Evolution Of Mimicry Research Articles

Costs of Learning and the Evolution of Mimetic Signals.

Predators must use the appearance of their prey to decide whether it is likely to be defended. Most theory assumes that predators have completed learning about prey appearance, yet we do not understand how predators learn which aspects of appearance to use for classifying prey. If sampling prey can be risky, predators might forgo opportunities to learn about the relationship between prey appearance and defense. Using Bayesian inference and dynamic programming, we modeled how the immediate risks and future rewards of learning about prey appearance influence how predators learn. In addition, we explored how variation in predator learning affects the evolution of mimicry, which occurs when two prey evolve to share a common signal to predators. We found that when learning about prey with distinct appearances was expensive, optimal predators tended to lump them into the same category or exhibit an unwillingness to sample at all (neophobia). This resulted in a reduction in selection for defensive mimicry. However, the same predator behavior favored the evolution of aggressive mimicry, because in that case, mimics benefited from being sampled. When prey were very rare and costs of sampling them were high, predators exhibited neophobia, refusing to attack. This behavior could forestall the evolution of mimicry and instead select for polymorphism.

Model toxin level does not directly influence the evolution of mimicry in the salamander Plethodon cinereus

The resemblance between palatable mimics and unpalatable models in Batesian mimicry systems is tempered by many factors, including the toxicity of the model species. Model toxicity is thought to influence both the occurrence of mimicry and the evolution of mimetic phenotypes, such that mimicry is most likely to persist when models are particularly toxic. Additionally, model toxicity may influence the evolution of mimetic phenotype by allowing inaccurate mimicry to evolve through a mechanism termed ‘relaxed selection’. We tested these hypotheses in a salamander mimicry system between the model Notophthalmus viridescens and the mimic Plethodon cinereus, in which N. viridescens toxicity takes the form of tetrodotoxin. Surprisingly, though we discovered geographic variation in model toxin level, we found no support for the hypotheses that model toxicity directly influences either the occurrence of mimicry or the evolution of mimic phenotype. Instead, a link between N. viridescens size and toxicity may indirectly lead to relaxed selection in this mimicry system. Additionally, limitations of predator perception or variation in the rate of phenotypic evolution of models and mimics may account for the evolution of imperfect mimicry in this salamander species. Finally, variation in predator communities among localities or modern changes in environmental conditions may contribute to the patchy occurrence of mimicry in P. cinereus.

A global analysis of water and nitrogen relationships between mistletoes and their hosts: broad‐scale tests of old and enduring hypotheses

SummaryMistletoes use far more water per unit carbon fixed during photosynthesis than their hosts (i.e. they have lower ‘water use efficiency’,WUE). The widely cited ‘nitrogen‐parasitism hypothesis’ posits that N is the most limiting resource for mistletoes and that they use their faster transpiration rates to acquire sufficient N from the host xylem. In a rather different context, the ‘mimicry hypothesis’ arose in the literature suggesting that some mistletoes mimic the morphology of host leaves in order to deploy higher N leaves without suffering higher levels of herbivory. These two non‐exclusive hypotheses share the common goal of trying to explain patterns of mistletoe leaf N concentration.We set out to test the generality of both hypotheses at broad geographic scale using data for 168 mistletoes–host pairs, from 39 sites, encompassing all continents except Antarctica. We drew together data from published literature and our own field data on two key plant functional traits, leaf N concentration (Nmass) and leaf carbon isotopic composition (δ13C) (representing long‐termWUEand degree of stomatal control over photosynthesis).Key findings included (i) little or no support for the N‐parasitism hypothesis: differences in mistletoe and host Nmassexplained only 3% variation in differences in leaf δ13C, and mistletoe–host differences in leaf δ13C were unrelated to whether or not the hosts were N‐fixers (presumed to have higher N concentration in xylem sap); (ii) partial support for the mimicry hypothesis: mimic mistletoes generally had higher Nmasswhen associated with N‐fixing hosts (but, on non‐N‐fixing hosts there was no such pattern); and (iii) more broadly, mistletoes showed similar trait responses as their hosts to environmental drivers; for example, they showed similar‐magnitude shifts in Nmassand δ13C in relation to site aridity.Contrary to current belief, our findings suggest that nitrogen is not the limiting nutrient for mistletoes, at least not the main component driving the faster transpiration rates. Our results also give insight into the evolution of mimicry in mistletoes and show, for the first time, that mistletoes are also constrained by local water availability, exhibiting clear trait adaptations to environmental gradients. By reconsidering these issues at broad geographic scale and across a large number of species, our findings substantially modify current knowledge on the ecology and physiology of mistletoes and their hosts.

