Biased predation could promote convergence yet maintain diversity within Müllerian mimicry rings of Oreina leaf beetles

Müllerian mimicry is a classic example of adaptation, yet Müller's original theory does not account for the diversity often observed in mimicry rings. Here, we aimed to assess how well classical Müllerian mimicry can account for the colour polymorphism found in chemically defended Oreina leaf beetles by using field data and laboratory assays of predator behaviour. We also evaluated the hypothesis that thermoregulation can explain diversity between Oreina mimicry rings. We found that frequencies of each colour morph were positively correlated among species, a critical prediction of Müllerian mimicry. Predators learned to associate colour with chemical defences. Learned avoidance of the green morph of one species protected green morphs of another species. Avoidance of blue morphs was completely generalized to green morphs, but surprisingly, avoidance of green morphs was less generalized to blue morphs. This asymmetrical generalization should favour green morphs: indeed, green morphs persist in blue communities, whereas blue morphs are entirely excluded from green communities. We did not find a correlation between elevation and coloration, rejecting thermoregulation as an explanation for diversity between mimicry rings. Biased predation could explain within‐community diversity in warning coloration, providing a solution to a long‐standing puzzle. We propose testable hypotheses for why asymmetric generalization occurs, and how predators maintain the predominance of blue morphs in a community, despite asymmetric generalization.     

Defining the colour pattern phenotype in bumble bees (Bombus): a new model for evo devo

Few insects exhibit the striking colour pattern radiation found in bumble bees (Bombus), which have diversified globally into a wide range of colours and patterns. Their potent sting is often advertised by conspicuous bands of contrasting colour commonly mimicked by scores of harmless (Batesian mimics) and noxious species (Müllerian co‐mimics). Despite extensive documentation of colour pattern diversification, next to nothing is known about the genetic regulation of pattern formation in bumble bees, hindering progress toward a more general model of the evolution of colour pattern mimicry. A critical first step in understanding the colour pattern genotype is an unambiguous understanding of the phenotype under selection, which has not been objectively defined in bumble bees. Here, we quantitatively define the principal colour pattern elements that comprise the phenotype array across all species. Matrix analysis of meticulously scored colour patterns of ～95% of described species indicates there are 12 discrete primary ‘ground plan’ elements in common among all species, many of which correspond to segmentation patterning. Additional secondary elements characterize individual species and geographical variants. The boundaries of these elements appear to correspond to expression patterns of Hox genes in Drosophila and Apis but also suggest novel post‐Hox specialization of abdominal patterning. Our findings provide the first foundation for exploring candidate genes regulating adaptive pattern variation in bumble bees and broaden the framework for understanding common genetic mechanisms of pattern evolution in insects. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 384–404.     

The distribution of bumblebee colour patterns worldwide: possible significance for thermoregulation, crypsis, and warning mimicry

Bumblebee colour patterns can be highly variable within species, but are often closely similar among species. The present study takes a quantitative approach to survey bumblebee colour patterns in order to address some of the most basic questions concerning resemblances: (1) do colour‐pattern groups exist; (2) are species within colour‐pattern groups geographically clumped; and (3) are some colour‐pattern groups associated with particular kinds of habitat? The results using data for 632 worker patterns from all of the world’s bumblebee species show that: (1) there are many repeating colour patterns, forming relatively few groups of species with similar patterns; (2) colour‐pattern groups can be recognized using simple rules; and (3) species within the 24 largest colour‐pattern groups are significantly aggregated in particular areas of the world. Three principal divisions of colour‐pattern groups are associated with three likely functions: (1) the darkest bumblebees are associated primarily with the tropics, where a thermoregulatory function is suggested; (2) the palest bumblebees are associated with intermediate northern latitudes, where a cryptic function in drying grasslands is suggested; and (3) the intermediate, strongly banded bumblebees are widespread, although these patterns predominate where banding may have advantages as collective warning signals to predators (Müllerian mimicry). Further studies are needed to test these explanations. © The Natural History Museum, London. Journal compilation © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92 , 97–118.     

Mutualistic mimicry enhances species diversification through spatial segregation and extension of the ecological niche space

Species richness varies among clades, yet the drivers of diversification creating this variation remain poorly understood. While abiotic factors likely drive some of the variation in species richness, ecological interactions may also contribute. Here, we examine one class of potential contributors to species richness variation that is particularly poorly understood: mutualistic interactions. We aim to elucidate large‐scale patterns of diversification mediated by mutualistic interactions using a spatially explicit population‐based model. We focus on mutualistic Müllerian mimicry between conspicuous toxic prey species, where convergence in color patterns emerges from predators' learning process. To investigate the effects of Müllerian mimicry on species diversification, we assume that some speciation events stem from shifts in ecological niches, and can also be associated with shift in mimetic color pattern. Through the emergence of spatial mosaics of mimetic color patterns, Müllerian mimicry constrains the geographical distribution of species and allows different species occupying similar ecological niches to exist simultaneously in different regions. Müllerian mimicry and the resulting spatial segregation of mimetic color patterns thus generate more balanced phylogenetic trees and increase overall species diversity. Our study sheds light on complex effects of Müllerian mimicry on ecological, spatial, and phylogenetic diversification.     

