A molecular phylogeny of the checkered beetles and a description of Epiclininae a new subfamily (Coleoptera: Cleroidea: Cleridae)

We provide the first molecular phylogeny of the clerid lineage (Coleoptera: Cleridae, Thanerocleridae) within the superfamily Cleroidea to examine the two most recently proposed hypotheses of higher level classification. Phylogenetic relationships of checkered beetles were inferred from approximately ～5000 nt of both nuclear and mitochondrial rDNA (28S, 16S and 12S) and the mitochondrial protein‐coding gene COI. A worldwide sample of ～70 genera representing almost a quarter of generic diversity of the clerid lineage was included and phylogenies were reconstructed using Bayesian and Maximum Likelihood approaches. Results support the monophyly of many proposed subfamilies but were not entirely congruent with either current classification system. The subfamilial relationships within the Cleridae are resolved with support for three main lineages. Tillinae are supported as the sister group to all other subfamilies within the Cleridae, whereas Thaneroclerinae, Korynetinae and a new subfamily formally described here, Epiclininae subf.n ., form a sister group to Clerinae + Hydnocerinae.     

Phylogenomic relationships of bioluminescent elateroids define the ‘lampyroid’ clade with clicking Sinopyrophoridae as its earliest member

Bioluminescence has been hypothesized as aposematic signalling, intersexual communication and a predatory strategy, but origins and relationships among bioluminescent beetles have been contentious. We reconstruct the phylogeny of the bioluminescent elateroid beetles (i.e. Elateridae, Lampyridae, Phengodidae and Rhagophthalmidae), analysing genomic data of Sinopyrophorus Bi & Li, and in light of our phylogenetic results, we erect Sinopyrophoridae Bi & Li, stat.n . as a clicking elaterid‐like sister group of the soft‐bodied bioluminescent elateroid beetles, that is, Lampyridae, Phengodidae and Rhagophthalmidae. We suggest a single origin of bioluminescence for these four families, designated as the ‘lampyroid clade’, and examine the origins of bioluminescence in the terminal lineages of click beetles (Elateridae). The soft‐bodied bioluminescent lineages originated from the fully sclerotized elateroids as a derived clade with clicking Sinopyrophorus and Elateridae as their serial sister groups. This relationship indicates that the bioluminescent soft‐bodied elateroids are modified click beetles. We assume that bioluminescence was not present in the most recent common ancestor of Elateridae and the lampyroid clade and it evolved among this group with some delay, at the latest in the mid‐Cretaceous period, presumably in eastern Laurasia. The delimitation and internal structure of the elaterid‐lampyroid clade provides a phylogenetic framework for further studies on the genomic variation underlying the evolution of bioluminescence.     

The model of early evolution of aposematic coloration

First stages of evolution of aposematic coloration include a region of negative selection. During these stages, individuals with aberrant coloration remain to be rare, while predators are still not able to associate coloration with unpalatability. The simulation model is proposed, in which this "problematic zone" is overcome by individual selection for the increasing of unpalatable prey conspicuity in a small unisexual population. It is shown that under this assumption aposematic coloration develops within a wide range of parameters such as the cost of unpalatability, the cost of coloring, the survival rate of unpalatable prey after being attacked by na?ve predator, the probability of discovering of differently colored preys by predator as well as the predator's learning rate and memory depth. Thus, the early evolution ofaposematic coloration does not require any unusual or unique set of circumstances; aposematic coloration along with concomitant Bates mimicry inevitably evolve within a wide range of initial conditions. The loss of cryptic coloration by the original form (e.g., due to a change of food preferences, and thereby the structure of a background coloring, changes in habitat structure, color mutations etc.) is one such condition.     

