Thermoregulatory significance of wing melanization in Pieris butterflies (Lepidoptera: Pieridae): physics,posture, and pattern

Summary Pieris butterflies use a novel behavioral posture for thermoregulation called reflectance basking, in which the wings are used as solar reflectors to reflect radiation to the body. As a means of exploring the thermoregulatory significance of wing melanization patterns, I examine the relation of basking posture and wing color pattern to body temperature. A mathematical model of the reflectance process predicts certain combinations of dorsal wing melanization pattern and basking posture that maximize body temperature. Laboratory experiments and field observations show that this model correctly predicts qualitative differences in the relation of body temperature to basking posture based on differences in the extent of dorsal melanization on the wing margins, both between species and between sexes within species of Pieris. This is the first demonstration in insects that coloration of the entire wing surface can affect thermoregulation. Model and experimental results suggest that, in certain wing regions, increased melanization can reduce body temperature in Pieris; this effect of melanization is exactly the opposite of that found in other Pierid butterflies that use their wings as solar absorbers. These results are discussed in terms of the evolution of wing melanization pattern and thermoregulatory behavior in butterflies.     

EVOLUTION AND COADAPTATION OF THERMOREGULATORY BEHAVIOR AND WING PIGMENTATION PATTERN IN PIERID BUTTERFLIES

This paper addresses the question of how the relationship between morphological structure and functional performance differs in related groups of organisms. I describe the relationship between a suite of phenotypic characters (behavioral posture and the pattern of wing pigmentation) and one function of these characters (thermoregulatory performance) for two groups of butterflies in the family Pieridae, focusing on how behavior and wing pattern interact to affect specific aspects of thermoregulation. Using both natural and experimentally created variation in wing-melanization patterns, I develop and test a series of predictions about the relations among thermoregulatory posture, melanization pattern, body temperature, and flight activity. Results show that increased melanization in different wing regions has positive, negative, or neutral effects in increasing body temperature of Pieris butterflies. The angle of the wings used during basking alters the relative importance of different modes of heat transfer and thereby determines the contribution of different dorsal wing regions to thermoregulation. Experimentally increased dorsal melanization can either increase or decrease the onset of flight activity and can directly alter thermoregulatory posture. For Pieris, dorsal melanization affects basking and flight, while ventral melanization primarily affects overheating. These results are used to generate a functional map relating melanization pattern to thermoregulatory performance in Pieris. Reflectance-basking posture, white background color, and melanization pattern represent coadapted characters in Pieris that interact to determine thermoregulatory performance. The differences in thermoregulatory posture and background color between pierid butterflies in the subfamilies Pierinae and Coliadinae have led to a reorganization and partial reversal of the thermoregulatory effects of melanization pattern. I suggest that this change in the physical mechanism of thermoregulatory adaption in pierids has qualitatively altered the nature of selection on wing-melanization pattern.     

Thermal ecology of Pieris butterflies (Lepidoptera: Pieridae): a new mechanism of behavioral thermoregulation

Summary I document a new mechanism for behavioral thermoregulation, not previously described in animals, called reflectance basking. This behavior, described here for Pieris butterflies, involves the use of the wings as solar reflectors that reflect solar radiation onto the body to increase body temperature. Results show that Pieris require thoracic (body) temperature. between 29° and 40° C in order to take off and fly, and achieve these elevated temperatures by basking. Diurnal patterns of population flight activity are closely correlated with patterns of body temperature during basking. Behavioral studies indicate that 1) Pieris orient to solar radiation, 2) they use thermoregulatory postures consistent with reflectance basking, and 3) they do not use the basking postures found in other Pierid butterflies (i.e., the Coliadinae). There are consistent differences in wing angles used in reflectance basking between Pieris in different subgenera. Results are discussed with respect to thermoregulation and wing color in other Pierid butterflies, and suggest that a re-evaluation of the functional significance of melanization in Pieris is needed.     

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.     