Gradual and contingent evolutionary emergence of leaf mimicry in butterfly wing patterns.

BackgroundSpecial resemblance of animals to natural objects such as leaves provides a representative example of evolutionary adaptation. The existence of such sophisticated features challenges our understanding of how complex adaptive phenotypes evolved. Leaf mimicry typically consists of several pattern elements, the spatial arrangement of which generates the leaf venation-like appearance. However, the process by which leaf patterns evolved remains unclear.ResultsIn this study we show the evolutionary origin and process for the leaf pattern in Kallima (Nymphalidae) butterflies. Using comparative morphological analyses, we reveal that the wing patterns of Kallima and 45 closely related species share the same ground plan, suggesting that the pattern elements of leaf mimicry have been inherited across species with lineage-specific changes of their character states. On the basis of these analyses, phylogenetic comparative methods estimated past states of the pattern elements and enabled reconstruction of the wing patterns of the most recent common ancestor. This analysis shows that the leaf pattern has evolved through several intermediate patterns. Further, we use Bayesian statistical methods to estimate the temporal order of character-state changes in the pattern elements by which leaf mimesis evolved, and show that the pattern elements changed their spatial arrangement (e.g., from a curved line to a straight line) in a stepwise manner and finally establish a close resemblance to a leaf venation-like appearance.ConclusionsOur study provides the first evidence for stepwise and contingent evolution of leaf mimicry. Leaf mimicry patterns evolved in a gradual, rather than a sudden, manner from a non-mimetic ancestor. Through a lineage of Kallima butterflies, the leaf patterns evolutionarily originated through temporal accumulation of orchestrated changes in multiple pattern elements.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-014-0229-5) contains supplementary material, which is available to authorized users.

Müllerian mimicry as a result of codivergence between velvet ants and spider wasps.

Recent studies have delineated a large Nearctic Müllerian mimicry complex in Dasymutilla velvet ants. Psorthaspis spider wasps live in areas where this mimicry complex is found and are phenotypically similar to Dasymutilla. We tested the idea that Psorthaspis spider wasps are participating in the Dasymutilla mimicry complex and that they codiverged with Dasymutilla. We performed morphometric analyses and human perception tests, and tabulated distributional records to determine the fit of Psorthaspis to the Dasymutilla mimicry complex. We inferred a dated phylogeny using nuclear molecular markers (28S, elongation factor 1-alpha, long-wavelength rhodopsin and wingless) for Psorthaspis species and compared it to a dated phylogeny of Dasymutilla. We tested for codivergence between the two groups using two statistical analyses. Our results show that Psorthaspis spider wasps are morphologically similar to the Dasymutilla mimicry rings. In addition, our tests indicate that Psorthaspis and Dasymutilla codiverged to produce similar color patterns. This study expands the breadth of the Dasymutilla Müllerian mimicry complex and provides insights about how codivergence influenced the evolution of mimicry in these groups.

Rejection of parasitic eggs in passerine hosts: Size matters more for a non-ejecter

The evolution of egg mimicry by parasites and the recognition of foreign eggs by hosts are important components of the coevolutionary arms race between brood parasites and their hosts, which is one of the most behaviorally complex of all host–parasite interactions. To examine cues used by the Yellow Warbler (Setophaga petechia), a non-ejecter that buries or deserts eggs laid by parasitic Brown-headed Cowbirds (Molothrus ater), we added model eggs of different sizes and colors to nests. We also reviewed the literature to investigate the effects of model egg surface color (background and maculation) and size on the response of hosts that eject. We predicted that size would be more important for Yellow Warblers as they likely use tactile cues to bury or desert parasitized clutches and color cannot be assessed tactilely. In Yellow Warblers, rejection frequency increased as size and color diverged more from real warbler eggs. Egg size was not generally used as a criterion for egg rejection, however, across different species that eject parasitic eggs. Color was the only model egg parameter, out of color and size, that significantly affected rejection in these ejecter hosts. Tactile cues are therefore not used by ejecters but are more important in a host that uses methods of rejection that do not require egg discrimination, such as burial and desertion. Of metrics that took into account the ultraviolet range, achromatic Just Noticeable Differences (brightness) in Yellow Warblers better predicted rejection of model eggs based on color than chromatic Just Noticeable Differences (hue). The high costs of burial and desertion may have led to multiple (size and color) egg discrimination abilities in the Yellow Warbler.

