Feature Saltation and the Evolution of Mimicry

ORIGINAL ARTICLE

doi:10.1111/j.1558-5646.2011.01482.x

FEATURE SALTATION AND THE EVOLUTION OF MIMICRY

Gabriella Gamberale-Stille,1,2 Alexandra C. V. Balogh,1,3 Birgitta S. Tullberg,1 and Olof Leimar1,4 1Department of Zoology, Stockholm University, 10691 Stockholm, Sweden 2E-mail: [email protected] 3Environmental & Marine Biology, Abo˚ Akademi University, FIN-20520 Turku, Finland 4Wissenschaftskolleg zu Berlin, Wallotstrasse 19, 14193 Berlin, Germany

Received May 27, 2011 Accepted September 26, 2011

In Batesian mimicry, a harmless prey species imitates the warning coloration of an unpalatable model species. A traditional suggestion is that mimicry evolves in a two-step process, in which a large mutation ﬁrst achieves approximate similarity to the model, after which smaller changes improve the likeness. However, it is not known which aspects of predator psychology cause the initial mutant to be perceived by predators as being similar to the model, leaving open the question of how the crucial ﬁrst step of mimicry evolution occurs. Using theoretical evolutionary simulations and reconstruction of examples of mimicry evolution, we show that the evolution of Batesian mimicry can be initiated by a mutation that causes prey to acquire a trait that is used by predators as a feature to categorize potential prey as unsuitable. The theory that species gain entry to mimicry through feature saltation allows us to formulate scenarios of the sequence of events during mimicry evolution and to reconstruct an initial mimetic appearance for important examples of Batesian mimicry. Because feature-based categorization by predators entails a qualitative distinction between nonmimics and passable mimics, the theory can explain the occurrence of imperfect mimicry.

KEY WORDS: Animal cognition, Batesian mimicry, categorization, defensive coloration, signaling.

The debate on Batesian mimicry evolution (Bates 1862), over predators’ learning about prey (Schmidt 1958). This can have im- whether the process is gradual or saltational (Punnet 1915; Fisher portant implications for the so-called two-step process of mimicry 1927; Goldschmidt 1945), started nearly a century ago. In this de- evolution (Nicholson 1927; Turner 1984; Ruxton et al. 2004). In bate, the importance of predator perception was acknowledged, the two-step process, a large mutation first achieves approximate but no comprehensive theory of how predators recognize and dif- similarity to the model, after which smaller changes can improve ferentiate prey was developed. The currently prevailing idea of the likeness. Our aim here is to employ ideas from animal psy- how predators perceive model-mimic similarity is that all aspects chology about categorization of complex stimuli to explain how of appearance have the same kind of impact on prey recognition predators can perceive the initial mimetic mutant as being similar and generalization (Turner 1981; Dittrich et al. 1993; Ruxton et al. to the model. The explanation thus sheds light on the crucial first 2004; Bain et al. 2007). Where strikingly imperfect mimicry has step of Batesian mimicry evolution. been observed, it is generally explained as wide generalization We suggest that predators form categories to decide on prey of a highly distasteful model (Ruxton et al. 2004). A contrast- suitability. If the categorization is based primarily on a single ing approach is to apply the claim by Tinbergen (1951) “that an prey trait, a relatively small genetic change in prey may produce animal does not react to all the changes in the environment that a large change in appearance as perceived by predators. Such its sense organs can receive, but only to a small part of them” to feature saltation could cause a qualitative shift in categorization