Conservative coevolution of Müllerian mimicry in a group of rift lake catfish

Biological mimicry has long been viewed as a powerful example of natural selection's ability to drive phenotypic evolution, although continuing debates surround the mechanisms leading to its development and the nature of these mimetic relationships. Müllerian mimicry, in which unpalatable species derive a mutual selective benefit through evolved phenotypic similarity, has alternatively been proposed to evolve through either a two-step process initiated by a large mutational change, or through continuous gradual evolution toward a common aposematic phenotype. I exposed a model predatory fish species to two species of endemic Lake Tanganyikan Synodontis to provide evidence for aposematism and the presence of Müllerian mimicry in these species. Predators quickly became conditioned to avoid the venomous catfish and did not discriminate between the two species when they were switched, supporting a hypothesis of functional Müllerian mimicry in this group of similarly colored fish. Ancestral state reconstructions and statistical comparisons of color pattern divergence in Tanganyikan Synodontis indicate that Müllerian mimicry in these catfish has developed through diversification of an aposematic common ancestor with subsequent conservative mutualistic coevolution among its daughter lineages, rather than advergent evolution of a mimic toward a nonrelated model, as assumed by widely accepted models of Müllerian mimicry evolution.     

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.     

Evolution of the wave: aerodynamic and aposematic functions of butterfly wing motion

Many unpalatable butterfly species use coloration to signal their distastefulness to birds, but motion cues may also be crucial to ward off predatory attacks. In previous research, captive passion-vine butterflies Heliconius mimetic in colour pattern were also mimetic in motion. Here, I investigate whether wing motion changes with the flight demands of different behaviours. If birds select for wing motion as a warning signal, aposematic butterflies should maintain wing motion independently of behavioural context. Members of one mimicry group (Heliconius cydno and Heliconius sapho) beat their wings more slowly and their wing strokes were more asymmetric than their sister-species (Heliconius melpomene and Heliconius erato, respectively), which were members of another mimicry group having a quick and steady wing motion. Within mimicry groups, wing beat frequency declined as its role in generating lift also declined in different behavioural contexts. In contrast, asymmetry of the stroke was not associated with wing beat frequency or behavioural context-strong indication that birds process and store the Fourier motion energy of butterfly wings. Although direct evidence that birds respond to subtle differences in butterfly wing motion is lacking, birds appear to generalize a motion pattern as much as they encounter members of a mimicry group in different behavioural contexts.     

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

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

A role for phenotypic plasticity in the evolution of aposematism

The evolution of warning coloration (aposematism) has been difficult to explain because rare conspicuous mutants should suffer a higher cost of discovery by predators relative to the cryptic majority, while at frequencies too low to facilitate predator aversion learning. Traditional models for the evolution of aposematism have assumed conspicuous prey phenotypes to be genetically determined and constitutive. By contrast, we have recently come to understand that warning coloration can be environmentally determined and mediated by local prey density, thereby reducing the initial costs of conspicuousness. The expression of density-dependent colour polyphenism is widespread among the insects and may provide an alternative pathway for the evolution of constitutive aposematic phenotypes in unpalatable prey by providing a protected intermediate stage. If density-dependent aposematism can function as an adaptive intermediate stage for the evolution of constitutive aposematic phenotypes, differential reaction norm evolution is predicted among related palatable and unpalatable prey populations. Here, I present empirical evidence that indicates that (i) the expression of density-dependent colour polyphenism has differentially evolved between palatable and unpalatable populations of the grasshopper Schistocerca emarginata (= lineata) (Orthoptera: Acrididae), and (ii) variation in plasticity between these populations is commensurate with the expected costs of conspicuousness.     

Conspicuousness,color resemblance,and toxicity in geographically diverging mimicry: The pan‐Amazonian frog Allobates femoralis

Predation risk is allegedly reduced in Batesian and Müllerian mimics, because their coloration resembles the conspicuous coloration of unpalatable prey. The efficacy of mimicry is thought to be affected by variation in the unpalatability of prey, the conspicuousness of the signals, and the visual system of predators that see them. Many frog species exhibit small colorful patches contrasting against an otherwise dark body. By measuring toxicity and color reflectance in a geographically variable frog species and the syntopic toxic species, we tested whether unpalatability was correlated with between‐species color resemblance and whether resemblance was highest for the most conspicuous components of coloration pattern. Heterospecific resemblance in colorful patches was highest between species at the same locality, but unrelated to concomitant variation in toxicity. Surprisingly, resemblance was lower for the conspicuous femoral patches compared to the inconspicuous dorsum. By building visual models, we further tested whether resemblance was affected by the visual system of model predators. As predicted, mimic‐model resemblance was higher under the visual system of simulated predators compared to no visual system at all. Our results indicate that femoral patches are aposematic signals and support a role of mimicry in driving phenotypic divergence or mimetic radiation between localities.     