The evolution of molecular mimicry in parasites: a mathematical model

Parasite strains that are molecular mim¬ics are more likely to evade the immune system. When parasites evade a host’s the im¬mune system, their numbers grow, and these parasites are readily spread to new hosts. But, if molecular mimics are more transmissible, why is molecular mimicry then not more com-mon?

Rapid evolution of mimicry following local model extinction

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

Characterising the phenotypic diversity of Papilio dardanus wing patterns using an extensive museum collection.

The history of 20th Century evolutionary biology can be followed through the study of mimetic butterflies. From the initial findings of discontinuous polymorphism through the debates regarding the evolution of mimicry and the step-size of evolutionary change, to the studies on supergene evolution and molecular characterisation of butterfly genomes, mimetic butterflies have been at the heart of evolutionary thought for over 100 years. During this time, few species have received as much attention and in-depth study as Papilio dardanus. To assist all aspects of mimicry research, we present a complete data-derived overview of the extent of polymorphism within this species. Using historical samples permanently held by the NHM London, we document the extent of phenotypic variation and characterise the diversity present in each of the subspecies and how it varies across Africa. We also demonstrate an association between “imperfect” mimetic forms and the transitional race formed in the area where Eastern and Western African populations meet around Lake Victoria. We present a novel portal for access to this collection, www.mimeticbutterflies.org, allowing remote access to this unique repository. It is hoped that this online resource can act as a nucleus for the sharing and dissemination of other collections databases and imagery connected with mimetic butterflies.

Gradual and contingent evolutionary emergence of leaf mimicry in butterfly wing patterns

BackgroundSpecial resemblance of animals to natural objects such as leaves provides a representative example of evolutionary adaptation. The existence of such sophisticated features challenges our understanding of how complex adaptive phenotypes evolved. Leaf mimicry typically consists of several pattern elements, the spatial arrangement of which generates the leaf venation-like appearance. However, the process by which leaf patterns evolved remains unclear.ResultsIn this study we show the evolutionary origin and process for the leaf pattern in Kallima (Nymphalidae) butterflies. Using comparative morphological analyses, we reveal that the wing patterns of Kallima and 45 closely related species share the same ground plan, suggesting that the pattern elements of leaf mimicry have been inherited across species with lineage-specific changes of their character states. On the basis of these analyses, phylogenetic comparative methods estimated past states of the pattern elements and enabled reconstruction of the wing patterns of the most recent common ancestor. This analysis shows that the leaf pattern has evolved through several intermediate patterns. Further, we use Bayesian statistical methods to estimate the temporal order of character-state changes in the pattern elements by which leaf mimesis evolved, and show that the pattern elements changed their spatial arrangement (e.g., from a curved line to a straight line) in a stepwise manner and finally establish a close resemblance to a leaf venation-like appearance.ConclusionsOur study provides the first evidence for stepwise and contingent evolution of leaf mimicry. Leaf mimicry patterns evolved in a gradual, rather than a sudden, manner from a non-mimetic ancestor. Through a lineage of Kallima butterflies, the leaf patterns evolutionarily originated through temporal accumulation of orchestrated changes in multiple pattern elements.

Rapid evolution of mimicry following local model extinction

Rapid evolution of mimicry following local model extinction

PREDATOR PERCEPTION OF BATESIAN MIMICRY AND CONSPICUOUSNESS IN A SALAMANDER

In Batesian mimicry a palatable mimic deceives predators by resembling an unpalatable model. The evolution of Batesian mimicry relies on the visual capabilities of the potential predators, as prey detection provides the selective force driving evolutionary change. We compared the visual capabilities of several potential predators to test predictions stemming from the hypothesis of Batesian mimicry between two salamanders: the model species Notophthalmus viridescens, and polymorphic mimic, Plethodon cinereus. First, we found mimicry to be restricted to coloration, but not brightness. Second, only bird predators appeared able to discriminate between the colors of models and nonmimic P. cinereus. Third, estimates of salamander conspicuousness were background dependent, corresponding to predictions only for backgrounds against which salamanders are most active. These results support the hypothesis that birds influence the evolution of Batesian mimicry in P. cinereus, as they are the only group examined capable of differentiating N. viridescens and nonmimetic P. cinereus. Additionally, patterns of conspicuousness suggest that selection from predators may drive the evolution of conspicuousness in this system. This study confirms the expectation that the visual abilities of predators may influence the evolution of Batesian mimicry, but the role of conspicuousness may be more complex than previously thought.