The responses of wild jacamars (Galbula ruficauda,Galbulidae) to aposematic,aposematic and cryptic,and cryptic butterflies in central Brazil

1. This article reports the responses of wild, adult jacamars to butterflies with distinct coloration types in central Brazil. Fully aposematic species, i.e. those exhibiting bright and/or contrasting colours on both wing surfaces (= A/A), were predominantly sight‐rejected by birds and, with one exception, the few butterflies attacked and captured were taste‐rejected afterwards. 2. Aposematic and cryptic butterflies, i.e. those exhibiting bright and/or contrasting colours on the upper and cryptic colours on the underwings (= A/C) were sight‐rejected while flying, when they show their conspicuous colours to predators. This suggests that birds associate butterfly colours with their difficulty of capture, as in the case of Morpho and several Coliadinae species. These butterflies, however, were heavily attacked at rest, when they are cryptic. 3, Fully cryptic butterflies, i.e. those exhibiting cryptic colours on both wing surfaces (= C/C) did not elicit sight rejections by birds. Comparisons involving the number of attacks and the capture success of flying and resting individuals showed no significant differences in species more frequently observed like some cracker butterflies (Hamadryas feronia and H. februa) and Taygetis laches. Compared with the A/C Coliadinae, these butterflies showed a lesser, although not significantly different, ability to escape while flying, but a greater and significantly different ability to escape while at rest. 4, A hunting tactic of jacamars, which consists of following flying A/C and C/C butterflies on sight, and waiting until they perch to locate and attack them, is described for the first time.     

Testing the role of ecological selection on colour pattern variation in the butterfly Parnassius clodius

Colour pattern has served as an important phenotype in understanding the process of natural selection, particularly in brightly coloured and variable species like butterflies. However, different selective forces operate on aspects of colour pattern, for example by favouring warning colours in eyespots or alternatively favoring investment in thermoregulatory properties of melanin. Additionally, genetic drift influences colour phenotypes, especially in populations undergoing population size change. Here, we investigated the relative roles of genetic drift and ecological selection in generating the phenotypic diversity of the butterfly Parnassius clodius. Genome‐wide patterns of single nucleotide polymorphism data show that P. clodius forms three population clusters, which experienced a period of population expansion following the last glacial maximum and have since remained relatively stable in size. After correcting for relatedness, morphological variation is best explained by climatic predictor variables, suggesting ecological selection generates trait variability. Solar radiation and precipitation are both negatively correlated with increasing total melanin in both sexes, supporting a thermoregulatory function of melanin. Similarly, wing size traits are significantly larger in warmer habitats for both sexes, supporting a Converse Bergmann Rule pattern. Bright red coloration is negatively correlated with temperature seasonality and solar radiation in males, and weakly associated with insectivorous avian predators in univariate models, providing mixed evidence that selection is linked to warning coloration and predator avoidance. Together, these results suggest that elements of butterfly wing phenotypes respond independently to different sources of selection and that thermoregulation is an important driver of phenotypic differentiation in Parnassian butterflies.     

Susceptibility of Transgenic and Wildtype Zebra Danios, Danio rerio, to Predation

The effects to ecosystems by genetically modified organisms are still unknown, yet a transgenic version (the red glofish or red fluorescent protein (RFP) transgenic zebra danio) of the zebra danio, Danio rerio, a common aquarium fish, has become the first transgenic pet sold in the USA. It has been hypothesized that RFP zebra danios will not persist in nature because they will be preferentially preyed upon due to their red coloration; however, the bright coloration of wildtype zebra danios may indicate they are aposematic since they are not preyed upon immediately by predators in their native range. These hypotheses were addressed via nine predation experiments with largemouth bass, Micropterus salmoides, as predator and combinations of mosquitofish, Gambusia affinis, wildtype zebra danios, and RFP zebra danios as prey. Neither wildtype nor RFP transgenic zebra danios are aposematic since both varieties were readily consumed by largemouth bass in laboratory trials. Both varieties were preyed upon in approximately equal proportion (1.4 to 1.0) so the bright, apparently conspicuous coloration of the transgenic zebra danios did not increase their susceptibility to predation. In these laboratory trials, largemouth bass did not preferentially prey upon a native fish, the mosquitofish, relative to wildtype zebra danios (1.2 to 1.0). Based on the results of these experiments, wildtype zebra danios and RFP transgenic zebra danios are likely to be preyed upon in a similar fashion as native forage fish.     

