Feature saltation and the evolution of mimicry

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.     

Unpalatability of viceroy butterflies (Limenitis archippus) and their purported mimicry models,Florida queens (Danaus gilippus)

Summary Understanding the dynamics of defensive mimicry requires accurately characterizing the comparative palatability of putative models and mimics. The Florida viceroy butterfly (Limenitis archippus floridensis) is traditionally considered a palatable Batesian mimic of the purportedly distasteful Florida queen (Danaus gilippus berenice). I re-evaluated this established hypothesis by directly assessing palatability of viceroys and queens to red-winged blackbirds in a laboratory experiment. Representative Florida viceroys were surprisingly unpalatable to red-wings; only 40% of viceroy abdomens were entirely eaten (compared to 98% of control butterfly abdomens), and nearly one-third were immediately tasterejected after a single peck. In fact, the viceroys were significantly more unpalatable than representative Florida queens, of which 65% were eaten and 14% taste-rejected. Thus, viceroys and queens from the sampled populations exemplify Müllerian rather than Batesian mimicry, and the viceroy appears to be the stronger model. These findings prompt a reassessment of the ecological and evolutionary dynamics of this classic mimicry relationship.     

The interaction of thorns and symbiotic ants as an effective defence mechanism of swollen-thorn acacias

Evidence is provided for the interaction of ants (Crematogaster spp.) and thorns as a means of defence against browsing mammals for one species of African myrmecophyte, Acacia drepanolobium. Two experiments were conducted using goats as representative mammalian browsers. In the first experiment, the defences of individual branches were manipulated in order to assess the effectiveness of ants and thorns both on their own and together as anti-herbivore defences. It was shown that ants on their own are more effective defences for a single branch than having neither ants nor thorns, but ants from a single branch do not add significantly to the effectiveness of thorns as an anti-herbivore defence. The second experiment looked at the effect of a whole tree of ants and how they interacted with thorns in the defence of the tree. It was shown that ants from a whole tree do significantly add to the effectiveness of thorns as an anti-herbivore defence. In all cases, the goat refused to go back to and feed from a tree whose ants had just attacked it. Thorns on their own, however, do not act as total browsing deterrents. They slow down the rate of feeding but animals may compensate for this by feeding for longer periods of time. The interaction of a whole tree of ants and thorns is a very effective browsing deterrent which causes the animal to stop feeding almost immediately, therefore keeping the amount of foliage lost to a minimum. These results provide support for the hypothesis that the ant-acacia relationship (in the case of A. drepanolobium) evolved at least partly because of pressure from browsing mammals. Received: 20 October 1997 / Accepted: 28 February 1998     

Batesian mimicry promotes pre‐ and postmating isolation in a snake mimicry complex

We evaluated whether Batesian mimicry promotes early‐stage reproductive isolation. Many Batesian mimics occur not only in sympatry with their model (as expected), but also in allopatry. As a consequence of local adaptation within both sympatry (where mimetic traits are favored) and allopatry (where nonmimetic traits are favored), divergent, predator‐mediated natural selection should disfavor immigrants between these selective environments as well as any between‐environment hybrids. This selection might form the basis for both pre‐ and postmating isolation, respectively. We tested for such selection in a snake mimicry complex by placing clay replicas of sympatric, allopatric, or hybrid phenotypes in both sympatry and allopatry and measuring predation attempts. As predicted, replicas with immigrant phenotypes were disfavored in both selective environments. Replicas with hybrid phenotypes were also disfavored, but only in a region of sympatry where previous studies have detected strong selection favoring precise mimicry. By fostering immigrant inviability and ecologically dependent selection against hybrids (at least in some habitats), Batesian mimicry might therefore promote reproductive isolation. Thus, although Batesian mimicry has long been viewed as a mechanism for convergent evolution, it might play an underappreciated role in fueling divergent evolution and possibly even the evolution of reproductive isolation and speciation.     