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. Ranitomeyaimitator 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 Mullerian mimicry, but no prior empirical studies on learned avoidance by predators support this claim. In this study we used young chickens (Gallusdomesticus) as naive 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 Mullerian mimicry. Chickens exposed to either stimulus species demonstrated reciprocal learned avoidance; thus our results indicate that this complex functions as a Mullerian mimicry system. This study provides novel empirical evidence supporting predictions of the Mullerian 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.

Molecular evolution of protein-RNA mimicry as a mechanism for translational control

Elongation factor P (EF-P) is a conserved ribosome-binding protein that structurally mimics tRNA to enable the synthesis of peptides containing motifs that otherwise would induce translational stalling, including polyproline. In many bacteria, EF-P function requires post-translational modification with (R)-β-lysine by the lysyl-tRNA synthetase paralog PoxA. To investigate how recognition of EF-P by PoxA evolved from tRNA recognition by aminoacyl-tRNA synthetases, we compared the roles of EF-P/PoxA polar contacts with analogous interactions in a closely related tRNA/synthetase complex. PoxA was found to recognize EF-P solely via identity elements in the acceptor loop, the domain of the protein that interacts with the ribosome peptidyl transferase center and mimics the 3'-acceptor stem of tRNA. Although the EF-P acceptor loop residues required for PoxA recognition are highly conserved, their conservation was found to be independent of the phylogenetic distribution of PoxA. This suggests EF-P first evolved tRNA mimicry to optimize interactions with the ribosome, with PoxA-catalyzed aminoacylation evolving later as a secondary mechanism to further improve ribosome binding and translation control.

Imperfect Mimicry and the Limits of Natural Selection

Mimicry--when one organism (the mimic) evolves a phenotypic resemblance to another (the model) due to selective benefits--is widely used to illustrate natural selection's power to generate adaptations. However, many putative mimics resemble their models imprecisely, and such imperfect mimicry represents a specific challenge to mimicry theory and a general one to evolutionary theory. Here, we discuss 11 nonmutually exclusive hypotheses for imperfect mimicry. We group these hypotheses according to whether imperfect mimicry reflects: an artifact of human perception, which is not shared by any naturally occurring predators and therefore is not truly an instance of imperfect mimicry; genetic, developmental or time-lag constraints, which (temporarily) prevent a response to selection for perfect mimicry; relaxed selection, where imperfect mimicry is as adaptive as perfect mimicry; or tradeoffs, where imperfect mimicry is (locally) more adaptive than perfect mimicry. We find that the relaxed selection hypothesis has garnered the most support. However, because only a few study systems have thus far been comprehensively evaluated, the relative contributions of the various hypotheses toward explaining the evolution of imperfect mimicry remain unclear. Ultimately, clarifying why imperfect mimicry exists should provide critical insights into the limits of natural selection in producing complex adaptations.

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

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

Convergent specialization – the sharing of pollinators by sympatric genera of sexually deceptive orchids

Summary Pollinator sharing can offer powerful insights into the floral traits associated with the evolution of a pollination system and the consequences of floral differences for pollinator behaviour. Here, we investigate the first known case of pollinator sharing between two sexually deceptive plant genera. Floral manipulations were used to test the importance of floral traits for pollinator behaviour and pollination efficiency. We also explored the ecological differences enabling species co‐occurrence. Drakaea livida and Caladenia pectinata (Orchidaceae) exhibit dramatic differences in floral display and the insectiform appearance of the labellum, yet both are pollinated by sexually attracted males of the thynnine wasp Zaspilothynnis nigripes. Because of the prevalence of cryptic species in some genera of thynnine wasps, we confirmed pollinator sharing by a mark–recapture study and sequencing of the mtDNA CO1 region. Floral dissections revealed that semiochemicals used to attract the pollinator are released from the labellum in D. livida and sepaline clubs in C. pectinata. Drakaea livida was more efficient at converting pollinator attraction into potential pollen deposition leading to higher fruit set. Floral manipulations showed that pollinator contact with the labellum increases when it is the point of semiochemical release. However, sexual attraction to the labellum remained infrequent in C. pectinata in all experimental treatments. While their distribution and climatic range show extensive overlap, the differences in edaphic requirements of the two orchid species suggest that they rarely co‐occur. Therefore, the potential cost of sharing the same pollinator species is not realized. Synthesis. This case of pollinator sharing confirms that morphological traits do not place a strong constraint on the evolution of sexual deception. However, interspecific differences in floral traits have important consequences for converting attraction into pollination, suggesting that selection can act to increase efficiency at multiple steps of the pollination process. This system provides a novel opportunity to elucidate the chemical, visual and morphological adaptations underpinning the evolution of sexual mimicry.