Effect of sex and bright coloration on survival and predator‐induced wing damage in an aposematic lantern fly with startle display

1. Aposematic coloration in prey promotes its survival by conspicuously advertising unpalatability to predators. Although classical examples of aposematic signals involve constant presentation of a signal at a distance, some animals suddenly display warning colours only when they are attacked. 2. Characteristics of body parts suddenly displayed, such as conspicuous coloration or eyespot pattern, may increase the survival of the prey by startling the predator, and/or by signalling unpalatability to the predators at the moment of attack. 3. The adaptive value of such colour patterns suddenly displayed by unpalatable prey has not been studied. We experimentally blackened the red patch in the conspicuous red–white–black hindwing pattern displayed by an unpalatable insect Lycorma delicatula White (Hemiptera: Fulgoridae) in response to predator's attack. 4. There was no evidence that the presence of the red patch increased prey survival over several weeks. We hypothesise that predators generalised from the red–white–black patches on the hindwings of unpalatable L. delicatula to any similar wing display as a signal of unpalatability. Because a higher proportion of males than females stay put at their resting sites, displaying their wings in response to repeated attacks by predators, wing damage was more frequent in males than in females. 5. To our knowledge, this is the first experimental test of an adaptive role of aposematic signals presented by unpalatable prey during sudden displays triggered by direct predatory attack.     

An Analysis of Predator Selection to Affect Aposematic Coloration in a Poison Frog Species

Natural selection is widely noted to drive divergence of phenotypic traits. Predation pressure can facilitate morphological divergence, for example the evolution of both cryptic and conspicuous coloration in animals. In this context Dendrobatid frogs have been used to study evolutionary forces inducing diversity in protective coloration. The polytypic strawberry poison frog (Oophaga pumilio) shows strong divergence in aposematic coloration among populations. To investigate whether predation pressure is important for color divergence among populations of O. pumilio we selected four mainland populations and two island populations from Costa Rica and Panama. Spectrometric measurements of body coloration were used to calculate color and brightness contrasts of frogs as an indicator of conspicuousness for the visual systems of several potential predators (avian, crab and snake) and a conspecific observer. Additionally, we conducted experiments using clay model frogs of different coloration to investigate whether the local coloration of frogs is better protected than non-local color morphs, and if predator communities vary among populations. Overall predation risk differed strongly among populations and interestingly was higher on the two island populations. Imprints on clay models indicated that birds are the main predators while attacks of other predators were rare. Furthermore, clay models of local coloration were equally likely to be attacked as those of non-local coloration. Overall conspicuousness (and brightness contrast) of local frogs was positively correlated with attack rates by birds across populations. Together with results from earlier studies we conclude that conspicuousness honestly indicates toxicity to avian predators. The different coloration patterns among populations of strawberry poison frogs in combination with behavior and toxicity might integrate into equally efficient anti-predator strategies depending on local predation and other ecological factors.     

A parallel geographical mosaic of morphological and behavioural aposematic traits of the newt, Cynops pyrrhogaster (Urodela: Salamandridae)

Aposematic animals advertise their unprofitability to potential predators with conspicuous coloration, occasionally in combination with other life-history traits. Theory posits that selection on functionally interrelated aposematic characters promotes the unidirectional evolution of these characters, resulting in an increase or decrease in the effectiveness of the signal. To test whether this prediction applies on a microevolutionary scale, the intra- and interpopulational variations in aposematic coloration, behaviour (which enhances the effectiveness of the coloration) and body size of newts, Cynops pyrrhogaster (Urodela: Salamandridae), were investigated. A parallel geographical mosaic of variation in aposematic coloration and behaviour among populations, independent of body size, was found. Newts on islands displayed more conspicuous aposematic traits than those on the mainland, both morphologically and behaviourally. There was no significant relationship between variation in coloration and behaviour within populations. Male newts displayed more conspicuous coloration than females. Surveys of potential predators suggest that variable natural selection at a local scale, such as predation pressure, may primarily be responsible for the microevolution of variable aposematic traits in newts.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 613–622.     

