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.     

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.     

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.     

The evolution of a Müllerian mimic in a spatially distributed community

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.     

Inter-species variation in unpalatability does not explain polymorphism in a mimetic species

Conspicuous colouration in unpalatable organisms acts as a warning signal of their unprofitability, a phenomenon known as aposematism. The protection conferred by such colouration can lead to evolutionary convergence in warning signals between aposematic species, because sharing warning signals reduces the per capita cost of predator learning. Consequently, most aposematic species display a single colour pattern and participate in a single mimetic community (i.e. mimicry ring) at any given locality. However, some, like the Amazonian butterfly Heliconius numata, are polymorphic and participate in several mimicry rings within the same locality. We tested whether the unexpected polymorphism of H. numata could be due to a weak defence against predators. Poorly defended species participating in a mimicry ring are subject to negative frequency dependent selection, because their presence weakens the protection provided by the shared signal. This could promote polymorphism and participation in multiple mimicry rings. Using wild caught great tits (Parus major), we compared the palatability of H. numata to one of its locally monomorphic co-mimics (Mechanitis polymnia) and to two other locally monomorphic Heliconius species (H. melpomene and H. erato). The tested birds strongly rejected the polymorphic species H. numata, as well as the two other Heliconius species. Unexpectedly, a significantly weaker rejection was found towards M. polymnia, which relies on different toxic compounds to Heliconius. Our study demonstrates that the origin of polymorphic mimicry in H. numata is unlikely to stem from low unpalatability and raises new questions on defence variation within mimetic communities.     

Development of microsatellite loci from a reference genome for the Neotropical butterfly Heliconius numata and its close relatives

The Neotropical butterfly Heliconius numata (Lepidoptera: Nymphalidae: Heliconiinae) is known for its striking diversity of wing color patterns driven by the Müllerian mimicry of multiple local models and controlled by a single supergene locus. Such fine‐scale variation of traits under strong selection offers a unique opportunity for the study of the ecology and genetics of adaptation. However, little is still known of the population processes driving geographical variation in wing‐pattern phenotypes. We report the characterization of 26 microsatellite markers for the butterfly H. numata, including six located inside the wing color‐pattern supergene region. All markers are polymorphic, with allele numbers ranging from 2 to 21 per locus, an observed heterozygosity of 0.111 to 0.848 and an expected heterozygosity of 0.126 to 0.942. A subset of 18 of these markers was tested on five closely related sympatric Heliconius species with an amplification success ranging from 88% to 94%. The obtained set of microsatellite markers provides a new and useful set of tools to investigate patterns of differentiation and selection in populations of mimetic Heliconius butterflies. Moreover, markers developed within the color‐pattern supergene will facilitate characterization of the association between the genetic architecture and the functional diversity of wing patterns. Finally, the cross‐species amplification success of the described markers extends their utility to also encompass comparative population genetic studies of closely related species within a clade of rapidly diversifying species.     

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.     

The effect of alternative prey on the dynamics of imperfect Batesian and Müllerian mimicries

Both Batesian and Müllerian mimicries are considered classical evidence of natural selection where predation pressure has, at times, created a striking similarity between unrelated prey species. Batesian mimicry, in which palatable mimics resemble unpalatable aposematic species, is parasitic and only beneficial to the mimics. By contrast, in classical Müllerian mimicry the cost of predators' avoidance learning is shared between similar unpalatable co-mimics, and therefore mimicry benefits all parties. Recent studies using mathematical modeling have questioned the dynamics of Müllerian mimicry, suggesting that fitness benefits should be calculated in a way similar to Batesian mimicry; that is, according to the relative unpalatability difference between co-mimics. Batesian mimicry is very sensitive to the availability of alternative prey, but the effects of alternative prey for Müllerian dynamics are not known and experiments are rare. We designed two experiments to test the effect of alternative prey on imperfect Batesian and Müllerian mimicry complexes. When alternative prey were scarce, imperfect Batesian mimics were selected out from the population, but abundantly available alternative prey relaxed selection against imperfect mimics. Birds learned to avoid both Müllerian models and mimics irrespective of the availability of alternative prey. However, the rate of avoidance learning of models increased when alternative prey were abundant. This experiment suggests that the availability of alternative prey affects the dynamics of both Müllerian and Batesian mimicry, but in different ways.     

Specialized avian predators repeatedly attack novel color morphs of Heliconius butterflies

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.     

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.     

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.     

