The Role of Predators in Maintaining the Geographic Organization of Aposematic Signals

Selective predation of aposematic signals is expected to promote phenotypic uniformity. But while these signals may be uniform within a population, numerous species display impressive variations in warning signals among adjacent populations. Predators from different localities who learn to avoid distinct signals while performing intense selection on others are thus expected to maintain such a geographic organization. We tested this assumption by placing clay frog models, representing distinct color morphs of the Peruvian poison dart frog Ranitomeya imitator and a nonconspicuous frog, reciprocally between adjacent localities. In each locality, avian predators were able to discriminate between warning signals; the adjacent exotic morph experienced up to four times more attacks than the local one and two times more than the nonconspicuous phenotype. Moreover, predation attempts on the exotic morph quickly decreased to almost nil, suggesting rapid learning. This experiment offers direct evidence for the existence of different predator communities performing localized homogenizing selection on distinct aposematic signals.

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title: The complex business of survival by aposematism.
abstract: The theory of warning signals dates back to Wallace but is still confusing, controversial and complex. Because predator avoidance of warningly coloured prey (aposematism) is based upon learning and reinforcement, it is difficult to understand how initially rare conspicuous forms subsequently become common. Here, we discuss several possible resolutions to this apparent paradox. Many of these ideas have been largely ignored as a result of implicit assumptions about predator behaviour and assumed lack of variation in the predators, prey and the predation process. Considering the spatial and temporal variation in and mechanisms of behaviour of both predators and prey will make it easier to understand the process and evolution of aposematism.

title: STRONG NATURAL SELECTION IN A WARNING‐COLOR HYBRID ZONE
abstract: Frequency‐dependent selection on warning color can maintain narrow hybrid zones between unpalatable prey taxa. To measure such selection, we transferred marked Heliconius erato (Lepidoptera: Nymphalidae) in both directions across a 10‐km‐wide hybrid zone between Peruvian races differing in color pattern. These experimental H. erato were released at four sites, along with control H. erato of the phenotype native to each site. Survival of experimental butterflies was significantly lower than that of controls at two sites and overall. Most selection, measured as differences in survival, occurred soon after release. Selection against foreign morphs was 52% (confidence limits: 25–71 %) and was probably due to bird attacks on unusual warning‐color morphs (more than 10% of the recaptures had beak marks). Since only three major loci determine the color‐pattern differences, this suggests an average selection coefficient of 0.17 per locus, sufficient to maintain the narrow clines in H. erato.

title: Three-butterfly system provides a field test of müllerian mimicry
abstract: In 1879, Müller proposed that two brightly coloured distasteful butterfly species (co-models) that share a single warning-colour pattern would benefit by spreading the selective burden of educating predators. The mutual benefit of sharing warning signals among distasteful species, so-called müllerian mimicry, is supported by comparative evidence, theoretical studies and laboratory simulations; however, to date, this key exemplar of adaptive evolution has not been experimentally tested in the field. To measure natural selection generated by müllerian mimicry, I exploited the unusual polymorphism of Heliconius cydno (Lepidoptera: Nymphalidae). Here I show increased survival of H. cydno morphs that match locally abundant monomorphic co-model species. This study demonstrates müllerian mimicry in the field. It also shows that müllerian mimicry with several co-models generates geographically divergent selection, which explains the existence of polymorphism in distasteful species with warning coloration.

title: Does Müllerian Mimicry Work in Nature? Experiments with Butterflies and Birds (Tyrannidae)1
abstract: The selective advantage of Mullerian mimicry in nature was investigated by releasing live mimetic and nonmimetic butterflies close to wild, aerial-hunting tropical kingbirds (Tyrannus melancholicus) and cliff-flycatchers (Hirundinea ferruginea) in three Amazon habitats (rain forest, a city, and “canga” vegetation). Only mimetic butterflies elicited sight-rejections by birds, but protection conferred by mimicry was restricted to sites in which both predators and mimics co-occurred, as in the case of six mimicry rings at a forest site and two at a city site. Most other Mullerian mimics released at city and canga vegetation were heavily attacked and consumed by birds. These results appear to reflect the birds' previous experiences with resident butterfly faunas and illustrate how birds' discriminatory behavior varied among habitats that differed in butterfly species and mimicry ring composition.