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

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

Molecular mechanisms of dominance evolution in Müllerian mimicry

Natural selection acting on dominance between adaptive alleles at polymorphic loci can be sufficiently strong for dominance to evolve. However, the molecular mechanisms underlying such evolution are generally unknown. Here, using Müllerian mimicry as a case‐study for adaptive morphological variation, we present a theoretical analysis of the invasion of dominance modifiers altering gene expression through different molecular mechanisms. Toxic species involved in Müllerian mimicry exhibit warning coloration, and converge morphologically with other toxic species of the local community, due to positive frequency‐dependent selection acting on these colorations. Polymorphism in warning coloration may be maintained by migration–selection balance with fine scale spatial heterogeneity. We modeled a dominance modifier locus altering the expression of the warning coloration locus, targeting one or several alleles, acting in cis or trans, and either enhancing or repressing expression. We confirmed that dominance could evolve when balanced polymorphism was maintained at the color locus. Dominance evolution could result from modifiers enhancing one allele specifically, irrespective of their linkage with the targeted locus. Nonspecific enhancers could also persist in populations, at frequencies tightly depending on their linkage with the targeted locus. Altogether, our results identify which mechanisms of expression alteration could lead to dominance evolution in polymorphic mimicry.     

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

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

Müllerian mimicry of a quantitative trait despite contrasting levels of genomic divergence and selection

Hybrid zones, where distinct populations meet and interbreed, give insight into how differences between populations are maintained despite gene flow. Studying clines in genetic loci and adaptive traits across hybrid zones is a powerful method for understanding how selection drives differentiation within a single species, but can also be used to compare parallel divergence in different species responding to a common selective pressure. Here, we study parallel divergence of wing colouration in the butterflies Heliconius erato and H. melpomene, which are distantly related Müllerian mimics which show parallel geographic variation in both discrete variation in pigmentation, and quantitative variation in structural colour. Using geographic cline analysis, we show that clines in these traits are positioned in roughly the same geographic region for both species, which is consistent with direct selection for mimicry. However, the width of the clines varies markedly between species. This difference is explained in part by variation in the strength of selection acting on colour traits within each species, but may also be influenced by differences in the dispersal rate and total strength of selection against hybrids between the species. Genotyping‐by‐sequencing also revealed weaker population structure in H. melpomene, suggesting the hybrid zones may have evolved differently in each species, which may also contribute to the patterns of phenotypic divergence in this system. Overall, we conclude that multiple factors are needed to explain patterns of clinal variation within and between these species, although mimicry has probably played a central role.     

Causes and Consequences of a Lack of Coevolution in Müllerian mimicry

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

Evidence for a Müllerian mimetic radiation in Asian pitvipers

Müllerian mimicry, in which toxic species gain mutual protection from shared warning signals, is poorly understood in vertebrates, reflecting a paucity of examples. Indirect evidence for mimicry is found if monophyletic species or clades show parallel geographic variation in warning patterns. Here, we evaluate a hypothesis of Müllerian mimicry for the pitvipers in Southeast Asia using a phylogeny derived from DNA sequences from four combined mitochondrial regions. Mantel matrix correlation tests show that conspicuous red colour pattern elements are significantly associated with sympatric and parapatric populations in four genera. To our knowledge, this represents the first evidence of a Müllerian mimetic radiation in vipers. The putative mimetic patterns are rarely found in females. This appears paradoxical in light of the Müllerian prediction of monomorphism, but may be explained by divergent selection pressures on the sexes, which have different behaviours. We suggest that biased predation on active males causes selection for protective warning coloration, whereas crypsis is favoured in relatively sedentary females.     