Wing patterning genes and coevolution of Müllerian mimicry in Heliconius butterflies: Support from phylogeography,cophylogeny, and divergence times

Examples of long‐term coevolution are rare among free‐living organisms. Müllerian mimicry in Heliconius butterflies had been suggested as a key example of coevolution by early genetic studies. However, research over the last two decades has been dominated by the idea that the best‐studied comimics, H. erato and H. melpomene, did not coevolve at all. Recently sequenced genes associated with wing color pattern phenotype offer a new opportunity to resolve this controversy. Here, we test the hypothesis of coevolution between H. erato and H. melpomene using Bayesian multilocus analysis of five color pattern genes and five neutral genetic markers. We first explore the extent of phylogenetic agreement versus conflict between the different genes. Coevolution is then tested against three aspects of the mimicry diversifications: phylogenetic branching patterns, divergence times, and, for the first time, phylogeographic histories. We show that all three lines of evidence are compatible with strict coevolution of the diverse mimicry wing patterns, contrary to some recent suggestions. Instead, these findings tally with a coevolutionary diversification driven primarily by the ecological force of Müllerian mimicry.     

Cryptic differences in colour among Müllerian mimics: how can the visual capacities of predators and prey shape the evolution of wing colours?

Antagonistic interactions between predators and prey often lead to co‐evolution. In the case of toxic prey, aposematic colours act as warning signals for predators and play a protective role. Evolutionary convergence in colour patterns among toxic prey evolves due to positive density‐dependent selection and the benefits of mutual resemblance in spreading the mortality cost of educating predators over a larger prey assemblage. Comimetic species evolve highly similar colour patterns, but such convergence may interfere with intraspecific signalling and recognition in the prey community, especially for species involved in polymorphic mimicry. Using spectrophotometry measures, we investigated the variation in wing coloration among comimetic butterflies from distantly related lineages. We focused on seven morphs of the polymorphic species Heliconius numata and the seven corresponding comimetic species from the genus Melinaea. Significant differences in the yellow, orange and black patches of the wing were detected between genera. Perceptions of these cryptic differences by bird and butterfly observers were then estimated using models of animal vision based on physiological data. Our results showed that the most strikingly perceived differences were obtained for the contrast of yellow against a black background. The capacity to discriminate between comimetic genera based on this colour contrast was also evaluated to be higher for butterflies than for birds, suggesting that this variation in colour, likely undetectable to birds, might be used by butterflies for distinguishing mating partners without losing the benefits of mimicry. The evolution of wing colour in mimetic butterflies might thus be shaped by the opposite selective pressures exerted by predation and species recognition.     

Mimetic colour pattern evolution in the highly polymorphic Bombus trifasciatus (Hymenoptera: Apidae) species complex and its comimics

Müllerian mimetic systems have uncovered some of the dynamic processes by which natural selection can drive the radiation of convergent and divergent phenotypes. We examined evolution involving Müllerian mimicry in bumble bees by documenting the distribution and evolution of colour patterns amongst three colour‐polymorphic lineages –Bombus trifasciatus Smith, Bombus haemorrhoidalis Smith, and Bombus breviceps Smith – that mimic each other across ～14 colour groups in South‐East Asia. Using mitochondrial DNA sequence data, we estimated relationships within each lineage to infer the processes that gave rise to the colour diversity and develop hypotheses on species recognition. We expanded on our assessment of species delineation in the B. trifasciatus lineage using three nuclear gene fragments and morphometrics. Comparison of colour patterns amongst georeferenced specimens showed considerable variation in the degree and geographical range of mimicry amongst mimicry groups. Phylogenetic estimates show high rates of colour pattern evolution, with colour variation often exceeding variation within the fast‐evolving mitochondrial genes. The molecular data, and to some degree the morphometric data, support unique histories for several taxa recognized previously within the B. trifasciatus lineage, which may include several species. Early vicariant events within the B. trifasciatus lineage are likely to have occurred ～2.2 Mya in the mountains of south‐west China. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166 , 805–826.     

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.     

All-female broods and mimetic polymorphism in Acraea encedon (L.) (Lepidoptera: Acraeidae) in Tanzania

In some populations of the African butterfly, Acraea encedon, there are two kinds of females, one producing offspring in a normal 1:1 sex ratio, the other producing females only; in other populations the sex ratio is apparently normal. All-female broods had hitherto been mainly associated with populations in which field sampling revealed an excess of females. The all-female brood trait is described from a population at Dar es Salaam which field sampling suggested was normal, and this indicates that the trait may be much more widespread and common than had previously been supposed. This discovery also extends the known distribution of the trait across Africa from Sierra Leone to eastern Tanzania. The butterfly is also a polymorphic Müllerian mimic of Danaus chrysippus, which is a highly unusual phenomenon as Müllerian mimicry is almost invariably monomorphic. The relative frequencies of two corresponding colour forms of the two species of butterflies at Dar es Salaam adds support to the hypothesis that they are indeed Mullerian mimics. The results of breeding experiments suggest that the polymorphic forms in Acraea encedon are allelic with dominance.     