C 2011 The Author(s). Evolution C 2011 The Society for the Study of Evolution. 807 Evolution 66-3: 807–817 GABRIELLA GAMBERALE-STILLE ET AL. from suitable to unsuitable prey, thereby initiating mimicry evo- Materials and Methods lution. In contrast, if simultaneous mutational changes in several We examined Batesian mimicry evolution through computer sim- different traits would be required, the initial phase of the two-step ulations of predator–prey communities. The approach is inspired process becomes implausible. For this reason, and based on our by our previous theoretical work on the evolution of Mullerian¨ evolutionary simulations, we further hypothesize that if the fea- mimicry (Balogh et al. 2010). Prey appearance is represented as ture used for categorization is made up of more than one trait, an array of trait values, x = (x1, ..., xn), in an n-dimensional trait selection for mimicry becomes constrained by the appearance of space. the ancestral state of the mimic-to-be. Thus, one or more components of the feature may need to evolve for nonmimetic reasons NONMIMETIC PREY NICHE (e.g., thermoregulation) before a saltation to mimicry becomes In Batesian mimicry evolution, a mimic-to-be starts out as a likely. In our simulations, we explore the importance of a feature species of “ordinary” palatable prey, which might be part of a saltation, the effect of feature dimensionality, and the effect of the larger community that the predator frequently encounters and appearance of the ancestral state on the probability of Batesian knows is edible. For the modeling, we need to specify the inter- mimicry evolution. action between these kinds of prey and predators. We have taken Psychological theories of categorization and concept forma- into account two types of effects. First, considering the situation tion propose that objects are represented as collections of features. in which a hunting predator is in the vicinity, an ordinary prey By comparing common and distinctive features, individuals cat- individual has a reduced probability of being attacked because egorize objects as similar or dissimilar (Tversky 1977; Treisman it might avoid discovery (crypsis), but also because there may and Gelade 1980). Experiments show that animals often use one be other ordinary prey in the vicinity that attract the predator’s or a few features when discriminating among stimuli (Troje et al. attention, or because body proportions and other aspects of the 1999). There are also studies indicating that such categorization phenotype of ordinary prey improve their ability to escape an at- occurs in predators discriminating suitable from unsuitable prey tack, compared to members or mimics of an aposematic species (Schmidt 1958; Aronsson and Gamberale-Stille 2008). A related (Ruxton et al. 2004). In general, we can describe a nonmimetic strategy of similarity judgment is to encode stimuli hierarchi- prey niche as a region of trait space and, for simplicity, we use a cally at two levels of detail: category-level information is used spherical region. We also use a function to describe fitness effects first to sort stimuli into crude categories, whereupon fine-grain for this niche: information completes the judgment (Huttenlocher et al. 2000). 1 We propose a hierarchical or sequential stimulus processing by f (x) = . (1) 0 1 + exp [ρ (|x − x |−R )] predators, in which first a feature is used for crude categorization, 0 0 0 followed by a comparison of additional prey traits. The signifi- | − | cance for mimicry evolution is that, if predators have the tendency The point x0 is the center of the region, x x0 is the = to generalize broadly between prey types that share a feature, there distance of x from the center, R0 0.15 is the radius of the ρ = may be sufficient advantage for new, imperfect mimics to become region, and 0 50 measures the steepness of the function at established. Fine-grained judgments can then favor subsequent the boundary. The proportional reduction in the probability that a improvement of the mimicry. nearby predator will successfully attack a focal nonmimetic prey In this study we develop the theory of Batesian mimicry evo- individual is then taken to be lution in two ways. First, we use individual-based simulations to 1 − f0(x)κ, (2) investigate the evolution of Batesian mimicry when predators process prey stimuli in a sequential or hierarchical manner, involving where κ = 0.8 is a parameter (between 0 and 1) that measures the feature-based categorization followed by generalization over all strength of effects such as crypsis and escape capability, which prey traits. For illustration purposes we use one specific example serve to protect nonmimetic prey from predation. of mimicry evolution in our simulations, but the qualitative sim- Second, we allowed for the possibility that predators learn ulation results are general and can be applied to different cases. more slowly about the palatability of individual ordinary prey, Second, we explore well-known examples of Batesian mimicry in the sense of a lower rate of forming an association between and construct scenarios of mimicry evolution for these, in accor- palatability and a particular ordinary prey appearance x.Weused dance with the results of our simulations. The scenarios illustrate a parameter L0 = 0.2 (between 0 and 1) to scale the learning the two-step process, in which the first step assumes feature cate- rate for prey that a predator classifies as ordinary. For simplicity, gorization by predators and gives rise to an imperfect but passable we assumed that the probability of this classification is given by incipient mimic, which can be seen as a kind of “missing link” in f0(x), so if a prey item’s traits are in the nonmimetic prey niche, it the evolution of mimicry. is likely to be classified as ordinary prey (in principle, other prey