title: The genetic basis of an adaptive radiation: warning colour in two Heliconius species
abstract: Mimetic colour pattern races of Heliconius butterflies provide a striking example of adaptive radiation and numerous crossing experiments have investigated the genetics of these racial differences. However, colour pattern differentiation between closely related Heliconius species has not been previously studied. Here we present data from crosses between H. erato cyrbia and its sister species, H. himera. The genetic architecture underlying colour pattern divergence between these species is identical to that observed between races of H. erato. As in inter–racial crosses, colour pattern differences resulted from segregation at a few major loci. Evidence from 1321 offspring in 4 F1, 17 backcross, 7 F2 and 21 further crosses showed that two major loci controlled most of the colour pattern differences between H. erato and H. himera. There were strong interactions between these loci in their patterns of expression and evidence for other loci with relatively minor phenotypic effects. More importantly, based on patterns of expression within broods and linkage with Aconitase, we conclude that these major loci were homologous with those known to be responsible for colour pattern differences within H. erato. Our crosses also permit a re–evaluation of the relationships between colour pattern races of H. erato. This suggests that H. e. hydara, which occurs across a major mtDNA break, is the ancestral phenotype from which other races have evolved. Based on this assumption, we find no evidence to support the recent suggestion that apparently homologous colour pattern alleles have arisen multiple times.

title: A Müllerian mimicry ring in Appalachian millipedes
abstract: Few biological phenomena provide such an elegant and straightforward example of evolution by natural selection as color mimicry among unrelated organisms. By mimicking the appearance of a heavily defended aposematic species, members of a second species gain protection from predators and, potentially, enhanced fitness. Mimicking a preexisting warning advertisement is economical because a potentially costly novel one can be avoided; simultaneously, the addition of more aposematic individuals enhances the overall warning effect. The better-known mimetic systems comprise tropical taxa, but here, we show a remarkable example of color mimicry in 7 species of blind, cyanide-generating millipedes endemic to the Appalachian Mountains of temperate North America. Because these millipedes lack eyes, there is no sexual selection or intraspecific signaling for coloration, providing an ideal system for mimicry studies. We document a Müllerian symbiosis where unrelated species vary in color and pattern over geographical space but appear identical where they co-occur. By using spectral color data, estimations of evolutionary history, and detailed field observations of species abundance, we test 4 predictions of Müllerian mimicry theory and begin to unravel the story of an elaborate mimetic diversification in the forests of Appalachia.

title: Evolution of mimicry in the New World Dysdercus (Hemiptera: Pyrrhocoridae)
abstract: Evolution of mimicry rings is reconstructed for the New World species of cotton‐stainer bugs (Dysdercus, Hemiptera: Pyrrhocoridae). Using a cladistic analysis of 43 species (including D. silaceus Doesburg, 1968 stat. nov. and D. modestus Doesburg, 1968 stat. nov.), evolution of colour patterns and biogeographical history of the clade are hypothesized. Three probable mimicry rings are obtained from the analysis, together with data about their possible model–mimic or comimic–comimic structures: (a) ‘Yellow’ species in north‐western South America and in the Andes (several possible models, D. rusticus, D. mimus part., D. imitator part., and D. collaris part. as mimics); (b) ‘Median Yellow–Black’ species with a median‐forewing black pattern in north‐western South America and Central America (several possible models, D. basialbus as a mimic); (c) ‘Median Red–Black’ species with a median‐forewing black pattern in the Caribbean islands (D. andreae, D. discolor, D. neglectus–D. sanguinarius clade, and D. jamaicensis–D. fervidus–D. ocreatus clade as comimics). A few additional, less supported rings are also identified. Two highly polymorphic species (D. obscuratus, D. mimus) seem to enter different mimicry rings in different regions.

title: EVOLUTION OF MIMICRY PATTERNS IN METRIORRHYNCHUS (COLEOPTERA: LYCIDAE): THE HISTORY OF DISPERSAL AND SPECIATION IN SOUTHEAST ASIA
abstract: The concept of Müllerian mimicry suggests convergent evolution to an intermediate pattern and does not predict polymorphism in mimicry rings. We examined the evolution of mimicry patterns and the order of divergence of various factors, including the role of aposematic patterns in speciation, in a clade of net‐winged beetles with a robust phylogeny that suggests that they dispersed from the Australian to Asian plate. We found strong evidence for the evolution of mimicry via advergence in Metriorrhynchus because older patterns are represented in the Oriental region within more than 100 species of lycids from several lineages. Advergence was likely the cause of the observed intraspecific polymorphism in contrast to the predicted universal monomorphism. Polymorphism was found in populations of two species in Sumatra and Borneo and in populations fine‐tuned to subtle variants in various habitats. The advergence is likely to be based on the small population sizes of immigrants. The differences in population sizes result in much higher benefits for dispersing species than native populations. Speciation was trigged by the divergence in aposematic coloration, and the genetic differences accumulated slowly during incomplete isolation. We assumed that the differentiation in genitalia through sexual selection ultimately reinforced speciation initiated by the shift between mimicry patterns.