Coral snake mimicry: live snakes not avoided by a mammalian predator

The occurrence of coral snake coloration among unrelated venomous and non-venomous New World snake species has often been explained in terms of warning coloration and mimicry. The idea that snake predators would avoid coral snakes in nature seems widely established and is postulated in many discussions on coral snake mimicry. However, the few workers that have tested a potential aposematic function of the conspicuous colour pattern focused exclusively on behaviour of snake predators towards coloured abstract models. Here we report on behaviour of temporarily caged, wild coatis (Nasua narica) when confronted with co-occurring live snakes, among which were two species of venomous coral snakes. Five different types of responses have been observed, ranging from avoidance to predation, yet none of the coatis avoided either of the two coral snake species or other species resembling these. As in earlier studies coatis appeared to avoid coral snake models, our findings show that results from studies with abstract snake models cannot unconditionally serve as evidence for an aposematic function of coral snake coloration.     

Teasing apart crypsis and aposematism – evidence that disruptive coloration reduces predation on a noxious toad

Both cryptic and aposematic colour patterns can reduce predation risk to prey. These distinct strategies may not be mutually exclusive, because the impact of prey coloration depends on a predator's sensory system and cognition and on the environmental background. Determining whether prey signals are cryptic or aposematic is a prerequisite for understanding the ecological and evolutionary implications of predator–prey interactions. This study investigates whether coloration and pattern in an exceptionally polymorphic toad, Rhinella alata, from Barro Colorado Island, Panama reduces predation via background matching, disruptive coloration, and/or aposematic signaling. When clay model replicas of R. alata were placed on leaf litter, the model's dorsal pattern – but not its colour – affected attack rates by birds. When models were placed on white paper, patterned and un‐patterned replicas had similar attack rates by birds. These results indicate that dorsal patterns in R. alata are functionally cryptic and emphasize the potential effectiveness of disruptive coloration in a vertebrate taxon.     

Avoidance of an aposematically coloured butterfly by wild birds in a tropical forest

1. Birds are considered to be the primary selective agents for warning colouration in butterflies, and select for aposematic mimicry by learning to avoid brightly coloured prey after unpleasant experiences. It has long been thought that bright colouration plays an important role in promoting the avoidance of distasteful prey by birds. 2. The hypothesis that warning colouration facilitates memorability and promotes predator avoidance was tested by means of a field experiment using distasteful model butterflies. Artificial butterflies with a Heliconius colour pattern unknown to local birds were generated using bird vision models, either coloured or achromatic, and hung in tree branches in a tropical forest. Two sequential trials were conducted at each site to test avoidance by naïve and experienced predators. 3. There was a significant reduction in predation in the second trial. Also, coloured models were attacked less than achromatic models. Specifically, coloured butterflies were attacked significantly less in the second trial, but there was no significant decrease in predation on achromatic models. 4. The present results imply an important role for colour in enhancing aversion of aposematic butterflies. It has also been demonstrated that previous experience of distasteful prey can lead to enhanced avoidance in subsequent trials, supporting mimicry theory.     

Wing coloration and reflectance in Morpho butterflies as related to reproductive behavior and escape from avian predators

Summary Different species of large tropical butterflies belonging to the genus Morpho vary dramatically in both the amount of blue color on their wings and the associated irridescence (reflectance). This paper discusses how such a morphological properties may be related to both courtship behavior and effective means of reducing predation (especially by birds) in the low density adult populations. Essentially, the hypothesis is advanced that territorial species of Morpho can afford to possess very conspicuous wing coloration that may facilitate courtship interactions, in addition to spacing the territorial male population over the suitable habitat. While territoriality may be favored by natural selection, such behavior can only evolve if the species involved possess effective means of reducing predation, because territoriality in morphos is an extremely predictable form of behavior, toward which predators can easily orient. Two alternate hypotheses are advanced to account for low predation in a territorial morpho, Morpho amathonte, a species in which males are very bright and showy. The first hypothesis, which is more consistent with traditional ideas on the function of bright colors in morpho wings, maintains that predators learn quickly to avoid these butterflies as prey, since they are very difficult to catch. The second hypothesis, suggests that conspicuous territorial male morphos actually employ pursuit-stimuli to invite birds to attack and be subsequently unsuccessful.     