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types, outside of the particular region of trait space, might also item is classified as having the feature, a broad generalization fall into the category of ordinary nonmimetic prey). From what is width ω will be used for all trait dimensions. An interpretation known about the importance of prey salience and visual contrast is that when the feature is shared, the predator becomes less dis- against the background for predator learning (Ruxton et al. 2004), criminating with respect to differences in other details of prey such an influence on the rate of learning seems realistic. However, appearance. If the feature is present only in the model, we as- our simulations showed that it has little effect on Batesian mimicry sume that there is no generalization between the model and the evolution, in particular in comparison with the effects described new prey. Finally, if the feature would be lacking in both the pre- by equation (2), so it plays no role for our results. For this reason, viously experienced and the new prey, a narrow generalization we do not discuss it further. width σ is used for all traits. After a successful attack, a predator has information about FEATURE-BASED CATEGORIZATION OF the prey unpalatability y (ranging from high palatability, y = –1 UNPALATABLE PREY to high unpalatability, y = 1), in addition to the multidimensional One or more of the prey traits can be used by predators for the phenotype x. We describe the predator’s experience as a list of the categorization of unpalatable prey. The reaction of predators to xi and yi for the prey it has attacked, together with the feature- prey appearances may partly be innate (Ruxton et al. 2004), but based classification. The probability of the predator successfully to a large extent categorization would be the result of a predator’s attacking a discovered prey is written as experience of unpalatable prey. The overall idea is that catego- 1 − f (x)κ rization of prey is an efficient way for predators to deal with a q h, x = 0 . ( ) + − (4) complex world (Kikuchi and Pfennig 2010a). We will not go into 1 exp [s(h h0)] details in our modeling about how experiences give rise to categorization. We simply assume that a region of the trait space In this expression, equation (2) was used to adjust the prob- corresponds to high salience and therefore can play the role of a ability of attack for nonmimetic prey and h depends on the ap- feature. For one-dimensional features, we used x1 as the feature pearance x of the prey and on the predator’s experience. The dimension, and the part of the trait space that corresponds to an dependence on h has a sigmoid shape, h0 = 2.5istheinflex- interval of this dimension as a feature region. The probability that ion point of that curve, and s = 2 is a measure of the steep- a predator classifies a prey item as possessing the feature is a ness of the curve at that point. We can think of h as the degree sigmoid function of the distance of the prey item’s feature trait of attack inhibition towards prey with appearance x and it is from the center of the feature interval. Thus, the probability of given by feature classification is m h(x) = g(x, xi , F, Fi ) yi , (5) = 1 , f (x) (3) i=1 1 + exp [ρ(|x1 − x1F |−RF )] where m is the number of previously attacked prey, F is a 0/1 where R is half the length of the interval with center at x and F 1F variable that indicates whether the feature was detected for the ρ = 100 measures the steepness of the function at the boundary of current prey item, and Fi is a similar indicator for prey i in the list the region. We also examine features based on two traits, which of experiences. The probability that F = 1 is given by equation may reduce the likelihood of a mutational feature saltation and (3) and the function g is given by thus constrain mimicry evolution. For these we used x1 and x2 ⎧ ⎪ 2 2 as feature dimensions, and as feature region the part of the trait ⎨ exp[−|x − xi | /(2σ )] if F = Fi = 0 2 2 space in which these two traits are within a circle of radius RF and g(x, xi , F, Fi ) = exp[−|x − x | /(2ω )] if F = F = 1, ⎩⎪ i i center at (x1F ,x2F ), with the probability of feature classification 0ifF = Fi (6) given by a relation as the one in equation (3). where

FEATURE-BASED GENERALIZATION AND LEARNING n | − |2 = − 2 We assume that the processing of similarity judgments occurs hi- x xi (x j xij) (7) j=1 erarchically (Huttenlocher et al. 2000). Consider a predator that has learned to avoid the appearance of the individuals of an apose- is the squared Euclidean distance between stimuli, and σ = matic population (the models), who all have a certain feature. 0.1 and ω = 0.8 are the narrow and wide generalization When the predator encounters a new prey individual, it first clas- widths. sifies it as either having or lacking the feature. This classification As in a number of previous modeling studies of the evolution affects the next level of the decision-making hierarchy. If the prey of mimicry (Balogh and Leimar 2005; Franks and Sherratt 2007;

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Ruxton et al. 2008; Balogh et al. 2010), the learning process can color space. The saturation (x1 = S) of the yellow thorax color be viewed as the accumulation of inhibition. was allowed to vary while keeping the hue (H) and lightness (L) constant, with HSL given by H = 0.60, 0.10 ≤ S ≤ 0.91, SIMULATION OF PREDATOR–PREY INTERACTIONS L = 0.50. Low values of S correspond to a greenish gray tho- At the start of a simulation, the prey populations are monomor- rax color and high values correspond to bright yellow. The ab- phic. The prey individuals reproduce sexually and have a diploid domen color was defined as x2 = L, with HSL given by H = genotype, with one locus for each trait and free recombination 0.60, S = 0.10, 0.03 ≤ L ≤ 0.43, thus varying L and keeping H between loci. The individuals of the next generation are formed and S constant. High values of L correspond to a gray abdomen by randomly selecting (with replacement) parents among the sur- and low values correspond to dark or black shades. We used a vivors from the current generation. Mutations occur with a prob- genotype–phenotype mapping according to the following sigmoid ability of 0.0005 per allele and mutational increments are drawn function: from a reflected exponential distribution with standard deviation − = + bk ak , 0.05. xk ak − ξ − (11) 1 + e c( k z) The community consists of N p = 100 predators and two prey types, a and b. Prey type b is the model and has high unpalatabil- where k = 1,2, ξk is a genotypic value in the range 0 ≤ ξk ≤ = ity yb 1 whereas the potential mimic, prey type a, is palatable 1, ak is the lower asymptote of xk , bk is the upper asymptote, with ya = –0.5. At the start of every season, the prey types have c measures the steepness of the sigmoid curve, and z gives the population sizes Na = 1000 and Nb = 5000. A predator indepen- position of the inflexion point (see Fig. S1 in the supporting = dently encounters prey at a rate u 0.04 per unit time and prey online material; a1 = 0.10, b1 = 0.91, a2 = 0.03, b2 = 0.43, c = individual. The population size Na(t)orNb(t) changes after every 20, z = 0.50). The mapping is meant to describe the production time a predator successfully attacks prey of either type (successful of pigment, in the case of x1 yellow pigment and in the case of x2 = attacks are always fatal). The duration T 1 of a season is divided melanin, as a function of the concentration ξk of a transcription into small intervals t = 0.0004 of time. The probabilities Pa and factor.