Dual mimicry in the dimorphic eusocial wasp Mischocyttarus mastigophorus Richards (Hymenoptera: Vespidae)

The eusocial vespid wasp Mischocyttarus mastigophorus exhibits two colour morphs, with males and females of each morph co-occurring at Monteverde, Costa Rica. Each morph closely resembles a different sympatric species of swarm-founding wasp in the genus Agelaia. We propose that the Agelaia species are models for a dual mimicry system. The Agelaia species (A. yepocapa , mimicked by the M. mastigophorus pale morph, and A. xanthopus , mimicked by the M. mastigophorus dark morph) are locally abundant wasps with large, aggressively defended colonies. The mimic and models are restricted to high-elevation habitat in the Monteverde area, and the elevational ranges of both Agelaia species partially overlap the elcvational range of M. mastigophorus. Relative frequencies of the M. mastigophorus colour morphs vary with elevation, with the pale morph predominating at lower elevations. Elevational differences in the relative abundances of the Agelaia species suggest that the models act as a selective force maintaining the M. mastigophorus colour polymorphism at Monteverde. Mischocyttarus mastigophorus overlaps only A. xanthopus in the northern part of its range (S. Mexico), and overlaps only A. yepocapa in the southern part of its range (Ecuador). We hypothesize that the M. mastigophorus colour morphs evolved in allopatry and later came into contact in Central America. Appropriate high-elevation habitat for cloud forest species is distributed as discrete patches in Central America and Northern South America. The island-like nature of suitable habitat may favour the isolation and rapid evolutionary diversification of vespid species that are restricted to high elevations in the Neotropics.     

Dynamics of the evolution of Batesian mimicry: molecular phylogenetic analysis of ant-mimicking Myrmarachne (Araneae: Salticidae) species and their ant models

Batesian mimicry is seen as an example of evolution by natural selection, with predation as the main driving force. The mimic is under selective pressure to resemble its model, whereas it is disadvantageous for the model to be associated with the palatable mimic. In consequence one might expect there to be an evolutionary arms race, similar to the one involving host-parasite coevolution. In this study, the evolutionary dynamics of a Batesian mimicry system of model ants and ant-mimicking salticids is investigated by comparing the phylogenies of the two groups. Although Batesian mimics are expected to coevolve with their models, we found the phylogenetic patterns of the models and the mimics to be indicative of adaptive radiation by the mimic rather than co-speciation between the mimic and the model. This shows that there is strong selection pressure on Myrmarachne, leading to a high degree of polymorphism. There is also evidence of sympatric speciation in Myrmarachne, the reproductive isolation possibly driven by female mate choice in polymorphic species.     

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.     

Predation on snakes of Argentina: Effects of coloration and ring pattern on coral and false coral snakes

The occurrence of coral snake coloration among unrelated venomous and non‐venomous snake species has often been explained in terms of warning coloration and mimicry. In Argentina, no field tests have been conducted to confirm this mimetic association between one venomous coral species (Micrurus phyrrocryptus, Elapidae) and two non‐venomous snake species with a similar color pattern (Lystrophis pulcher and Oxyrhopus rhombifer, Colubridae). The aims of this work were to test for the possible aposematic or cryptic function of the ring pattern and coloration of coral snakes and false coral snakes from central Argentina, and to analyse whether the pattern is effective throughout the year. Predation on snakes was estimated by using non‐toxic plasticine replicas of ringed venomous and non‐venomous snakes and unbanded green snakes placed along transects in their natural habitat during the dry and rainy season. Ringed color pattern was attacked by predators despite the background color. One of the replica types was attacked more than expected during the dry season, suggesting that both shape and width of rings may influence the choice by predators. The reaction of predators towards replicas that mimic snake species with ringed patterns is independent of the geographical region, and we can conclude that mimicry characteristics are quite general when the true models are present in the area.     

Effects of a larval antipredator response and larval diet on adult phenotype in an aposematic ladybird beetle

Many ladybird beetles respond to a potential predation event by `reflex bleeding' or secreting a noxious defensive chemical that is similar to hemolymph. Both adults and larvae show this response. Reflex bleeding is known to reduce predator attack rates and increase prey survival after an attack, especially when reflex bleeding is employed in combination with other cues such as odor and warning coloration. In this experiment, we examined how variability in the number of reflex bleeding events and food quality in the larval stage of the aposematic ladybird beetle Harmonia axyridis affected elytral color, development time, and terminal size in adults. Effects of reflex bleeding were subtle and may have been influenced by diet treatments. Adult color did not differ between bleed treatment groups but beetles that reflex bled tended to take longer to develop and grow to smaller sizes than control group beetles. There were clear and strong effects of larval diet on adult phenotype: an ad libitum pollen diet resulted in paler adult coloration, shorter development time, and larger adult size relative to a limited-availability aphid diet. Our results suggest that the best environment for producing bright-red coloration may not be the best environment for favorable expression of life history characters, especially under stressful conditions. Interactions between different life history stages of H. axyridis are also discussed. Received: 20 April 1997 / Accepted: 30 September 1997     