Did aggregation favour the initial evolution of warning coloration? A novel world revisited

From experiments using novel prey signals to avoid innate reactions to traditional signals, Alatalo & Mappes (1996, Nature, 382, 708-710) concluded that gregariousness would have selected for warning coloration as it originated for the first time, whereas a solitary prey distribution would not. We have investigated this suggestion in experiments using the same novel prey and background symbols and wild-caught great tit, Parus major, predators. We compared the attack rate on cryptic unpalatable and aposematic unpalatable prey in either a solitary or an aggregated treatment. In the aggregated treatment we found no difference in attack rate on cryptic and aposematic prey. In the solitary treatment the attack rate on aposematic prey was significantly lower after one attack and at the end of the experiment. Thus, we conclude that, in so far as these experiments mimic an original predator-prey relationship, they do not give support to the idea that aggregation would have favoured the evolution of warning coloration in unpalatable prey. Copyright 2000 The Association for the Study of Animal Behaviour.     

Adaptive change in protective coloration in adult striated shieldbugs Graphosoma lineatum (Heteroptera: Pentatomidae): test of detectability of two colour forms by avian predators

1. Protective coloration in insects may be aposematic or cryptic, and some species change defensive strategy between instars. In Sweden, the adult striated shieldbugs Graphosoma lineatum (Heteroptera: Pentatomidae) undergo a seasonal colour change from pale brown and black striation in the pre‐hibernating adults, to red and black striation in the same post‐hibernating individuals. To the human eye the pre‐hibernating adults appear cryptic against the withered late summer vegetation, whereas the red and black post‐hibernating adults appear aposematic. This suggests a possibility of a functional colour change. However, what is cryptic to the human eye is not necessarily cryptic to a potential predator. 2. Therefore we tested the effect of coloration in adult G. lineatum on their detectability for avian predators. Great tits (Parus major) were trained to eat sunflower seeds hidden inside the emptied exoskeletons of pale or red G. lineatum. Then the detection time for both colour forms was measured in a dry vegetation environment. 3. The birds required a longer time to find the pale form of G. lineatum than the red one. The pale form appears more cryptic on withered late summer vegetation than the red form, not only to the human eye but also to avian predators. The result supports the idea that the adult individuals of G. lineatum undergo a functional change from a cryptic protective coloration to an aposematic one.     

The use of colour characters in phylogenetic reconstruction

The use of coloration as a source of characters in phylogenetic reconstruction is investigated using 54 published data sets. Studies were divided into two categories based on a priori postulated roles of the coloration: (1) aposematic and mimetic coloration and (2) nonaposematic, nonmimetic coloration plus dual signals. Colour characters superficially appear to provide similar phylogenetic signal to morphological ones in the case of aposematic and mimetic coloration but significantly less in other situations. However, the data indicated that the apparent signal in the aposematic/mimetic studies tends to be in greater conflict with the morphological signal. It is proposed that this reflects constraints in the evolution of colour characters that are part of aposematic/mimetic patterns and not that they are necessarily good indicators of phylogeny.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 193–202.     

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.     