Pb of an individual predator encountering prey types a and b in a For the abdomen shape, we inscribed the abdomen in a rect- time interval are angle with constant width = 1 and defined x3 as the height of the

rectangle, with 1 ≤ x3 ≤ 2 (illustrated in Fig. S2). We kept the P = u · t · N (t) (8) a a surface area of the abdomen constant = 1 by assuming an increas- and ingly triangular and elongated shape with increasing values of x3. The alleles at the diploid loci for each of the three traits additively = · · . Pb u t Nb (t) (9) determine the genotypic values ξ1 and ξ2 in equation (11) and the

abdomen length x3. The size of the time interval t is small enough for both Pa and P to be small. In this way, we can ignore the possibility of b CASE SCENARIOS several encounters during t. Thus, the probability of no prey To illustrate the results of the evolutionary simulations, we inves- being encountered at all is tigate a number of well-known cases of Batesian mimicry. We selected and analyzed the case studies in the following way. First, Pnone = 1 − (Pa + Pb) . (10) the unpalatable model whose appearance is mimicked should When encountering a prey individual with appearance x, have a central position in a mimicry ring containing several the probability of attack is computed according to equation (4), species. We searched for candidate feature traits among the vi- which depends on the current state of the predator’s inhibition, sually prominent traits that are shared by the members of the from equation (5). If there is an attack, the event is added to the ring. Second, it should be possible to reconstruct a likely an- predator’s experience. This is repeated for each predator, after cestral appearance of the mimic-to-be, based on phylogenetic which the next time interval is handled in the same way, until the information and comparative reasoning. Third, a feature trait was end of the season. selected based on the possibility of single-locus control. If two or more feature dimensions would be required, and pleiotropic TRAIT SPACE FOR SIMULATION EXAMPLE single-locus control of these dimensions seemed unlikely, we ex- In the simulations, the prey had three traits—green/yellow thorax amined whether nonmimetic evolution could produce a phenotype color x1, gray/black abdomen color x2, and elongated/square ab- that would be a likely starting point for a feature mutation. Pro- domen shape x3—each of which was controlled by an unlinked ceeding in this way, we obtained scenarios of Batesian mimicry diploid locus. For the coordinates x1 and x2,weusedtheHSL evolution, starting with a reconstructed original appearance of the

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backing up the scenarios is found in the supporting online material (Supporting Information).

Results EVOLUTIONARY SIMULATIONS Saltational evolution of Batesian mimicry may have occurred in the Yellow-banded sphinx (Rubinoff and Le Roux 2008), which is a moth that mimics bumblebees (see below). We used this example for our evolutionary simulations. Figure 1A illustrates the trait space and the evolution of Batesian mimicry. The green sphere represents the nonmimetic prey niche, which is within the category of “ordinary prey” and is the starting-point of mimics- to-be in a simulation. Predators use thorax color as a feature: for a sufficiently high saturation of yellow, as illustrated by the yellow feature region in Figure 1A, which corresponds to

x1F = 0.85 and RF = 0.15 in equation (3), they tend to categorize prey as modellike, by generalizing more widely over all prey traits. At the start of the simulation illustrated in Figure 1A and Figure 2, the members of the model population have trait value