Experimental field tests of Batesian mimicry in the swallowtail butterfly Papilio polytes

The swallowtail butterfly Papilio polytes is known for its striking resemblance in wing pattern to the toxic butterfly Pachliopta aristolochiae and is a focal system for the study of mimicry evolution. Papilio polytes females are polymorphic in wing pattern, with mimetic and nonmimetic forms, while males are monomorphic and nonmimetic. Past work invokes selection for mimicry as the driving force behind wing pattern evolution in P. polytes. However, the mimetic relationship between P. polytes and P. aristolochiae is not well understood. In order to test the mimicry hypothesis, we constructed paper replicas of mimetic and nonmimetic P. polytes and P. aristolochiae, placed them in their natural habitat, and measured bird predation on replicas. In initial trials with stationary replicas and plasticine bodies, overall predation was low and we found no differences in predation between replica types. In later trials with replicas mounted on springs and with live mealworms standing in for the butterfly's body, we found less predation on mimetic P. polytes replicas compared to nonmimetic P. polytes replicas, consistent with the predator avoidance benefits of mimicry. While our results are mixed, they generally lend support to the mimicry hypothesis as well as the idea that behavioral differences between the sexes contributed to the evolution of sexually dimorphic mimicry.     

On the evolution of mimicry in avian nestlings

Batesian mimicry (BM), where a nontoxic species resembles a toxic species with aposematic coloring, has been recently described for a Neotropical species of the suboscine passerine (Laniocera hypopyrra). Understanding the order and series in which these characteristics evolved is unknown and requires character information from closely related taxa. Here, we trace the origin of mimetic traits and how they evolved by examining antipredator characteristics using images and other field‐collected trait data from nest and nestlings along with data available in the literature for the Laniisominae clade and closely related taxa. We found that morphological modifications of the downy feathers appeared first in the broader clade leading to the Laniisominae clade followed by further morphological and behavioral characteristics within the Laniisominae clade leading to the full BM. Images of nestlings in the Laniisominae and closely related clades demonstrated the extent of antipredator and camouflage characteristics. We found a complex set of behavioral and morphological traits in this clade for reducing predation from hiding to camouflage to mimicry. We further propose the evolution of two distinctive mimicry strategies in the Laniisominae clade: (1) Batesian Mimicry, as described above and (2) Masquerade, resemblance to inedible objects commonly found in their local environment. This complex set of antipredator traits shed light on the diversity of antipredator characteristics in avian nestlings, particularly in neotropical areas where the avian diversity is highest. Unfortunately, there are hundreds of species in the neotropics that lack basic natural history information on nesting traits, and therefore, we are likely missing critical information on the diversity of antipredator characteristics across avian nestlings.     

Experimental and phylogenetic evidence for floral mimicry in a guild of fly-pollinated plants

Mimicry, as an adaptive explanation for the resemblance between organisms, is not always readily distinguishable from, inter alia , coincidence, shared ancestry, or convergent evolution. We tested the hypothesis that two rare South African orchid taxa Brownleea galpinii ssp. major (nectar-producing) and Disa cephalotes ssp. cephalotes (non-rewarding) are mimics of the nectar-producing flowers of a relatively common species, Scabiosa columbaria (Dipsacaceae), with which they always occur sympatrically. Flowers of the orchids were apparently unscented and had similar dimensions and almost identical spectral reflectance to the flowers of Scabiosa . The orchids were pollinated exclusively by long-proboscid flies (Tabanidae and Nemestrinidae) that feed mainly on nectar in Scabiosa flowers. Choice experiments showed that these flies did not discriminate between the orchids and Scabiosa when alighting on their flat-topped inflorescences. However, flies were not attracted to related orchids dissimilar to Scabiosa , or to inflorescences of B. galpinii that had been artificially reconstructed in the shape of a spike, rather than a flat-topped capitulum. A phylogenetic analysis showed traits that give the orchids a resemblance to Scabiosa , such as a flat-topped inflorescence and cream floral colouration with dark spots and short spurs, to be mostly apomorphic features, and therefore likely to be relatively recent adaptations for mimicry. We caution that the term mimic should not be applied to species whose resemblance to another species is due entirely to plesiomorphic traits that, in all likelihood, evolved prior to the ecological association.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 289–304.     