Protection by association: evidence for aposematic commensalism

Aposematism is a well known and widely used strategy for reducing predation by conspicuous signalling of unprofitability. However, the increased conspicuousness could make this strategy costly if there are no secondary defences to back the signal up. This has made the elucidation of the evolutionary mechanisms for aposematism and that of the closely‐related Batesian and Mullerian mimicry difficult. The present study aims to test whether cryptic and nondefended prey could reduce their predation risk by grouping with aposematic and defended prey. To do this, we used groups of artificial baits that were either cryptic and palatable or conspicuous and unpalatable, along with the corresponding control treatments. These were then presented in mixed and homogeneous treatment groups within a field setting and the local wild bird assemblage was allowed to select and remove baits at will. The results obtained show that undefended non‐aposematic prey can benefit by grouping with aposematic prey, with no evidence that predation rates for aposematic prey were adversely affected by this association. These results provide insights into the evolution of Batesian mimicry. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 81–89.     

Phylogenetic comparative analysis supports aposematic colouration–body size association in millipede assassins (Hemiptera: Reduviidae: Ectrichodiinae)

The diversity of colour patterns and its importance in interactions with the environment make colouration in animals an intriguing research focus. Aposematic colouration is positively correlated with body size in certain groups of animals, suggesting that warning colours are more effective or that crypsis is harder to achieve in larger animals. Surprisingly, this relationship has not been recovered in studies investigating insects, which may have been confounded by a focus on aposematic taxa that are also gregarious. Millipede assassin bugs (Hemiptera: Reduviidae: Ectrichodiinae) comprise species with cryptic and aposematic colour patterns across a range of body sizes, are typically solitary as adults and are thus an excellent model for investigating a possible association between colouration and body size. Here, we use a comprehensive phylogeny for Ectrichodiinae, ancestral state reconstruction of colouration, and phylogenetic comparative methods to test for a colouration–body size association. The ancestor of Ectrichodiinae is reconstructed as cryptically coloured, with multiple subsequent transitions between aposematic and cryptic colouration. Aposematic colouration is positively associated with male body length and supports the hypothesis that selection on Ectrichodiinae body size may influence evolutionary transitions between aposematic and cryptic colouration or alternatively that selection for aposematic colouration influences body size evolution.     

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.     

The evolution of conspicuous facultative mimicry in octopuses: an example of secondary adaptation?

The ‘Mimic Octopus’Thaumoctopus mimicus Norman & Hochberg, 2005 exhibits a conspicuous primary defence mechanism (high‐contrast colour pattern during ‘flatfish swimming’) that may involve facultative imperfect mimicry of conspicuous and/or inconspicuous models, both toxic and non‐toxic (Soleidae and Bothidae). Here, we examine relationships between behavioural and morphological elements of conspicuous flatfish swimming in extant octopodids (Cephalopoda: Octopodidae), and reconstructed ancestral states, to examine potential influences on the evolution of this rare defence mechanism. We address the order of trait distribution to explore whether conspicuous flatfish swimming may be an exaptation that usurps a previously evolved form of locomotion for a new purpose. Contrary to our predictions, based on the relationships we examined, flatfish swimming appears to have evolved concurrently with extremely long arms, in a clade of sand‐dwelling species. The conspicuous body colour pattern displayed by swimming T. mimicus may represent a secondary adaptation potentially allowing for mimicry of a toxic sole, improved disruptive coloration, and/or aposematic coloration. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 68–77.     

Molecular phylogenetics of Elateriformia (Coleoptera): evolution of bioluminescence and neoteny