xb = (0.90, 0.05, 1.05) and the potential Batesian mimics start

at xa = (0.15, 0.40, 1.50). This means that they initially have traits situated in the center of the nonmimetic prey niche (the green sphere in Fig. 1A), having a greenish gray thorax color, and an elongated, gray abdomen. The model individuals have a saturated yellow thorax, and a black, square abdomen. In Figure 1A, the model traits would be situated in the lower right part of the yellow box. In the simulation, after around 1400 generations, Figure 1. Illustration of the trait space for the Yellow-banded a feature mutant succeeded in entering the mimicry ring (Figs. 1A sphinx example. The trait x gives the saturation of yellow thorax 1 and 2B), after which the mimic appearance gradually approached color, x2 the lightness of the abdomen, and x3 its elongation. (A) Traits within the green sphere correspond to a nonmimetic prey the model (Figs. 1A and 2 C, D). niche, whereas those within the yellow box have a high probabil- In further simulations, we explored the possibility that preda- ity of being classiﬁed by predators as possessing the feature, that tors use the combination of a yellow thorax and a dark abdomen is, a highly saturated yellow thorax color. The long arrow repre- for feature recognition in the Yellow-banded sphinx example. In sents a feature saltation and the train of smaller arrows represents these simulations, predators used a two-dimensional feature con- gradual evolution of the mimic towards the model appearance. sisting of the combination of a yellow thorax and a dark abdomen. The sketched phenotypes are drawn in the trait space roughly at We implemented the corresponding feature region in trait space positions that correspond to their traits. (B) The feature region is as the yellow cylinder segment illustrated in Figure 1B (the cen- changed to correspond to the combination of a yellow thorax and = a dark abdomen. The saltation in (A) no longer results in a pass- ter of the cylinder is (x1F ,x2F ) (1.0, 0.0) and the radius is able mimic. However, after an evolutionary change to a darker RF = 0.30). First, we conducted a simulation assuming the same abdomen (e.g., thermal melanism; dark sphere), a saltation to a nonmimetic ancestral appearance as in the previous case (Fig. 1A) yellow thorax produces a passable mimic, which then can evolve as the starting point. Over the duration of the simulation (25,000 towards increased similarity to the model. generations), no successful feature saltation occurred and no similarity to the model was established (Fig. S3). The likely reason is that double mutants, having both a yellow thorax and a dark mimic-to-be, followed by the application of a feature mutation abdomen, are very rare, and if they occur, recombination fairly to this appearance, creating an imperfect first mimic carrying the rapidly breaks down the trait combination producing the feature, feature, and finally a number of smaller changes in several traits, so their descendants inherit the feature only to a limited extent. leading to the current mimic appearance. Detailed information This implies that simultaneous evolutionary saltations in multiple,

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Figure 3. Mimicry evolution in the Yellow-banded sphinx. In this scenario, Batesian mimicry evolves from an ancestral appearance (A), initiated by a saltation in thorax color that produces passable mimicry (B), followed by successive improvements towards a more accurate mimic (C) of the bumblebee model (D). The assumed ancestral appearance (A) is similar to the sister species, the Willowherb hawkmoth, which has a color pattern typical of their genus, Proserpinus. The yellow thorax of the imperfect mimic (B) may be used as a feature by predators, to classify unproﬁtable prey. The perfected mimic (C) has a melanistic, shortened, and broadened abdomen.

sion. In general, the appearance of such preadaptations, enabling a subsequent change to approximate similarity, can be an important ingredient in the evolution of Batesian mimicry.

SCENARIOS OF SALTATIONAL BATESIAN MIMICRY EVOLUTION Figure 2. Evolutionary simulation of the origin of mimicry The Yellow-banded sphinx occurs in the northern parts of North through feature saltation (as outlined in Fig. 1A). Prey appearance America and is believed to be a mimic of bumblebees. In the sce- has three components: thorax color, x ; abdomen color, x ;and 1 2 nario, the ancestral appearance (Fig. 3A) is similar to the extant abdomen shape, x3. (A) Phenotypes of individuals from mimic and model populations at four points in time: before mimicry evolves, sister species that shares a green–gray, possibly cryptic, color pat- at the ﬁrst appearance of feature mutants, after further adjust- tern with the majority of the species in the genus (Rubinoff and ment of mimicry, and when mimicry is nearly perfected. Light blue Le Roux 2008). The feature mutation consists in an increased yel- (orange) points in (B) to (D) indicate traits of randomly sampled in- low pigmentation of the thoracic scales (Fig. 3B). The mutation dividuals of the mimic (model) population. Blue and orange crosses results in a qualitative change in appearance and could shift the indicate traits of the corresponding phenotypes in (A). perception of the moth so that many predators categorize it as a bumblebee when it is foraging for nectar. The scenario is based on genetically independent feature traits are unlikely to contribute to the evolutionary simulation described in Figure 1A and Figure 2. mimicry evolution. As an alternative to the scenario in Figure 3, one could also Second, we assumed a nonmimetic ancestral appearance consider the possibility indicated in Figure 1B, that the feature with a somewhat darker abdomen (Fig. 1B), which for instance that characterizes the bumblebee mimicry ring is a combination could result from selection for thermoregulation in colder condi- of a yellow thorax and an otherwise dark body. In such a case, tions (thermal melanism is common in insects; Clusella Trullas thermal melanism (Clusella Trullas et al. 2007) could play the et al. 2007). For this ancestral appearance, simulation showed role of a preadaptation for mimicry evolution, as outlined in that mimicry can evolve through feature saltation (Figs. 1B and Figure 1B. S4), even if the feature is two-dimensional. Effectively, because A trait functions as a feature by aiding the efficient classi- the starting phenotype already possesses one feature component, fication of prey. A feature should thus be salient, that is, easily the feature saltation is reduced to changing the remaining dimen- perceived by potential predators. To play an important role in