title: Molecular phylogenetic evidence for a mimetic radiation in Peruvian poison frogs supports a Müllerian mimicry hypothesis
abstract: Examples of Müllerian mimicry, in which resemblance between unpalatable species confers mutual benefit, are rare in vertebrates. Strong comparative evidence for mimicry is found when the colour and pattern of a single species closely resemble several different model species simultaneously in different geographical regions. Todemonstrate this, it is necessary to provide compelling evidence that the putative mimics do, in fact, form a monophyletic group. We present molecular phylogenetic evidence that the poison frog Dendrobates imitator mimics three different poison frogs in different geographical regions in Peru. DNA sequences from four different mitochondrial gene regions in putative members of a single species are analysed using parsimony, maximum-likelihood and neighbour-joining methods. The resulting hypotheses of phylogenetic relationships demonstrate that the different populations of D.imitator form a monophyletic group. To our knowledge, these results provide the first evidence for a Müllerian mimetic radiation in amphibians in which a single species mimics different sympatric species in different geographical regions.

title: Refugial isolation and secondary contact in the dyeing poison frog Dendrobates tinctorius
abstract: Recent palaeoclimactic research suggests that fluctuating environmental conditions throughout the Pleistocene of Amazonia occurred with previously unrecognized frequency. This has resulted in a theoretical shift from glacially influenced fluctuations to those driven by precessional rhythms. This theoretical revolution has a profound impact on expectations of biotic diversity within biogeographical regions that have long been based on the idea of large‐scale landscape fragmentation associated with increased aridity and glacial cycles. Generally speaking, this shifts phylogeographical expectations from that of (i) large areas of sympatry of closely related (but not sister) species whose origins lie in separate refugia, and current distributions are the results of cyclic connectivity of those two refugia (refuge hypothesis), to that of (ii) fine scale genetic structure, often associated with elevation, and divergence well below expected speciation levels [disturbance–vicariance (DV) hypothesis]. To date there have been few tests of the expectations of the DV hypothesis based on empirical studies of Neotropical floral and faunal communities. Herein we examine phylogeographical structure of Dendrobates tinctorius, an amphibian species endemic to the uplands of the eastern Guiana Shield, based on sampling of 114 individuals from 24 localities. Phylogenetic, nested clade, and dispersal–vicariance (DIVA) analyses of cytochrome b sequence data reveal the presence of two mitochondrial lineages that are associated with previously identified western and eastern uplands of this area. The geographical distribution of mitochondrial haplotypes and the results of DIVA and coalescent analyses suggest that there has been extensive secondary contact between these lineages indicating a complex history of connectivity between these western and eastern highlands, supporting the predictions of the DV hypothesis.

title: Rapid Color Evolution in an Aposematic Species: A Phylogenetic Analysis of Color Variation in the Strikingly Polymorphic Strawberry Poison-dart Frog
abstract: Aposematism is one of the great mysteries of evolutionary biology. The evolution of aposematic coloration is poorly understood, but even less understood is the evolution of polymorphism in aposematic signals. Here, we use a phylogeographic approach to investigate the evolution of color polymorphism in Dendrobates pumilio, a well-known poison-dart frog (family Dendrobatidae), which displays perhaps the most striking color variation of any aposematic species. With over a dozen color morphs, ranging from bright red to dull green, D. pumilio provides an ideal opportunity to examine the evolution of color polymorphism and evolutionary shifts to cryptic coloration in an otherwise aposematic species. We constructed a phylogenetic tree for all D. pumilio color morphs from 3051bp of mtDNA sequence data, reconstructed ancestral states using parsimony and Bayesian methods, and tested the recovered tree against constraint trees using parametric bootstrapping to determine the number of changes to each color type. We find strong evidence for nearly maximal numbers of changes in all color traits, including five independent shifts to dull dorsal coloration. Our results indicate that shifts in coloration in aposematic species may occur more regularly than predicted and that convergence in coloration may indicate that similar forces are repeatedly driving these shifts.

