Aposematic Signals Research Articles

Lack of neophobic responses to color in a jumping spider that uses color cues when foraging (Habronattus pyrrithrix).

Chemically defended prey often advertise their toxins with bright and conspicuous colors. To understand why such colors are effective at reducing predation, we need to understand the psychology of key predators. In bird predators, there is evidence that individuals avoid novelty—including prey of novel colors (with which they have had no prior experience). Moreover, the effect of novelty is sometimes strongest for colors that are typically associated with aposematic prey (e.g., red, orange, yellow). Given these findings in the bird literature, color neophobia has been argued to be a driving force in the evolution of aposematism. However, no studies have yet asked whether invertebrate predators respond similarly to novel colors. Here, we tested whether naive lab-raised jumping spiders (Habronattus pyrrithrix) exhibit similar patterns of color neophobia to birds. Using color-manipulated living prey, we first color-exposed spiders to prey of two out of three colors (blue, green, or red), with the third color remaining novel. After this color exposure phase, we gave the spiders tests where they could choose between all three colors (two familiar, one novel). We found that H. pyrrithrix attacked novel and familiar-colored prey at equal rates with no evidence that the degree of neophobia varied by color. Moreover, we found no evidence that either prey novelty nor color (nor their interaction) had an effect on how quickly prey was attacked. We discuss these findings in the context of what is known about color neophobia in other animals and how this contributes to our understanding of aposematic signals.

Aposematic signaling and seasonal variation in dorsal pelage in a venomous mammal.

In mammals, colouration patterns are often related to concealment, intraspecific communication, including aposematic signals, and physiological adaptations. Slow lorises (Nycticebus spp.) are arboreal primates native to Southeast Asia that display stark colour contrast, are highly territorial, regularly enter torpor, and are notably one of only seven mammal taxa that possess venom. All slow loris species display a contrasting stripe that runs cranial‐caudally along the median sagittal plane of the dorsum. We examine whether these dorsal markings facilitate background matching, seasonal adaptations, and intraspecific signaling. We analyzed 195 images of the dorsal region of 60 Javan slow loris individuals (Nycticebus javanicus) from Java, Indonesia. We extracted greyscale RGB values from dorsal pelage using ImageJ software and calculated contrast ratios between dorsal stripe and adjacent pelage in eight regions. We assessed through generalized linear mixed models if the contrast ratio varied with sex, age, and seasonality. We also examined whether higher contrast was related to more aggressive behavior or increased terrestrial movement. We found that the dorsal stripe of N. javanicus changed seasonally, being longer and more contrasting in the wet season, during which time lorises significantly increased their ground use. Stripes were most contrasting in younger individuals of dispersal age that were also the most aggressive during capture. The dorsal stripe became less contrasting as a loris aged. A longer stripe when ground use is more frequent can be related to disruptive colouration. A darker anterior region by younger lorises with less fighting experience may allow them to appear larger and fiercer. We provide evidence that the dorsum of a cryptic species can have multimodal signals related to concealment, intraspecific communication, and physiological adaptations.

Appearance matters: multiple functional signals of body colours in a weevil

Visual signals in animals are often shaped by sexual selection. For aposematic species, advantages may result from advertising unpalatability to decrease predation and attracting mates to increase reproductive success. On Green Island, Taiwan, most Eupyrgops waltonianus weevils have metallic blue spots on the body; however, some weevils have no conspicuous coloration. The role of coloration in sexual selection and any disadvantages encountered by dull individuals are unknown. To understand whether morphological traits affect mating success in E. waltonianus , we compared different traits between mating and nonmating individuals in the field. A manipulation experiment was also used to test whether coloration affects mating choice and behaviour. The function of colour as an aposematic signal was tested. Results showed that body size and coloration were important indicators of female mating success in field and laboratory experiments, respectively. In the field, males preferred to mate with larger, more conspicuous females, and females preferred to mate with conspicuous males; however, no such preference was shown in the laboratory. Intrasexual competition was stronger in males than in females. Predators avoided colourful weevils. Thus, conspicuous coloration in both sexes is a multifunctional trait and could be an attractive or aposematic signal for different receivers. • The spots on weevils play an important role in survival and reproduction. • Higher spot area ratio was related to a higher mating probability in the field. • Weevils displayed higher levels of male-male than female-female competition. • Weevils' coloration could be attractive or aposematic depending on receiver type.

Negative intersexual genetic correlation for colour pattern in a variable aposematic insect

Abstract Despite the fact their coloration functions as an aposematic signal, and is thus expected to be under stabilizing selection, hibiscus harlequin bugs (Tectocoris diophthalmus) show an impressive level of variation in their iridescent coloration both within and between populations. To date the heritability of coloration in this species remains unknown. Here we focus on a single population in New South Wales (the southern part of this species’ Australian range), with the greatest colour variation. We reared full-sib families of known pedigree in the laboratory and analysed the extent of iridescent coloration at adulthood. We then looked for evidence of heritability, condition dependence and antagonistic sexual selection acting on colour in this species. We found significant heritability in the extent of iridescent coloration for both sexes, as well as in development time and body size, but no evidence that condition dependence played a role in the determination of adult coloration. There was, however, a sex by genotype interaction for iridescent cover, in the form of a negative intersexual genetic correlation: in families where sons had high iridescent cover the daughters had low, and vice versa. Our results suggest that different selective pressures may act on coloration in males and females of this species.

Meta-analytic evidence for quantitative honesty in aposematic signals.