Incorporating Motion into Investigations of mimicry

During the past thirty years, natural selection due to predation has been investigated with regard to prey motion in three areas that are relevant to the evolution of mimicry: (1) anti-apostatic selection, (2) locomotor mimicry, and (3) escape mimicry. Anti-apostatic selection, or selection against the odd individuals, arises when prey are at very high densities or when prey are Müllerian mimics. When prey are at high densities, motion of the prey increases selection against odd individuals. When the prey are Müllerian mimics, motion may also play an important role in strengthening selection against odd individuals. This may explain locomotor mimicry between Müllerian mimics. Locomotor mimicry arises when two distantly-related prey species appear alike in behaviour, and there is a corresponding suite of morphological, physiological, and biomechanical traits that the prey have in common. Locomotor mimicry has been demonstrated in Müllerian mimics. It is also predicted to occur in Batesian mimics but with important limitations due to selection by the predator for the prey to maintain the ability to escape if detected. Locomotor mimicry may also occur between palatable species that are alike as a result of unprofitable prey (or escape) mimicry. Escape mimicry arises when prey are difficult to capture. By frustration learning, the predator associates the colour of the prey with unprofitability. In all three instances, dis-similarity in colour or motion probably increases selection against the odd individual. In addition, the interaction of colour and motion gives rise to greater reliability of the signals to a specialist predator. However for a generalist predator, multiple component signals of the prey lead to errors in signal perception and greater risk of cheating. This revised version was published online in July 2006 with corrections to the Cover Date.     

Does Müllerian Mimicry Work in Nature? Experiments with Butterflies and Birds (Tyrannidae)1

The selective advantage of Müllerian 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 Müllerian 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.     

Phylogeny, systematics and evolution of mimetic wing patterns of Eterusia moths (Lepidoptera, Zygaenidae, Chalcosiinae)

Abstract. The aim of the present study was to investigate the phylogeny, systematics and evolution of the mimetic wing patterns of Eterusia, a day-flying moth genus that exhibits great morphological diversity, as well as the highest insular differentiation in eastern Asia and which has the most chaotic taxonomic history in the family Zygaenidae. We examined the wing patterns of the insects involved using visible and ultraviolet light (both reflectance and fluorescence). The phylogeny of thirty-four taxa, including all the recognized species of Eterusia plus two species of Soritia as outgroups, was reconstructed based on eighty adult morphological characters, including forty-one derived from colour patterns. Phylogenetic relationships based on the whole dataset revealed that (1) the most current concept of Eterusia is monophyletic, and (2) different types of mimetic pattern show different levels of phylogenetic conservation. To investigate the evolution of their colour patterns we inactivated all the relevant characters and reconstructed another phylogeny, which was found to differ significantly from the one based on the whole character set in the position of the E. risa species group. We used these phylogenetic hypotheses to test evolutionary predictions based on conventional Müllerian mimicry and quasi-Batesian mimicry dynamics. The results of permutation–tail–probability tests showed that the coloration characters are phylogenetically conserved, thus justifying a Müllerian interpretation. However, when comparing the observed topologies with hypothetical trees constrained to fit perfect Müllerian or quasi-Batesian scenarios using the Kishino–Hasegawa test, the observed phylogenies were more consistent with the phylogenetic prediction of quasi-Batesian mimicry. Therefore, we consider that applying these two phylogenetic methods to justify mimicry models may not always be practical. Finally, the taxonomy of Eterusia is revised. In total, two new species (E. austrochinensis, E. guanxiana), one new subspecies (E. risa palawanica) and four new synonyms (E. lativitta and E. fasciata of E. sublutea, E. coelestina of E. subcyanea, E. angustipennis gaedei of E. angustipennis angustipennis) are established.     

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

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

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

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

How to look like a mallow: evidence of floral mimicry between Turneraceae and Malvaceae

Abundant, many-flowered plants represent reliable and rich food sources for animal pollinators, and may even sustain guilds of specialized pollinators. Contrastingly, rare plants need alternative strategies to ensure pollinators' visitation and faithfulness. Flower mimicry, i.e. the sharing of a similar flower colour and display pattern by different plant species, is a means by which a rare species can exploit a successful model and increase its pollination services. The relationship between two or more rewarding flower mimic species, or Müllerian mimicry, has been proposed as mutualistic, in contrast to the unilaterally beneficial Batesian floral mimicry. In this work, we show that two different geographical colour phenotypes of Turnera sidoides ssp. pinnatifida resemble co-flowering Malvaceae in colour as seen by bees' eyes, and that these pollinators do not distinguish between them when approaching flowers in choice tests. Main pollinators of T. sidoides are bees specialized for collecting pollen in Malvaceae. We demonstrate that the similarity between at least one of the geographical colour phenotypes of T. sidoides and co-flowering Malvaceae is adaptive, since the former obtains more pollination services when growing together with its model than when growing alone. Instead of the convergent evolution pattern attributed to Müllerian mimicry, our data rather suggest an advergent evolution pattern, because only T. sidoides seems to have evolved to be more similar to its malvaceous models.     