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Figure 5. Origin of mimicry in females of the Mocker swallow- Figure 4. Mimicry evolution in the Red-spotted purple butterfly. tail butterfly. In the scenario, Batesian mimicry evolves from an In the scenario, Batesian mimicry evolves from an ancestral non- ancestral nonmimetic appearance (A), through an initial saltation mimetic appearance (A), through an initial saltation to passable to passable mimicry (B), followed by successive improvements of mimicry (B), followed by successive improvements of mimicry (C) mimicry (C) of the Friar model (D). The assumed ancestral appear- of the Pipevine swallowtail model (D). The nonmimicking ances- ance (A) is reconstructed as an intermediate between the female tral form (A) is similar to the conspecific White-banded admiral of the sister species, the Apple-green swallowtail, and the extant and other Palearctic Limenitis species. The melanism in the wings male Mocker swallowtail appearance. The light patches separated of the mimetic mutant (B) is a feature used by predators to clas- by the dark band across the front wings of the imperfect mimic sify distasteful prey. The perfected mimic, the Red-spotted purple (B) may be used as a feature by predators, to classify unprofitable in (C), has increased areas of blue-green iridizing structural color, prey. The perfected hippocoon mimic (C) has lost the tails, acquired decreased red areas, and a changed wing shape. a white background color and modified the shape of the black pattern. mimicry, it should also be shared by the species in a local mimicry A spectacular case of polymorphic mimicry occurs in the ring. An example is the dark brown or black wing color in the Mocker swallowtail butterfly, Papilio dardanus (Ruxton et al. much-studied butterfly mimicry ring centered around the Pipevine 2004). The species is distributed across sub-Saharan Africa, with swallowtail, Battus philenor, a toxic species of Central and North around 25 different female color morphs, many of which are America that is a model for several Batesian and Mullerian¨ mimics mimetic, and with nonmimetic, monomorphic males (Clark and (Platt et al. 1971; Platt 1975). The Red-spotted purple, Limenitis Vogler 2009). Phylogenetic and biogeographical evidence sup- arthemis astyanax, is known to be a Batesian mimic in this ring ports a single origin of mimicry in the species (Clark and Vogler (Platt et al. 1971; Platt 1975). In the Limenitis arthemis-complex, 2009), and the widespread female morph hippocoon and the there are three subspecies; the nonmimicking White-banded ad- similar-looking allopatric hippocoonides are thought to resemble miral,L.a.arthemis, and the Pipevine swallowtail mimics L. a. the original mimetic variant (Clarke and Sheppard 1960; Nijhout astyanax and L. a. arizonensis. Figure 4 shows a scenario of Bate- 2003). These two morphs mimic populations of the Friar, Amauris sian mimicry evolution in this group, with a white-banded form as niavius, and there is observational evidence that the mimicry is the ancestral state (Fig. 4A), as white banding is the rule among Batesian (Carpenter 1942). To characterize the origin of mimicry Palearctic Limenitis species (Mullen 2006). The feature mutation as a feature saltation (Fig. 5), one needs to specify the appear- involves increased melanism, covering most of the white bands ance of the female Mocker swallowtail before mimicry evolved, (Platt 1975) (Fig. 4B). White banding is mainly controlled by a as well as the first mimetic form. In the scenario, the ancestral single locus (Platt 1975), consistent with the idea that a single female appearance (Fig. 5A) is a modification of the females feature mutation could produce a large change in visual appear- of the sister species (Clark and Vogler 2009), the Apple-green ance, shifting the mutant (Fig. 4B) into the same category as the swallowtail Papilio phorcas, in the direction of the current males model (Fig. 4D). Subsequent gradual changes on the dorsal side of the Mocker swallowtail, representing a correlated response to of the wings include an increase in the areas with blue struc- presumed sexual selection on the males, who have diverged from tural color, a decrease in the orange-red spots, and a changed a typical Papilio male appearance (see Fig. S5 in the supporting wing shape (Fig. 4C), further improving the similarity to the online material). In this way, the scenario incorporates the princi- model. ple illustrated in Figure 1B, that nonmimetic evolutionary change