title: The evolution of a Müllerian mimic in a spatially distributed community.
abstract: Strong positive density-dependence should lead to a loss of diversity, but warning-colour and Müllerian mimicry systems show extraordinary levels of diversity. Here, we propose an analytical model to explore the dynamics of two forms of a Müllerian mimic in a heterogeneous environment with two alternative model species. Two connected populations of a dimorphic, chemically defended mimic are allowed to evolve and disperse. The proportions of the respective model species vary spatially. We use a nonlinear approximation of Müller's number-dependent equations to model a situation where the mortality for either form of the mimic decreases hyberbolically when its local density increases. A first non-spatial analysis confirms that the positive density-dependence makes coexistence of mimetic forms unstable in a single isolated patch, but shows that mimicry of the rarer model can be stable once established. The two-patch analysis shows that when models have different abundance in different places, local mimetic diversity in the mimic is maintained only if spatial heterogeneity is strong, or, more interestingly, if the mimic is not too strongly distasteful. Therefore, mildly toxic species can become polymorphic in a wider range of ecological settings. Spatial dynamics thus reveal a region of Müllerian polymorphism separating classical Batesian polymorphism and Müllerian monomorphism along the mimic's palatability spectrum. Such polymorphism-palatability relationship in a spatial environment provides a parsimonious hypothesis accounting for the observed Müllerian polymorphism that does not require quasi-Batesian dynamics. While the stability of coexistence depends on all factors, only the migration rate and strength of selection appear to affect the level of diversity at the polymorphic equilibrium. Local adaptation is predicted in most polymorphic cases. These results are in very good accordance with recent empirical findings on the polymorphic butterflies Heliconius numata and H. cydno.

title: Spatial mosaic formation through frequency-dependent selection in Müllerian mimicry complexes.
abstract: 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.

title: Mimicry on the edge: why do mimics vary in resemblance to their model in different parts of their geographical range?
abstract: Batesian mimics—benign species that predators avoid because they resemble a dangerous species—often vary geographically in resemblance to their model. Such geographical variation in mimic–model resemblance may reflect geographical variation in model abundance. Natural selection should favour even poor mimics where their model is common, but only good mimics where their model is rare. We tested these predictions in a snake-mimicry complex where the geographical range of the mimic extends beyond that of its model. Mimics on the edge of their model's range (where the model was rare) resembled the model more closely than did mimics in the centre of their model's range (where the model was common). When free-ranging natural predators on the edge of the model's range were given a choice of attacking replicas of good or poor mimics, they avoided only good mimics. By contrast, those in the centre of the model's range attacked good and poor mimics equally frequently. Generally, although poor mimics may persist in areas where their model is common, only the best mimics should occur in areas where their model is rare. Thus, counter-intuitively, the best mimics may occur on the edge of their model's range.

title: The role of predator selection on polymorphic aposematic poison frogs
abstract: Demonstrations of interactions between diverse selective forces on bright coloration in defended species are rare. Recent work has suggested that not only do the bright colours of Neotropical poison frogs serve to deter predators, but they also play a role in sexual selection, with females preferring males similar to themselves. These studies report an interaction between the selective forces of mate choice and predation. However, evidence demonstrating phenotypic discrimination by potential predators on these polymorphic species is lacking. The possibility remains that visual (avian) predators possess an inherent avoidance of brightly coloured diurnal anurans and purifying selection against novel phenotypes within populations is due solely to non-random mating. Here, we examine the influence of predation on phenotypic variation in a polymorphic species of poison frog, Dendrobates tinctorius. Using clay models, we demonstrate a purifying role for predator selection, as brightly coloured novel forms are more likely to suffer an attack than both local aposematic and cryptic forms. Additionally, local aposematic forms are attacked, though infrequently, indicating ongoing testing/learning and a lack of innate avoidance. These results demonstrate predator-driven phenotypic purification within populations and suggest colour patterns of poison frogs may truly represent a ‘magic trait’.

title: POSITIVE FREQUENCY‐DEPENDENT SELECTION ON WARNING COLOR IN ALPINE LEAF BEETLES
abstract: Müller's theory of warning color and mimicry, despite forming a textbook example of frequency‐dependent selection, has rarely been demonstrated in the wild. This may be largely due to the practical and statistical difficulties of measuring natural selection on mobile prey species. Here we demonstrate that this selection acts in alpine beetle communities by using tethered beetles exposed to natural predators. Oreina gloriosa leaf beetles (Coleoptera: Chrysomelidae) possess chemical defense in the form of cardenolides, accompanied by what appears to be warning color in bright metallic blues and greens. Individuals that match the locally predominant color morph have increased survival, with odds of week‐long survival increased by a factor of 1.67 over those that do not match. This corresponds to selection of 13% against foreign morphs. Such selection, acting in concert with variation in community composition, could be responsible for geographic variation in warning color. However, in the face of this purifying selection, the within‐population polymorphism seen in many Oreina species remains paradoxical.

