Ant-like Traits in Wingless Parasitoids Repel Attack from Wolf Spiders.

A recent study showed that a wingless parasitoid, Gelis agilis, exhibits a suite of ant-like traits that repels attack from wolf spiders. When agitated, G. agilis secreted 6-methyl-5-hepten-2-one (sulcatone), which a small number of ant species produce as an alarm/panic pheromone. Here, we tested four Gelis parasitoid species, occurring in the same food chain and microhabitats, for the presence of sulcatone and conducted two-species choice bioassays with wolf spiders to determine their degree of susceptibility to attack. All four Gelis species, including both winged and wingless species, produced sulcatone, whereas a closely related species, Acrolyta nens, and the more distantly related Cotesia glomerata, did not. In two-choice bioassays, spiders overwhelmingly rejected the wingless Gelis species, preferring A. nens and C. glomerata. However, spiders exhibited no preference for either A. nens or G. areator, both of which are winged. Wingless gelines exhibited several ant-like traits, perhaps accounting for the reluctance of spiders to attack them. On the other hand, despite producing sulcatone, the winged G. areator more closely resembles other winged cryptines like A. nens, making it harder for spiders to distinguish between these two species. C. glomerata was also preferred by spiders over A. nens, suggesting that other non-sulcatone producing cryptines nevertheless possess traits that make them less attractive as prey. Phylogenetic reconstruction of the Cryptinae reveals that G. hortensis and G. proximus are 'sister'species, with G. agilis, and G.areator in particular evolving along more distant trajectories. We discuss the possibility that wingless Gelis species have evolved a suite of ant-like traits as a form, of mimicry to repel predators on the ground.

Evolutionary Assembly of Communities in Butterfly Mimicry Rings.

Species co-occurrence in ecological communities is thought to be influenced by multiple ecological and evolutionary processes, especially colonization and competition. However, effects of other interspecific interactions and evolutionary relationships are less explored. We examined evolutionary histories of community members and roles of mutualistic and parasitic interactions (Müllerian and Batesian mimicry, respectively) in the assembly of mimetic butterfly communities called mimicry rings in tropical forests of the Western Ghats, India. We found that Müllerian mimics were phylogenetically clustered, sharing aposematic signals due to common ancestry. On the other hand, Batesian mimics joined mimicry rings through convergent evolution and random phylogenetic assembly. Since the Western Ghats are a habitat island, we compared species diversity and composition in its mimicry rings with those of habitat mainland to test effects of biogeographic connectivity. The Western Ghats consisted of fewer mimicry rings and an overall smaller number of aposematic species and mimics compared to habitat mainland. The depauperate mimicry rings in the Western Ghats could have resulted from stochastic processes, reflecting their long temporal and spatial isolation and trickling colonization by the mimetic butterfly communities. These results highlight how evolutionary history, biogeographic isolation, and stochastic colonization influence the evolutionary assembly and diversity of ecological communities.

Mimicry among Unequally Defended Prey Should Be Mutualistic When Predators Sample Optimally.

Understanding the conditions under which moderately defended prey evolve to resemble better-defended prey and whether this mimicry is parasitic (quasi-Batesian) or mutualistic (Müllerian) is central to our understanding of warning signals. Models of predator learning generally predict quasi-Batesian relationships. However, predators' attack decisions are based not only on learning alone but also on the potential future rewards. We identify the optimal sampling strategy of predators capable of classifying prey into different profitability categories and contrast the implications of these rules for mimicry evolution with a classical Pavlovian model based on conditioning. In both cases, the presence of moderately unprofitable mimics causes an increase in overall consumption. However, in the case of the optimal sampling strategy, this increase in consumption is typically outweighed by the increase in overall density of prey sharing the model appearance (a dilution effect), causing a decrease in mortality. It suggests that if predators forage efficiently to maximize their long-term payoff, genuine quasi-Batesian mimicry should be rare, which may explain the scarcity of evidence for it in nature. Nevertheless, we show that when moderately defended mimics are profitable to attack by hungry predators, then they can be parasitic on their models, just as classical Batesian mimics are.