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might be needed to set the stage for a mimetic feature saltation. Starting from the ancestral female appearance (Fig. 5A), a mutant having the light yellow forewing area split into separated patches (Clarke and Sheppard 1960; Nijhout 2003) (Fig. 5B) becomes a passable mimic of the Friar model (Fig. 5D). Morphologically, the mutant consists in an increased melanism of interspaces on the forewing (Clarke and Sheppard 1960; Nijhout 2003). The mimicry would be passable if predators use this aspect of the Friar’s color pattern—light patches, two on each side of the body, surrounded by a dark pattern (Fig. 5D)—as a feature for classification of prey. This role as a feature is supported by the sharing of the characteristic color pattern by several mimics of the Friar model, both Batesian and Mullerian,¨ for instance in a local West Figure 6. Mimicry evolution in the snake tribe Lampropeltini. Batesian mimicry evolves from an ancestral cryptic color pattern African mimicry ring (Owen 1974). Further, fine-tuning of the (A), initiated by a change of color in the dorsal blotches from hippocoon mimic includes a loss of the tails, a whitening of the brown to red, resulting in an imperfect mimic (B), followed by background color, and a modification of the shape of the black ﬁne-tuning of the appearance into more perfect mimicry (C) of pattern (Fig. 5C). the highly poisonous Eastern coral snake model (D). The ancestral Our scenarios so far have dealt with insects, but the same appearance (A) is a common cryptic pattern in extant Lampropel- principles of mimicry evolution can be applied to other groups tini. The change to red blotch color in the mutant (B) is used as of organisms. New World coral snakes in the family Elapidae are a feature by predators to classify dangerous prey. The more per- venomous and often brightly colored, typically with red, black, fected mimic (C) has body-encircling rings, a change from light brown to yellow color, and broader black bands. and yellow rings encircling the body. Many species of harmless snakes, for instance in the family Colubridae (e.g., milk snakes and king snakes) adopt a coloration similar to that of coral snakes, ors, repetitively displayed, could be a feature used by predators which has been interpreted as Batesian mimicry (Greene and to categorize dangerous and therefore unsuitable prey and may McDiarmid 1981; Pough 1988; Savage and Slowinski 1992). thus constitute the first step of mimicry evolution in Lampro- Based on phylogenetic information for Lampropeltini, it has been peltis and other lampropeltinine snakes (cf. Fig. 1 in Kikuchi argued that crypsis is the ancestral state and that coral snake and Pfennig 2010a). This kind of a feature-based categoriza- mimicry has evolved from crypsis within this group (Pyron and tion could explain the rough and imperfect mimicry in some Burbrink 2009). A typical colubrid coloration is that of Lam- milk snakes (Bryson et al. 2007). Following the feature muta- propeltis triangulum triangulum (Bryson et al. 2007), which has tion, further improvements in the resemblance to the model (Fig. darkish brown blotches lined with black on a lighter background 6D) are for instance the formation of rings from blotches, the (Fig. 6A) and is considered to be cryptic through background change from light brown to yellow, and an increase in the width matching and/or disruptivity. Other populations with ringed color of the black bands (Fig. 6C) to a more perfected mimicry as patterns in the species, as represented by L. t. elapsoides (Scarlet occurs in for instance L. elapsoides, L. alterna, L. pyromelana, and kingsnake), are considered as good mimics of M. fulvius (Bryson L. zonata. et al. 2007), whereas the form L. t. temporalis, has red blotches instead of rings, and has been regarded as a poor mimic (Pfennig et al. 2007). Discussion It has been suggested that an incipient Batesian mimic would The evolution of mimicry has offered a puzzle because it often in- require at least two coral snake colors (Hinman et al. 1997). volves major changes in a suite of characters. The main difficulty From the principle illustrated in Figure 1B, emphasizing the dif- for incipient mimicry is that mutants may find themselves in an ficulty of simultaneous saltational evolution in genetically in- adaptive valley, because their similarity to the model is insuffi- dependent traits, this implies that one coral snake color would cient and, in the case of Batesian mimicry, deviation from other need to be present before a feature matation occurs. In our sce- prey and perhaps a loss of crypsis reduce fitness. There is experi- nario, the feature mutation involves a change of brown areas mental evidence for adaptive valleys in Batesian mimicry evolu- (Fig 6A) to red in which the resulting poor mimic (Fig. 6B) tion (Mappes and Alatalo 1997), suggesting that the phenomenon might still be relatively cryptic at a distance, and therefore the could be common. In some cases, however, there might not be transition may not be very costly in terms of detectability. The a valley, which has been proposed in the context of coral snake appearance of black-bordered red blotches, two coral snake col- mimicry. In situations of high model toxicity and abundance,