Ecological and evolutionary processes drive the origin and maintenance of imperfect mimicry.

Although the forces behind the evolution of imperfect mimicry remain poorly studied, recent hypotheses suggest that relaxed selection on small-bodied individuals leads to imperfect mimicry. While evolutionary history undoubtedly affects the development of imperfect mimicry, ecological community context has largely been ignored and may be an important driver of imperfect mimicry. Here we investigate how evolutionary and ecological contexts might influence mimetic fidelity in Müllerian and Batesian mimicry systems. In Batesian hoverfly systems we find that body size is not a strong predictor of mimetic fidelity. However, in Müllerian velvet ants we find a weak positive relationship between body size and mimetic fidelity when evolutionary context is controlled for and a much stronger relationship between community diversity and mimetic fidelity. These results suggest that reduced selection on small-bodied individuals may not be a major driver of the evolution of imperfect mimicry and that other factors, such as ecological community context, should be considered when studying the evolution of imperfect mimicry.

Cryptic genetic and wing pattern diversity in a mimetic Heliconius butterfly.

Despite rampant colour pattern diversity in South America, Heliconius erato exhibits a 'postman' wing pattern throughout most of Central America. We examined genetic variation across the range of H. erato, including dense sampling in Central America, and discovered a deep genetic break, centred on the mountain range that runs through Costa Rica. This break is characterized by a novel mitochondrial lineage, which is nearly fixed in northern Central America, that branches basal to all previously described mitochondrial diversity in the species. Strong genetic differentiation also appears in Z-linked and autosomal markers, and it is further associated with a distinct, but subtle, shift in wing pattern phenotype. Comparison of clines in wing phenotype, mtDNA and nuclear markers indicate they are all centred on the mountains dividing Costa Rica, but that cline width differs among data sets. Phylogeographical analyses, accounting for this new diversity, rewrite our understanding of mimicry evolution in this system. For instance, these results suggest that H. erato originated west of the Andes, perhaps in Central America, and as many as 1 million years before its co-mimic, H. melpomene. Overall our data indicate that neutral genetic markers and colour pattern loci are congruent and converge on the same hypothesis-H. erato originated in northwest South America or Central America with a 'postman' phenotype and then radiated into the wealth of colour patterns present today.

Lepidopteran wing patterns and the evolution of satyric mimicry

The hypothesis of satyric mimicry postulates that the colour patterns of an animal may make its identity ambiguous, and this ambiguity interferes with the process of perception in vertebrate predators for a sufficient time to allow the potential prey to take evasive action. It has now been found that eyespots and other designs on the wings of many insect species are often coupled with other wing patterns and designs. These composite images often closely resemble heads and bodies of vertebrates (including birds and reptiles) and of various invertebrates. Such images can be perceived in living insects, although only rarely in set specimens because of displacement of the components. Visual processing by non-mammalian vertebrates generally involves attention to detail, suggesting that, at least initially, and unlike humans, they perceive embedded images on insect wings and bodies and ignore the whole or Gestalt. They are therefore likely to be confused by the ambiguity of the potential prey. It can be calculated that a delay of the order of only tenths of a second in the attack on a stationary insect by a predator could result in failure of capture. It is proposed in the present review that the concept of satyric mimicry be extended to include complex imagery of other organisms. Such iconic images, which often represent toxic or dangerous animals, are particularly common amongst saturniid moths and nymphalid and danaid butterflies (including the Monarch butterfly, Danaus plexippus). © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 203–214.