Phylogenetic relationships in the coleopteran Series Elateriformia (click beetles, jewel beetles, fireflies and allies) were investigated using > 3800 nucleotides of partial nuclear (small and large subunit rRNA genes) and mitochondrial (large subunit rRNA and cytochrome oxidase subunit I) gene sequences. The Elateriformia includes several soft‐bodied lineages, some of which retain larviform features in the adult stage (neoteny), and several major bioluminescent groups, including the families Lampyridae (fireflies), Phengodidae and Rhagophthalmidae whose relationships have been contentious. All recognized superfamilies (Elateroidea, Cantharoidea, Byrrhoidea, Buprestoidea, Dascilloidea, Scirtoidea) and 28 of the 37 families, represented in 112 individuals, were included in the analysis. Sequence alignment was based on static and dynamic homology assignments and partial removal of sequences of uncertain homology. Alignment variable regions caused a great deal of uncertainty but also contributed much of the phylogenetic signal that was insufficient to resolve deep relationships when these were removed. The main features of most analyses were the monophyly of Elateroidea + Cantharoidea (= Elateroidea sensu lato), with Omethidae + Telegeusidae frequently occupying the basal node in this group; the affinities of Dascilloidea, Buprestoidea and a (broadly paraphyletic) Byrrhoidea, with unclear relationships among them; and the monophyly of Scirtoidea (including Decliniidae) as a rather distant outgroup to all others. When mapped on the resulting trees, soft‐bodied lineages were polyphyletic, contradicting the former Cantharoidea that had been united by this trait. Transitions to neoteny were either simultaneous with, or subsequent to, the origin of soft‐bodiedness in a minimum of seven lineages. The bioluminescent groups Lampyridae (including the enigmatic genus Drilaster) and the tightly allied Phengodidae + Rhagophthalmidae were never monophyletic. The former showed close relationship to the species‐rich, soft‐bodied families Lycidae and Cantharidae, while the latter grouped with poorly resolved lineages at the base of Elateridae (click beetles). Hence, although key features as soft‐bodiedness, neoteny and bioluminescence in Coleoptera are largely confined to the Elateriformia, they appear to result from multiple origins, showing the propensity of closely related lineages to acquire similar features independently. © The Willi Hennig Society 2007.     

Change in protective coloration in the striated shieldbug <Emphasis Type="Italic">Graphosoma lineatum</Emphasis> (Heteroptera: Pentatomidae): predator avoidance and generalization among different life stages

There are two major forms of protective coloration, camouflage and warning coloration, which often entail different colour pattern characteristics. Some species change strategy between or within life stages and one such example is the striated shieldbug, Graphosoma lineatum. The larvae and the pale brownish-and-black striated pre-diapause adults are more cryptic in the late summer environment than is the red-and black striation that the adults change to after diapause in spring. Here we investigate if the more cryptic pre-diapause adult and larval coloration may affect the aposematic function of the coloration as compared to the red adult form. In a series of trials we presented fifth instar larvae, pale or red adults to shieldbug-naïve domestic chicks, Gallus gallus domesticus, to investigate the birds’ initial wariness, avoidance learning, and generalization between the three prey types. The naïve chicks found the red adults most aversive followed by pale adults, and they found the larvae the least aversive. The birds did not find the larvae unpalatable and did not learn to avoid them, while they learned to avoid the two adult forms and then to a similar degree. Birds generalized asymmetrically between life stages, positively from larvae to adults and negatively from adults to larvae. We conclude that the lower conspicuousness in the pale forms of G. lineatum may entail a reduced aposematic function, namely a reduced initial wariness in inexperienced birds. The maintenance of the colour polymorphism is discussed.     

EVOLUTION OF MIMICRY PATTERNS IN METRIORRHYNCHUS (COLEOPTERA: LYCIDAE): THE HISTORY OF DISPERSAL AND SPECIATION IN SOUTHEAST ASIA

The concept of Müllerian mimicry suggests convergent evolution to an intermediate pattern and does not predict polymorphism in mimicry rings. We examined the evolution of mimicry patterns and the order of divergence of various factors, including the role of aposematic patterns in speciation, in a clade of net-winged beetles with a robust phylogeny that suggests that they dispersed from the Australian to Asian plate. We found strong evidence for the evolution of mimicry via advergence in Metriorrhynchus because older patterns are represented in the Oriental region within more than 100 species of lycids from several lineages. Advergence was likely the cause of the observed intraspecific polymorphism in contrast to the predicted universal monomorphism. Polymorphism was found in populations of two species in Sumatra and Borneo and in populations fine-tuned to subtle variants in various habitats. The advergence is likely to be based on the small population sizes of immigrants. The differences in population sizes result in much higher benefits for dispersing species than native populations. Speciation was trigged by the divergence in aposematic coloration, and the genetic differences accumulated slowly during incomplete isolation. We assumed that the differentiation in genitalia through sexual selection ultimately reinforced speciation initiated by the shift between mimicry patterns.