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predators might generalize so widely that intermediates between from unsuitable prey, such as patterns on differently colored arti- an original appearance and accurate mimics are not attacked more ficial prey (Aronsson and Gamberale-Stille 2008), the amount of frequently than the original appearance (Kikuchi and Pfennig black in the black and yellow pattern in puffer fish mimics (Caley 2010a). Batesian mimicry evolution would then become a straight- and Schluter 2003), or ring order in coral snake mimicry (Kikuchi forward hill-climbing process. and Pfennig 2010b). There are also other explanations for imper- In situations where there is a fitness valley, our evolutionary fect mimicry, of which perhaps the most frequently suggested is simulations and scenarios show that the valley can be crossed if that common and highly distasteful models are compatible with predators pay particular attention to some characters and use these imperfect mimicry (Lindstrom¨ et al. 1997). Other possibilities are as features for categorization of complex prey stimuli. Feature- a plentitude of alternative prey (Lindstrom¨ et al. 2004) or the al- based categorization can thus be a crucial element in the evolution ternation over a season of different models (Sherratt 2002). There of Batesian mimicry and the results we obtained give credence to is evidence that mimetic accuracy can correlate negatively with the hypothesized two-step process in a space of realistic, multitrait model abundance (Harper and Pfennig 2007), but in general the appearances. The idea of feature-based classification by predators relative importance of the different possible explanations is not can also help explain the evolution of Mullerian¨ mimicry (Balogh known. et al. 2010), by minimizing the effect of selection against inter- A feature mutant represents a kind of “missing link” in Bate- mediates between aposematic forms. In addition, feature saltation sian mimicry evolution. We propose that its appearance can be could also help explain the occurrence of major gene effects in reconstructed and suggest potential scenarios of character evo- mimicry evolution (Baxter et al. 2009), and thus contribute to the lution for several well-known cases of mimicry. These scenarios on-going investigation of genetic changes during adaptation (Orr are based on several pieces of information, foremost the likely 2005). ancestral and model character states and in most cases the type The number of characters used for unprofitable prey recog- of genetic inheritance of traits. We suggest a new line of research nition considerably limits the probability for Batesian mimicry where the likelihood of specific scenarios are investigated in ex- to evolve. Our simulations suggest that if predators use multidi- periments in which manipulated prey are used to test whether the mensional features, and changes are needed in several genetically suggested character saltations function in predator categorization independent dimensions of prey appearance, no saltation occurs of unpalatable prey. In conclusion, we propose that the incorpo- and therefore no mimicry evolves. However, it is possible that ration of established psychological theories of categorization into some of the characters involved may evolve for other reasons, al- the analysis of mimicry can be fruitful. lowing mimicry evolution to follow. Such a case is illustrated for the Yellow-banded sphinx (Fig. 1B), where a presumed melanism ACKNOWLEDGMENTS precedes mimicry evolution. Also, in the scenario with the Mocker We thank C. Wiklund and R. Rutowski for valuable discussion. This work swallowtail butterfly (Fig. 5), we assumed preadaptation of the was supported by grants from the Swedish Research Council to each of the authors. ancestral female appearance. Our reasons for the assumed ancestral appearance is that it is unlikely for mimicry to evolve from a color pattern similar to that of the sister species P. phorcas,asitis LITERATURE CITED Aronsson, M., and G. Gamberale-Stille. 2008. Domestic chicks primarily unlikely that a single genetic change could give rise to a passable attend to colour, not pattern, when learning an aposematic coloration. mimic. Our assumed ancestral appearance in the scenario is in- Anim. Behav. 75:417–423. stead an intermediate between the female color pattern of the sister Bain, R. S., A. Rashed, V. J. Cowper, F. S. Gilbert, and T. N. Sherratt. 2007. species P. phorcas and the male P. dardanus appearance, which The key mimetic features of hoverflies through avian eyes. Proc. R. Soc. Lond. 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Supporting Information The following supporting information is available for this article:

Figure S1. Genotype–phenotype mappings for x1 and x2.

Figure S2. Definition of the abdomen shape parameter x3. Figure S3. Evolutionary simulation corresponding to the illustration in Figure 1B, in which the feature region represents a combination of a yellow thorax and a dark abdomen, so that a single-trait saltation to passable mimicry no longer is possible when starting from the nonmimetic prey niche indicated by the green sphere in Figure 1B. Figure S4. Evolutionary simulation corresponding to the illustration in Figure 1B, in which the feature region represents the combination of a yellow thorax and a dark abdomen. Figure S5. Reconstruction of an ancestral nonmimetic P. dardanus appearance. Appendix S1. Details of case scenarios. Appendix S2. Code and data files for the simulations.

Supporting Information may be found in the online version of this article.

Please note: Wiley-Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article.

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