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

title: Tracking the evolution of warning signals
abstract: EVOLUTIONARYstudies are hampered by a lack of experimental ways in which to test past events such as the origination of aposematism1–7, whereby unpalatable or poisonous prey signal their unprofitability, often by being warningly coloured. Inexperienced predators do learn to avoid unpalatable prey as a result of such signals8–10, but in addition there may be an inherited cautiousness about attacking when common or conspicuous warning signals are evident11–16. As current predators are not naive in the evolutionary sense, it is still not resolved3–7,17,18 whether aposematism originated only in aggregations of prey19,20 or among solitary prey as well21–23. Here we explore this controversy in evolutionarily naive predators by creating a novel world with warning signals not found in the environment. Initially, the aggregation of prey favoured the warning signals supporting Fisher's view24 of kin aggregations as the evolutionary starting point of aposematism. However, once predators had experienced warning signals, pre-existing avoidance seemed to facilitate evolution of Müllerian mimicry complexes25 with similar types of signals even among solitary prey.

title: Effects of novelty and gregariousness in survival of aposematic prey
abstract: We examined the reactions of captive wild great tits to novel unpalatable prey with (1) a traditional aposematic signal (black and yellow) (2) a novel signal (light pink), and (3) a control signal (brown). Prey were offered either singly or in groups to see whether novel signals with fewer possibilities for synergistic benefits are more dependent on grouping than are the traditional signals. Indeed, responses of birds toward unpalatable prey depended significantly on spatial distribution of prey (grouping versus solitary) and die type of die signal. Birds avoided more the traditional black and yellow signals than novel pink signals in both experimental set ups, but both of diese prey items survived better in aggregation than solitarily. The success of traditional signals may demonstrate the importance of synergistic selection across species in die evolution of warning coloration (Le., Mullerian mimicry). Unpalatable prey individuals benefit strongly from using irimilar color patterns. Our results suggest that aggregation may be important for die evolution of novel signals in particular, even if a synergistic selection component is also present Key words. Aposematism, great tit, gregariousness, novel signal, Parus major, traditional signal.

title: Multiple benefits of gregariousness cover detectability costs in aposematic aggregations
abstract: Understanding the early evolution of aposematic (warning) coloration has been a challenge for scientists, as a new conspicuous morph in a population of cryptic insects would have a high predation risk and would probably die out before local predators learnt to avoid it. Fisher presented the idea of aggregation benefit through the survival of related individuals; however, his theory has been strongly debated as the mechanisms that favour grouping have never been explored experimentally with the incorporation of detectability costs. Here we create a comprehensive ‘novel world’ experiment with the great tit (Parus major) as a predator to explore simultaneously the predation-related benefits and costs for aposematic aggregated prey, manipulating both group size and signal strength. Our results show that grouping would have been highly beneficial for the first aposematic prey individuals surrounded by naive predators, because (1) detectability risk increased only asymptotically with group size; (2) additional detectability costs due to conspicuous signals were marginal in groups; (3) even naive predators deserted the group after detecting unpalatability (dilution effect); and (4) avoidance learning of signal was faster in groups. None of these mechanisms require kin selection.

title: Co-mimics have a mutualistic relationship despite unequal defences
abstract: In the first clear mathematical treatment of natural selection, Müller proposed that a shared warning signal (mimicry) would benefit defended prey species by sharing out the per capita mortality incurred during predator education. Although mimicry is a mainstay of adaptationist thinking, there has been repeated debate on whether there is a mutualistic or a parasitic relationship between unequally defended co-mimic species. Here we show that the relationship between unequally defended species is mutualistic. We examined this in a ‘novel world’ of artificial prey with wild predators (great tit, Parus major). We kept the abundance of a highly defended prey (‘model’) constant and increased the density of a moderately defended prey (‘defended mimic’) of either perfect or imperfect mimetic resemblance to the model. Both model and defended mimic showed a net benefit from a density-dependent decrease in their per capita mortality. Even when the effect of dilution through density was controlled for, defended mimics did not induce additional attacks on the model, but we found selection for accurate signal mimicry. In comparison, the addition of fully edible (batesian) mimics did increase additional attacks on the model, but as a result of dilution this resulted in no overall increase in per capita mortality. By ignoring the effects of density, current theories may have overestimated the parasitic costs imposed by less defended mimics on highly defended models.

title: Experimental Evidence for Aposematism in the Dendrobatid Poison Frog Oophaga pumilio
abstract: Brightly colored poison frogs of the family Dendrobatidae contain an alkaloid-based chemical defense against predation. The bright coloration of these frogs is generally considered an aposematic signal to potential predators; however, relatively few studies have specifically tested this hypothesis. Herein we report the results of a field-based experiment designed to test the hypothesis of aposematism in the dendrobatid frog, Oophaga ( = Dendrobates) pumilio from the La Selva Biological Station, Costa Rica. We used plasticine frog models to evaluate natural predation rates as a function of color. Predation rates on brown models were almost twice that of red models, suggesting that predators avoid brightly colored frog models. Birds accounted for the majority of attacks on the models. The results of this study provide experimental evidence in support of the hypothesis that bright coloration in dendrobatids functions as an aposematic signal to predators.