Polymorphic Müllerian mimicry and interactions with thermal melanism in ladybirds and a soldier beetle: a hypothesis

It is argued that groups of similarly coloured species of coccinellids are Müllerian mimicry rings. This is based on a synthesis of the literature about the nature of their biology and aposematic colour patterns, their highly developed chemical defence and the responses of bird predators to them. The system of multiple mimicry ‘rings’ is illustrated for the Dutch coccinellid fauna. Some polymorphic species, including Adalia, exhibit red forms and black melanic forms which are apparently components of different putative mimicry rings. A similar reasoning is put forward with regard to the orange and the black forms of the soldier beetle Cuntharis livida. Hypotheses involving spatial variation in comimics, as have been developed to account for some other cases of polymorphic Miillerian mimicry, predict that sympatric polymorphic species exhibiting similar sets of phenotypes will show parallels in their geographical variation. This is tested for A. bipunctata and A. decempunctata in The Netherlands. On this local scale there is no parallel variation; A. bipunctata exhibits marked geographical differentiation whereas A. decempunctata shows a general uniformity in morph frequency. Observations on their population biology show that only in A. bipunctata is there a major spring period of adult reproduction on shrubs exposed to direct sunshine. Previous work has demonstrated an influence of thermal melanism in this period of the life cycle. It is suggested that local responses in species such as A. bipunctata may reflect a partial ‘escape’ from stabilizing aposematic selection. The basis of a steep cline found in C. livida, which opposes one in A. bipunctata, is unknown and unlikely to be related to mimicry. There is some evidence that the polymorphism is influenced by non-random mating. When species and communities of coccinellids are considered on a wide geographical scale many observations about their colour patterns and spatial variation, especially those of Dobzhansky, support an interaction between selection favouring mimetic resemblance and forms of climatic selection, especially thermal melanism. The polymorphism in Adalia is discussed in relation to a system of multiple mimicry rings and to Thompson's recent theoretical treatment of the maintenance of some polymorphisms for warning coloration by a balance between aposematic and apostatic selection. This becomes more tenable in coccinellids because of evidence that bird predators show a variable response to them. Frequency-independent selection arising from thermal melanism can provide the basis of spatial variation in equilibrium points. An alternative to such a hypothesis is one in which differences in unpalatability between species of coccinellids are emphasized (after experiments of Pasteels and colleagues). Some less unpalatable species such as Adalia may have responded to periods of prolonged disruptive selection acting in a frequency-dependent way to promote polymorphic mimicry associated with different modal colour patterns and intermediate in nature between classical Batesian and Müllerian mimicry. The likely occurrence of a supergene controlling polymorphism in some coccinellids is consistent with such an explanation.     

Müllerian mimetic radiation of Delias butterflies (Lepidoptera: Pieridae) in Bali and Timor

Mimicry rings are present among Delias butterflies, and those butterflies are also considered to be mimetic models of other lepidopteran insects; however, experimental evidence for their unpalatability to predators is limited. In Bali and Timor, a total of three mimicry rings of Delias species are present; particularly, male and female D. lemoulti join different rings in Timor. The present study examined the unpalatability of Delias in Bali and Timor to the caged avian predator Pycnonotus aurigaster. The birds ate eight Delias species in similar numbers, and ate the palatable butterfly Mycalesis horsfieldii much more frequently than Delias butterflies. The result suggests that the three mimicry rings of Delias species in Bali and Timor are Müllerian rather than Batesian. Based on previous findings on their phylogenetic relationships, the Müllerian mimicry rings of Delias in Bali and Timor are suggested to have emerged through the convergent evolution and phylogenetic constraints of wing color patterns. In the D. hyparete species group, mimetic radiation may have occurred between Bali and Timor.     

Variable Selection and the Coexistence of Multiple mimetic forms of the Butterfly Heliconius numata

Polymorphism in aposematic animals and coexistence of multiple mimicry rings within a habitat are not predicted by classical Müllerian mimicry. The butterfly Heliconius numata Cramer (Lepidoptera: Nymphalidae; Heliconiinae) is both polymorphic and aposematic. The polymorphism is due to variation at a single locus (or `supergene') which determines colour patterns involved in Müllerian mimicry. We sampled 11 sites in a small area (approx. 60×30km) of North-eastern Peru for H. numata and its co-mimics in the genus Melinaea and Athyrtis (Ithomiinae), and examined the role of temporal and spatial heterogeneity in the maintenance of polymorphism. Colour-patterns of Melinaea communities, which constitute the likely `mimetic environment' for H. numata, are differentiated on a more local scale than morphs of H. numata, but the latter do show a strong and significant response to local selection for colour-pattern. In contrast, analysis of enzyme polymorphism in H. numata across the region revealed no spatial structure, which is consistent with a high mobility of this species. Differences in spatial variability in the two taxa may have caused H. numata to become polymorphic, while temporal variability, not significant in this study, probably has a lesser effect. The mimetic polymorphism is therefore explained by means of multiple selection-migration clines at a single locus, a similar process to that which explains narrow hybrid zones between geographic races of other Heliconius butterflies. This revised version was published online in July 2006 with corrections to the Cover Date.