Are European White Butterflies Aposematic?

It has been suggested that the white coloration of Pieridae butterflies is a warning signal and therefore all white Pieridae could profit from a mimetic resemblance. We tested whether green-veined white (Pieris napi) and orange-tip (Anthocharis cardamines) butterflies benefit from white coloration. We compared their relative acceptability to wild, adult pied flycatchers (Ficedula hypoleuca) by offering live A. cardamines and P. napi together with two non-aposematic butterflies on the tray attached to birds' nesting boxes. Experienced predators equally attacked white and non-white butterflies, and the order of attack among the Pieridae was random. If anything, there was a slight indication that the female A. cardamines was the least favoured prey. Since birds did not avoid white coloration, we compared the palatability of these two species against known palatable and unpalatable butterflies by presenting them to great tits (Parus major). Pieris brassicae, which has been earlier described as unpalatable, was also included in the palatability test. However, there were no significant differences in the palatability of the butterflies to birds, and even P. brassicae was apparently palatable to the great tits. Our results do not unambiguously support the hypothesis that the white coloration of Pieridae would signal unpalatability. Nevertheless, in our last experiment, pied flycatchers often rejected or left untouched free flying P. napi and A. cardamines. This suggests that other features in a more natural situation, such as the agile flight pattern or odours might still make them unprofitable to birds. This revised version was published online in July 2006 with corrections to the Cover Date.     

Eye camouflage and false eyespots: chaetodontid responses to predators

Synopsis The roles of eye camouflage and eyespots are examined within the genusChaetodon as are the various theories explaining the evolutionary significance of the brilliant colors. While eye camouflage is not common among reef fishes, 91% of the 90 species ofChaetodon, have eyemasks (82) or black heads (4). Eye camouflage occurs concomitantly with diurnal false eyespots in 45.5% (41 of 90) of the species. Diurnal false eyespots serve to misdirect attacks by predators and/or to advertise unpalatability. False eyespots are located on areas of the body which allow escape and survival following an attack. Data suggesting that predators learn about the undesirability of butterflyfishes are presented. Butterflyfishes are inactive at night, forage during the day and spawn at dusk. It is unlikely that nocturnal color changes are useful in conspecific interactions and are therefore believed to provide visual cues to potential predators. Nocturnal eyespots probably function to intimidate potential predators but could also remind them of unpalatability. The aggression release hypothesis (Lorenz 1962, 1966) to explain the brilliant coloration of chaetodontids is not supported because butterflyfish coloration changes and few species are territorial. The species recognition hypothesis (Zumpe 1965) is not supported by results of field experiments. The disruptive coloration hypothesis (Longley 1917) is rejected as a general explanation for poster coloration but does explain the prevalence of eyebars ofChaetodon spp. The aposematic hypothesis (Gosline 1965) is supported by morphology, behavior, a lack of predation and field observations. The possibility of Mullerian mimicry is suggested. It is concluded that the primary selective force behind chaetodontid coloration, particularly eyespots, has been predation and color patterns have evolved to minimize this threat.     

DISSECTING CORRELATED CHARACTERS: ADAPTIVE ASPECTS OF PHENOTYPIC COVARIATION IN MELANIZATION PATTERN OF PIERIS BUTTERFLIES

In this study we address the question of how much of the covariation among phenotypic characters observed in natural populations is adaptive. We examine covariation among a set of phenotypic characters that describe the wing-melanization pattern of Pieris butterflies. Previous functional analyses of thermoregulatory performance allow us to predict a priori whether and how different wing melanic characters should be correlated. We quantify and analyze the variation in the wing-melanization pattern within species for a series of Pieris populations from relatively cool environments in North America and compare these results with the predictions based on our adaptive hypothesis. We consider adaptive covariation both for biogeographic variation among populations and for seasonal polyphenism (phenotypic plasticity) within populations. Our hypothesis correctly predicts many of the qualitative features of covariation in melanization among major regions of the wings, at the level of biogeographic variation among populations, for both males and females of Pieris occidentalis. When within-population variation is considered, agreement with the adaptive predictions varies considerably in different populations for both P. occidentalis and P. napi males and females. Agreement for P. napi, particularly the females, is generally poorer than for P. occidentalis. In both species, there is a consistent difference in melanization pattern between alpine and arctic sites; this difference is discussed in relation to the differences in the radiative environment between these two types of “cold” habitats. Our results suggest that some important aspects of phenotypic correlation among wing melanic characters in Pieris are adaptive. We emphasize the important distinction between covariation and co-occurrence of characters, and we discuss these results in relation to the extensive biogeographic variation and phenotypic plasticity (seasonal polyphenism) in Pieris wing-melanization patterns.     