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

title: Experimental Support for Aposematic Coloration in the Salamander Ensatina eschscholtzii xanthoptica: Implications for Mimicry of Pacific Newts
abstract: A field experiment was conducted to test the hypothesis that the plethodontid salamander Ensatina eschscholtzii xanthoptica benefits from aposematic coloration. Under field conditions, clay models painted to resemble E. e. xanthoptica were attacked significantly less often than models lacking the supposed aposematic colors. In addition, the head region of models was attacked significantly more frequently than random, suggesting the models were perceived as prey items. These results are consistent with the hypothesis that E. e. xanthoptica is a mimic of highly toxic Pacific Newts in the genus Taricha. The significance of the E. e. xanthoptica phenotype for the ring species biogeographic scenario and future research directions are briefly discussed.

title: Individual selection, kin selection, and the shifting balance in the evolution of warning colours: the evidence from butterflies
abstract: It is difficult to imagine how warning colours evolve in unpalatable prey. Firstly, novel warningly coloured variants gain no protection from their colours, since predators have not previously encountered and learnt their colour patterns. This leads to a frequency-dependent disadvantage of a rare variant within a species. Secondly, novel warningly coloured variants may be more conspicuous than non-aposematic prey. 
 
 
 
Nevertheless, it is obvious that many palatable butterflies have bright colours used in intraspecific communication and in duping predators. Other palatable butterflies are already warningly coloured. Should such butterflies evolve unpalatability, perhaps because of a host-plant shift, these bright colours would be preadapted to a warning role. Warning colours could then continue to evolve by enhancement of memorable characteristics of these patterns, or by mimicry. 
 
 
 
Even within lineages of warningly coloured, unpalatable butterflies, colour patterns have continued to evolve rapidly. This diversity of warning colour patterns could have evolved in a number of ways, including individual and kin selection, and by the shifting balance. Evidence for these mechanisms is discussed, as are the similarities between the evolution of warning colours and more general evolutionary processes, including sexual selection and speciation.

title: EVOLUTION OF DIVERSITY IN WARNING COLOR AND MIMICRY: Polymorphisms, Shifting
abstract: ▪ Abstract Mimicry and warning color are highly paradoxical adaptations. Color patterns in both Mullerian and Batesian mimicry are often determined by relatively few pattern-regulating loci with major effects. Many of these loci are “supergenes,” consisting of multiple, tightly linked epistatic elements. On the one hand, strong purifying selection on these genes must explain accurate resemblance (a reduction of morphological diversity between species), as well as monomorphic color patterns within species. On the other hand, mimicry has diversified at every taxonomic level; warning color has evolved from cryptic patterns, and there are mimetic polymorphisms within species, multiple color patterns in different geographic races of the same species, mimetic differences between sister species, and multiple mimicry rings within local communities. These contrasting patterns can be explained, in part, by the shape of a “number-dependent” selection function first modeled by Fritz Muller in 1879: Purifying selectio...

title: Estimates of selection and gene flow from measures of cline width and linkage disequilibrium in heliconius hybrid zones.
abstract: Hybrid zones can yield estimates of natural selection and gene flow. The width of a cline in gene frequency is approximately proportional to gene flow (sigma) divided by the square root of per-locus selection (square root of s). Gene flow also causes gametic correlations (linkage disequilibria) between genes that differ across hybrid zones. Correlations are stronger when the hybrid zone is narrow, and rise to a maximum roughly equal to s. Thus cline width and gametic correlations combine to give estimates of gene flow and selection. These indirect measures of sigma and s are especially useful because they can be made from collections, and require no field experiments. The method was applied to hybrid zones between color pattern races in a pair of Peruvian Heliconius butterfly species. The species are Müllerian mimics of one another, and both show the same changes in warning color pattern across their respective hybrid zones. The expectations of cline width and gametic correlation were generated using simulations of clines stabilized by strong frequency-dependent selection. In the hybrid zone in Heliconius erato, clines at three major color pattern loci were between 8.5 and 10.2 km wide, and the pairwise gametic correlations peaked at R approximately 0.35. These measures suggest that s approximately 0.23 per locus, and that sigma approximately 2.6 km. In erato, the shapes of the clines agreed with that expected on the basis of dominance. Heliconius melpomene has a nearly coincident hybrid zone. In this species, cline widths at four major color pattern loci varied between 11.7 and 13.4 km. Pairwise gametic correlations peaked near R approximately 1.00 for tightly linked genes, and at R approximately 0.40 for unlinked genes, giving s approximately 0.25 per locus and sigma approximately 3.7 km. In melpomene, cline shapes did not perfectly fit theoretical shapes based on dominance; this deviation might be explained by long-distance migration and/or strong epistasis. Compared with erato, sample sizes in melpomene are lower and the genetics of its color patterns are less well understood. In spite of these problems, selection and gene flow are clearly of the same order of magnitude in the two species. The relatively high per locus selection coefficients agree with "major gene" theories for the evolution of Müllerian mimicry, but the genetic architecture of the color patterns does not. These results show that the genetics and evolution of mimicry are still only sketchily understood.