Evolutionary implications of the form of predator generalization for aposematic signals and mimicry in prey

Generalization is at the heart of many aspects of behavioral ecology; for foragers it can be seen as an essential feature of learning about potential prey, because natural populations of prey are unlikely to be perfectly homogenous. Aposematic signals are considered to aid predators in learning to avoid a class of defended prey. Predators do this by generalizing between the appearance of prey they have previously sampled and the appearance of prey they subsequently encounter. Mimicry arises when such generalization occurs between individuals of different species. Our aim here is to explore whether the specific shape of the generalization curve can be expected to be important for theoretical predictions relating to the evolution of aposematism and mimicry. We do this by a reanalysis and development of the models provided in two recent papers. We argue that the shape of the generalization curve, in combination with the nature of genetic and phenotypic variation in prey traits, can have evolutionary significance under certain delineated circumstances. We also demonstrate that the process of gradual evolution of Müllerian mimicry proposed by Fisher is particularly efficient in populations with a rich supply of standing genetic variation in mimetic traits.     

Body size as a primary determinant of ecomorphological diversification and the evolution of mimicry in the lampropeltinine snakes (Serpentes: Colubridae)

Evolutionary correlations between functionally related character suites are expected as a consequence of coadaptation due to physiological relationships between traits. However, significant correlations may also exist between putatively unrelated characters due to shared relationships between those traits and underlying variables, such as body size. Although such patterns are often dismissed as simple body size scaling, this presumption may overlook important evolutionary patterns of diversification. If body size is the primary determinant of potential diversity in multiple unrelated characters, the observed differentiation of species may be governed by variability in body size, and any biotic or abiotic constraints on the diversification thereof. Here, we demonstrate that traits related to both predatory specialization (gape and diet preference) and predatory avoidance (the development of Batesian mimicry) are phylogenetically correlated in the North American snake tribe Lampropeltini. This is apparently due to shared relationships between those traits and adult body size, suggesting that size is the primary determinant of ecomorphological differentiation in the lampropeltinines. Diversification in body size is apparently not linked to climatic or environmental factors, and may have been driven by interspecific interactions such as competition. Additionally, we find the presence of a ‘key zone’ for the development of both rattle‐ and coral snake mimicry; only small snakes feeding primarily on ectothermic prey develop mimetic colour patterns, in or near the range of venomous model species.     

Independent evolution of sexual dimorphism and female‐limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas)

Several species of swallowtail butterflies (genus Papilio) are Batesian mimics that express multiple mimetic female forms, while the males are monomorphic and nonmimetic. The evolution of such sex‐limited mimicry may involve sexual dimorphism arising first and mimicry subsequently. Such a stepwise scenario through a nonmimetic, sexually dimorphic stage has been proposed for two closely related sexually dimorphic species: Papilio phorcas, a nonmimetic species with two female forms, and Papilio dardanus, a female‐limited polymorphic mimetic species. Their close relationship indicates that female‐limited polymorphism could be a shared derived character of the two species. Here, we present a phylogenomic analysis of the dardanus group using 3964 nuclear loci and whole mitochondrial genomes, showing that they are not sister species and thus that the sexually dimorphic state has arisen independently in the two species. Nonhomology of the female polymorphism in both species is supported by population genetic analysis of engrailed, the presumed mimicry switch locus in P. dardanus. McDonald–Kreitman tests performed on SNPs in engrailed showed the signature of balancing selection in a polymorphic population of P. dardanus, but not in monomorphic populations, nor in the nonmimetic P. phorcas. Hence, the wing polymorphism does not balance polymorphisms in engrailed in P. phorcas. Equally, unlike in P. dardanus, none of the SNPs in P. phorcas engrailed were associated with either female morph. We conclude that sexual dimorphism due to female polymorphism evolved independently in both species from monomorphic, nonmimetic states. While sexual selection may drive male–female dimorphism in nonmimetic species, in mimetic Papilios, natural selection for protection from predators in females is an alternative route to sexual dimorphism.     