The conceptual and practical implications of interpreting diet breadth mechanistically in generalist predatory insects

Seasonal polyphenism in animal colour patterns indicates that temporal variation in selection pressures maintains phenotypic plasticity. Spring generation of the polyphenic European map butterfly Araschnia levana has an orange–black fritillary‐like pattern whilst individuals of the summer generation are black with white bands across the wings. What selects for the colour difference is unknown. Because predation is a major selection pressure for insect coloration, we first tested whether map butterfly coloration could have a warning function (i.e. whether the butterflies are unpalatable to birds). In a following field experiment with butterfly dummies we tested whether the spring form is better protected than the summer form from predators in the spring, and vice versa in the summer. The butterflies were palatable to birds (blue tits Cyanistes caeruleus) and in the field the spring and summer form dummies were attacked equally irrespective of season. Therefore, we found no evidence that the map butterfly is warning‐coloured or that seasonal polyphenism is an adaptation to avian predation. Because insect coloration has multiple functions and map butterfly coloration is linked to morphology, life history and development it is likely that the interplay of several selection pressures explains the evolution of colour polyphenism. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Altitude and life‐history shape the evolution of Heliconius wings

Phenotypic divergence between closely related species has long interested biologists. Taxa that inhabit a range of environments and have diverse natural histories can help understand how selection drives phenotypic divergence. In butterflies, wing color patterns have been extensively studied but diversity in wing shape and size is less well understood. Here, we assess the relative importance of phylogenetic relatedness, natural history, and habitat on shaping wing morphology in a large dataset of over 3500 individuals, representing 13 Heliconius species from across the Neotropics. We find that both larval and adult behavioral ecology correlate with patterns of wing sexual dimorphism and adult size. Species with solitary larvae have larger adult males, in contrast to gregarious Heliconius species, and indeed most Lepidoptera, where females are larger. Species in the pupal‐mating clade are smaller than those in the adult‐mating clade. Interestingly, we find that high‐altitude species tend to have rounder wings and, in one of the two major Heliconius clades, are also bigger than their lowland relatives. Furthermore, within two widespread species, we find that high‐altitude populations also have rounder wings. Thus, we reveal novel adaptive wing morphological divergence among Heliconius species beyond that imposed by natural selection on aposematic wing coloration.     

Prey from the eyes of predators: Color discriminability of aposematic and mimetic butterflies from an avian visual perspective

Predation exerts strong selection on mimetic butterfly wing color patterns, which also serve other functions such as sexual selection. Therefore, specific selection pressures may affect the sexes and signal components differentially. We tested three predictions about the evolution of mimetic resemblance by comparing wing coloration of aposematic butterflies and their Batesian mimics: (a) females gain greater mimetic advantage than males and therefore are better mimics, (b) due to intersexual genetic correlations, sexually monomorphic mimics are better mimics than female‐limited mimics, and (c) mimetic resemblance is better on the dorsal wing surface that is visible to predators in flight. Using a physiological model of avian color vision, we quantified mimetic resemblance from predators’ perspective, which showed that female butterflies were better mimics than males. Mimetic resemblance in female‐limited mimics was comparable to that in sexually monomorphic mimics, suggesting that intersexual genetic correlations did not constrain adaptive response to selection for female‐limited mimicry. Mimetic resemblance on the ventral wing surface was better than that on the dorsal wing surface, implying stronger natural and sexual selection on ventral and dorsal surfaces, respectively. These results suggest that mimetic resemblance in butterfly mimicry rings has evolved under various selective pressures acting in a sex‐ and wing surface‐specific manner.