title: SPECIALIZED AVIAN PREDATORS REPEATEDLY ATTACK NOVEL COLOR MORPHS OF HELICONIUS BUTTERFLIES
abstract: The persistence of Müllerian mimicry and geographically distinct wing patterns, as observed in many Heliconius species (Lepidoptera: Nymphalidae), is difficult to explain from a predator’s perspective: predator selection against locally rare patterns must persist despite avoidance learning. Maintaining spatial color-pattern polymorphism requires local pattern avoidance, fine-scale discrimination among similar wing patterns, and repeated attacks on novel color patterns. I tested for these behaviors by presenting 80 adult rufous-tailed jacamars (Galbula ruficauda) with three morphs of Heliconius butterflies, and then presenting the same suite of butterflies to 46 of these jacamars between four and 429 days later. These trials offer the first direct evidence of the selective predator behavior required to maintain aposematic polymorphism: jacamars avoid local aposematic morphs while repeatedly attacking similar but novel morphs over time.

title: Can experienced birds select for Müllerian mimicry
abstract: Field experiments have shown that avian predators in the wild can select for similarity of warning signals in aposematic prey (Mullerian mimicry) because a common signal is better protected than a signal that is novel and rare. The original theory of Mullerian mimicry assumes that the mechanism promoting mimicry is predator learning; by sharing a signal, the comimic species share the mortality that is due to sampling by inexperienced predators. Predation events have not been observed in the wild, and learning experiments with naive bird predators in a laboratory have not unambiguously shown a benefit of a uniform signal compared with different signals. As predators in the field experiments are likely to be more experienced compared with previous laboratory experiments, we studied selection by experienced predators on a novel imperfect mimic. We trained great tits Parus major to avoid artificial aposematic models and subsequently introduced perfect and imperfect mimics at different frequencies. Birds with prior experience on the models selected against the imperfect mimics that were at a disadvantage also in a memory test conducted a week after their introduction. Selection against the imperfect mimics was antiapostatic. However, the imperfect mimics also benefited from some signal generalization to the models and possibly gained protection because the birds were familiar with the alternative cryptic prey that was also present. Our results suggest that experienced predators might be more important to the evolution of mimicry than the learning-based theory assumes.

title: Shift happens! Shifting balance and the evolution of diversity in warning colour and mimicry
abstract: 1. At first sight, it seems most unlikely that Heliconius warning colour races have evolved by means of stochastic peak shift or shifting balance.

title: Learning to avoid aposematic prey
abstract: The evolution of prey warning coloration is, literally, a textbook example of Darwinian adaptive evolution by natural selection. The cornerstone of this evolutionary process is a predation event, the dynamics of which are poorly understood. Aposematic (warningly coloured) prey are relatively unpalatable and their conspicuous appearance should enable predators to avoid them, but such is not always the case. Based on models of conditioned learning, it has been assumed that the number of aposematic prey that a predator will attack as it learns to avoid such prey should be constant or declining as the prey's abundance increases. However, empirical studies have shown that predators make more attacks on aposematic prey when those prey are more common. I suggest that this failure of theory to predict behaviour probably arises from limitations of the learning models in question. Rather than using mechanistic models of conditioned learning, I used signal detection theory to provide a functional characterization of the uncertainty that inexperienced predators encounter when learning to distinguish prey types. This characterization explains otherwise puzzling data on predation on aposematic prey and can offer insight on the selective pressures driving the evolution of aposematism and mimicry.