Diversity of warning signal and social interaction influences the evolution of imperfect mimicry

Mimicry, the resemblance of one species by another, is a complex phenomenon where the mimic (Batesian mimicry) or the model and the mimic (Mullerian mimicry) gain an advantage from this phenotypic convergence. Despite the expectation that mimics should closely resemble their models, many mimetic species appear to be poor mimics. This is particularly apparent in some systems in which there are multiple available models. However, the influence of model pattern diversity on the evolution of mimetic systems remains poorly understood. We tested whether the number of model patterns a predator learns to associate with a negative consequence affects their willingness to try imperfect, novel patterns. We exposed week‐old chickens to coral snake (Micrurus) color patterns representative of three South American areas that differ in model pattern richness, and then tested their response to the putative imperfect mimetic pattern of a widespread species of harmless colubrid snake (Oxyrhopus rhombifer) in different social contexts. Our results indicate that chicks have a great hesitation to attack when individually exposed to high model pattern diversity and a greater hesitation to attack when exposed as a group to low model pattern diversity. Individuals with a fast growth trajectory (measured by morphological traits) were also less reluctant to attack. We suggest that the evolution of new patterns could be favored by social learning in areas of low pattern diversity, while individual learning can reduce predation pressure on recently evolved mimics in areas of high model diversity. Our results could aid the development of ecological predictions about the evolution of imperfect mimicry and mimicry in general.     

Batesian mimics influence the evolution of conspicuousness in an aposematic salamander

Conspicuousness, or having high contrast relative to the surrounding background, is a common feature of unpalatable species. Several hypotheses have been proposed to explain the occurrence of conspicuousness, and while most involve the role of conspicuousness as a direct signal of unpalatability to potential predators, one hypothesis suggests that exaggerated conspicuousness may evolve in unpalatable species to reduce predator confusion with palatable species (potential Batesian mimics). This hypothesis of antagonistic coevolution between palatable and unpalatable species hinges on the ‘cost of conspicuousness’, in which conspicuousness increases the likelihood of predation more in palatable species than in unpalatable species. Under this mimicry scenario, four patterns are expected: (i) mimics will more closely resemble local models than models from other localities, (ii) there will be a positive relationship between mimic and model conspicuousness, (iii) models will be more conspicuous in the presence of mimics, and (iv) when models and mimics differ in conspicuousness, mimics will be less conspicuous than models. We tested these predictions in the salamander mimicry system involving Notophthalmus viridescens (model) and one colour morph of Plethodon cinereus (mimic). All predictions were supported, indicating that selection for Batesian mimicry not only influences the evolution of mimics, but also the evolution of the models they resemble. These findings indicate that mimicry plays a large role in the evolution of model warning signals, particularly influencing the evolution of conspicuousness.     

Salticid predation as one potential driving force of ant mimicry in jumping spiders

Many spiders possess myrmecomorphy, and species of the jumping spider genus Myrmarachne exhibit nearly perfect ant mimicry. Most salticids are diurnal predators with unusually high visual acuity that prey on various arthropods, including conspecifics. In this study, we tested whether predation pressure from large jumping spiders is one possible driving force of perfect ant mimicry in jumping spiders. The results showed that small non-ant-mimicking jumping spiders were readily treated as prey by large ones (no matter whether heterospecific or conspecific) and suffered high attack and mortality rates. The size difference between small and large jumping spiders significantly affected the outcomes of predatory interactions between them: the smaller the juvenile jumping spiders, the higher the predation risk from large ones. The attack and mortality rates of ant-mimicking jumping spiders were significantly lower than those of non-ant-mimicking jumping spiders, indicating that a resemblance to ants could provide protection against salticid predation. However, results of multivariate behavioural analyses showed that the responses of large jumping spiders to ants and ant-mimicking salticids differed significantly. Results of this study indicate that predation pressure from large jumping spiders might be one selection force driving the evolution of nearly perfect myrmecomorphy in spiders and other arthropods.