WHY DOES THE YELLOW‐EYED ENSATINA HAVE YELLOW EYES? BATESIAN MIMICRY OF PACIFIC NEWTS (GENUS TARICHA) BY THE SALAMANDER ENSATINA ESCHSCHOLTZII XANTHOPTICA

Color patterns commonly vary geographically within species, but it is rare that such variation corresponds with divergent antipredator strategies. The polymorphic salamander Ensatina eschscholtzii, however, may represent such a case. In this species, most subspecies are cryptically colored, whereas E. e. xanthoptica, the Yellow eyed ensatina, is hypothesized to be an aposematic mimic of highly toxic Pacific newts (genus Taricha). To test the mimicry hypothesis, we conducted feeding trials using Western Scrub-Jays, Aphelocoma californica. In every feeding trial, we found that jays, following presentation with the presumed model (T. torosa), were more hesitant to contact the presumed mimic (E. e. xanthoptica) than a control subspecies lacking the postulated aposematic colors (E. e. oregonensis). The median time to contact was 315 sec for the mimic and 52 sec for the control. These results support the mimicry hypothesis, and we suggest that E. e. xanthoptica is likely a Batesian mimic, rather a Müllerian or quasi-Batesian mimic, of Pacific newts.     

Alternative prey can change model–mimic dynamics between parasitism and mutualism

Classical (conventional) Müllerian mimicry theory predicts that two (or more) defended prey sharing the same signal always benefit each other despite the fact that one species can be more toxic than the other. The quasi‐Batesian (unconventional) mimicry theory, instead, predicts that the less defended partner of the mimetic relationship may act as a parasite of the signal, causing a fitness loss to the model. Here we clarify the conditions for parasitic or mutualistic relationships between aposematic prey, and build a model to examine the hypothesis that the availability of alternative prey is crucial to Müllerian and quasi‐Batesian mimicry. Our model is based on optimal behaviour of the predator. We ask if and when it is in the interest of the predator to learn to avoid certain species as prey when there is alternative (cryptic) prey available. Our model clearly shows that the role of alternative prey must be taken into consideration when studying model–mimic dynamics. When food is scarce it pays for the predator to test the models and mimics, whereas if food is abundant predators should leave the mimics and models untouched even if the mimics are quite edible. Dynamics of the mimicry tend to be classically Müllerian if mimics are well defended, while quasi‐Batesian dynamics are more likely when they are relatively edible. However, there is significant overlap: in extreme cases mimics can be harmful to models (a quasi‐Batesian case) even if the species are equally toxic. A crucial parameter explaining this overlap is the search efficiency with which indiscriminating vs. discriminating predators find cryptic prey. Quasi‐Batesian mimicry becomes much more likely if discrimination increases the efficiency with which the specialized predator finds cryptic prey, while the opposite case tends to predict Müllerian mimicry. Our model shows that both mutualistic and parasitic relationship between model and mimic are possible and the availability of alternative prey can easily alter this relationship.     

WING SHAPE VARIATION ASSOCIATED WITH MIMICRY IN BUTTERFLIES

Mimetic resemblance in unpalatable butterflies has been studied by evolutionary biologists for over a century, but has largely focused on the convergence in wing color patterns. In Heliconius numata, discrete color‐pattern morphs closely resemble comimics in the distantly related genus Melinaea. We examine the possibility that the shape of the butterfly wing also shows adaptive convergence. First, simple measures of forewing dimensions were taken of individuals in a cross between H. numata morphs, and showed quantitative differences between two of the segregating morphs, f. elegans and f. silvana. Second, landmark‐based geometric morphometric and elliptical Fourier outline analyses were used to more fully characterize these shape differences. Extension of these techniques to specimens from natural populations suggested that, although many of the coexisting morphs could not be discriminated by shape, the differences we identified between f. elegans and f. silvana hold in the wild. Interestingly, despite extensive overlap, the shape variation between these two morphs is paralleled in their respective Melinaea comimics. Our study therefore suggests that wing‐shape variation is associated with mimetic resemblance, and raises the intriguing possibility that the supergene responsible for controlling the major switch in color pattern between morphs also contributes to wing shape differences in H. numata.     

Investigating Müllerian mimicry: predator learning and variation in prey defences

Inexperienced predators are assumed to select for similarity of warning signals in aposematic species (Müllerian mimicry) when learning to avoid them. Recent theoretical work predicts that if co-mimic species have unequal defences, predators attack them according to their average unpalatability and mimicry may not be beneficial for the better defended co-mimic. In this study, we tested in a laboratory environment whether a uniform warning signal is superior to a variable one in promoting predator learning, and simultaneously whether co-mimics are preyed upon according to their average unpalatability. There was an interaction of signal variation and unpalatability but inexperienced birds did not select for signal similarity in artificial prey; when the prey was moderately defended a variable signal was even learnt faster than a uniform one. Due to slow avoidance learning, moderately defended prey had higher mortality than highly defended prey (although this was not straightforward), but mixing high and moderate unpalatability did not increase predation compared with high unpalatability. This does not support the view that predators are sensitive to varying unpalatability. The results suggest that inexperienced predators may neither strongly select for accurate Müllerian mimicry nor affect the benefits of mimicry when the co-mimics are unequally defended.