title: Warning signals, receiver psychology and predator memory
abstract: This review identifies four receiver psychology perspectives that are likely to be important in the design and evolution of warning signals. Three of these perspectives (phobia, learning and prey recognition) have been studied in detail, and I include a brief review of recent work. The fourth, a memory perspective, has received little attention and is developed here. A memory perspective asks, 'how might warning signals function to reduce forgetting of avoidances between encounters?'. To answer this question I review data from psychology literature that describe important features of animal long-term memory. These data suggest that components of warning signals may function to reduce forgetting (and therefore increase memorability) by (1) preventing forgetting of learnt prey discriminations; (2) jogging the memories of forgetful predators; and (3) biasing forgetting in favour of prey avoidance when the warning signal of a defended aposematic species is copied by an edible Batesian mimic. A combination of a learning and a memory perspective suggests that the features of aposematic prey that accelerate avoidance learning may also be the features that decelerate forgetting processes. If correct, this would have important implications for the comprehension of signal design. Finally, I suggest that the cryptic appearance of an edible prey may decelerate predator learning and accelerate predator forgetting, to the benefit of the prey. In terms of learning and memory, crypsis may be an antisignal.

title: The evolution of müllerian mimicry in multispecies communities
abstract: Prey species that are unprofitable to attack often share conspicuous colours and patterns with other coexisting defended species. This phenomenon, termed müllerian mimicry, has long been explained as a consequence of selection on defended prey to adopt a common way of advertising their unprofitability. However, studies using two unpalatable prey types have not always supported this theory. Here we show, using a system of humans hunting for computer-generated prey, that predators do not always generate strong selection for mimicry when there are two unprofitable prey types. By contrast, we demonstrate that when predators are faced with a range of different prey species, selection on unprofitable prey to resemble one another can be intense. Here the primary selective force is not one in which predators evaluate the profitabilities of distinct prey types independently, but one in which predators learn better to avoid unprofitable phenotypes that share traits distinguishing them from profitable prey. This need to simplify decision making readily facilitates the spread of imperfect mimetic forms from rarity, and suggests that müllerian mimicry is more likely to arise in multispecies communities.

title: Frequency‐dependent selection on aposematic prey: some experiments
abstract: Experiments to measure the strength of frequency-dependent selection on dimorphic populations of distasteful, brightly coloured prey were carried out, using pastry cylinders as prey and wild birds as predators. When the two forms were haphazardly intermingled, the birds took a relative excess of whichever form happened to be the rarer if all prey in the population were distasteful but selected the forms independently of frequency if they were all neutral in flavour. They did not take an excess of the rarer form from populations of distasteful prey when that form was distributed in a single clump rather than evenly dispersed among the commoner form. This confirms the expectation that rarer forms of aposematic animals are at a frequency-dependent disadvantage when they are intermingled with commoner forms but not when they occur in clusters.

title: Reproductive isolation caused by colour pattern mimicry
abstract: Speciation is facilitated if ecological adaptation directly causes assortative mating, but few natural examples are known. Here we show that a shift in colour pattern mimicry was crucial in the origin of two butterfly species. The sister species Heliconius melpomene and Heliconius cydno recently diverged to mimic different model taxa, and our experiments show that their mimetic coloration is also important in choosing mates. Assortative mating between the sister species means that hybridization is rare in nature, and the few hybrids that are produced are non-mimetic, poorly adapted intermediates. Thus, the mimetic shift has caused both pre-mating and post-mating isolation. In addition, individuals from a population of H. melpomene allopatric to H. cydno court and mate with H. cydno more readily than those from a sympatric population. This suggests that assortative mating has been enhanced in sympatry.

title: Advergence in Müllerian mimicry: the case of the poison dart frogs of Northern Peru revisited
abstract: Whether the evolution of similar aposematic signals in different unpalatable species (i.e. Müllerian mimicry) is because of phenotypic convergence or advergence continues to puzzle scientists. The poison dart frog Ranitomeya imitator provides a rare example in support of the hypothesis of advergence: this species was believed to mimic numerous distinct model species because of high phenotypic variability and low genetic divergence among populations. In this study, we test the evidence in support of advergence using a population genetic framework in two localities where R. imitator is sympatric with different model species, Ranitomeya ventrimaculata and Ranitomeya variabilis. Genetic analyses revealed incomplete sorting of mitochondrial haplotypes between the two model species. These two species are also less genetically differentiated than R. imitator populations on the basis of both mitochondrial and nuclear DNA comparisons. The genetic similarity between the model species suggests that they have either diverged more recently than R. imitator populations or that they are still connected by gene flow and were misidentified as different species. An analysis of phenotypic variability indicates that the model species are as variable as R. imitator. These results do not support the hypothesis of advergence by R. imitator. Although we cannot rule out phenotypic advergence in the evolution of Müllerian mimicry, this study reopens the discussion regarding the direction of the evolution of mimicry in the R. imitator system.