The combined use of noxious chemical defences and conspicuous warning colours is a ubiquitous anti-predator strategy. That such signals advertise the presence of defences is inherent to their function, but their predicted potential for quantitative honesty-the positive scaling of signal salience with the strength of protection-is the subject of enduring debate. Here, we systematically synthesized the available evidence to test this prediction using meta-analysis. We found evidence for a positive correlation between warning colour expression and the extent of chemical defences across taxa. Notably, this relationship held at all scales; among individuals, populations and species, though substantial between-study heterogeneity remains unexplained. Consideration of the design of signals revealed that all visual features, from colour to contrast, were equally informative of the extent of prey defence. Our results affirm a central prediction of honesty-based models of signal function and narrow the scope of possible mechanisms shaping the evolution of aposematism. They suggest diverse pathways to the encoding and exchange of information, while highlighting the need for deeper knowledge of the ecology of chemical defences to enrich our understanding of this widespread anti-predator adaptation.

Conspicuousness, phylogenetic structure, and origins of M\xfcllerian mimicry in 4000 lycid beetles from all zoogeographic regions

Biologists have reported on the chemical defences and the phenetic similarity of net-winged beetles (Coleoptera: Lycidae) and their co-mimics. Nevertheless, our knowledge has remained fragmental, and the evolution of mimetic patterns has not been studied in the phylogenetic context. We illustrate the general appearance of ~ 600 lycid species and ~ 200 co-mimics and their distribution. Further, we assemble the phylogeny using the transcriptomic backbone and ~ 570 species. Using phylogenetic information, we closely scrutinise the relationships among aposematically coloured species, the worldwide diversity, and the distribution of aposematic patterns. The emitted visual signals differ in conspicuousness. The uniform coloured dorsum is ancestral and was followed by the evolution of bicoloured forms. The mottled patterns, i.e. fasciate, striate, punctate, and reticulate, originated later in the course of evolution. The highest number of sympatrically occurring patterns was recovered in New Guinea and the Andean mountain ecosystems (the areas of the highest abundance), and in continental South East Asia (an area of moderate abundance but high in phylogenetic diversity). Consequently, a large number of co-existing aposematic patterns in a single region and/or locality is the rule, in contrast with the theoretical prediction, and predators do not face a simple model-like choice but cope with complex mimetic communities. Lycids display an ancestral aposematic signal even though they sympatrically occur with differently coloured unprofitable relatives. We show that the highly conspicuous patterns evolve within communities predominantly formed by less conspicuous Müllerian mimics and, and often only a single species displays a novel pattern. Our work is a forerunner to the detailed research into the aposematic signalling of net-winged beetles.

Examining the molecular basis of coat color in a nocturnal primate family (Lorisidae).

Organisms use color for camouflage, sexual signaling, or as a warning sign of danger. Primates are one of the most vibrantly colored Orders of mammals. However, the genetics underlying their coat color are poorly known, limiting our ability to study molecular aspects of its evolution. The role of the melanocortin 1 receptor (MC1R) in color evolution has been implicated in studies on rocket pocket mice (Chaetodipus intermediusi), toucans (Ramphastidae), and many domesticated animals. From these studies, we know that changes in MC1R result in a yellow/red or a brown/black morphology. Here, we investigate the evolution of MC1R in Lorisidae, a monophyletic nocturnal primate family, with some genera displaying high contrast variation in color patterns and other genera being monochromatic. Even more unique, the Lorisidae family has the only venomous primate: the slow loris (Nycticebus). Research has suggested that the contrasting coat patterns of slow lorises are aposematic signals for their venom. If so, we predict the MC1R in slow lorises will be under positive selection. In our study, we found that Lorisidae MC1R is under purifying selection (ω = 0.0912). In Lorisidae MC1R, there were a total of 75 variable nucleotides, 18 of which were nonsynonymous. Six of these nonsynonymous substitutions were found on the Perodicticus branch, which our reconstructions found to be the only member of Lorisidae that has predominantly lighter coat color; no substitutions were associated with Nycticebus. Our findings generate new insight into the genetics of pelage color and evolution among a unique group of nocturnal mammals and suggest putative underpinnings of monochromatic color evolution in the Perodicticus lineage.

Fireflies produce ultrasonic clicks during flight as a potential aposematic anti-bat signal

SummaryFireflies are known for emitting light signals for intraspecific communication. However, in doing so, they reveal themselves to many potential nocturnal predators from a large distance. Therefore, many fireflies evolved unpalatable compounds and probably use their light signals as anti-predator aposematic signals. Fireflies are occasionally attacked by predators despite their warning flashes. Bats are among the most substantial potential firefly predators. Using their echolocation, bats might detect a firefly from a short distance and attack it in between two flashes. We thus aimed to examine whether fireflies use additional measures of warning, specifically focusing on sound signals. We recorded four species from different genera of fireflies in Vietnam and Israel and found that all of them generated ultrasonic clicks centered around bats' hearing range. Clicks were synchronized with the wingbeat and are probably produced by the wings. We hypothesize that ultrasonic clicks can serve as part of a multimodal aposematic display.

Field evidence for colour mimicry overshadowing morphological mimicry.

Imperfect mimicry may be maintained when the various components of an aposematic signal have different salience for predators. Experimental laboratory studies provide robust evidence for this phenomenon. Yet, evidence from natural settings remains scarce.We studied how natural bird predators assess multiple features in a multicomponent aposematic signal in the Neotropical ‘clear wing complex’ mimicry ring, dominated by glasswing butterflies.We evaluated two components of the aposematic signal, wing colouration and wing morphology, in a predation experiment based on artificial replicas of glasswing butterflies (model) and Polythoridae damselflies (mimics) in their natural habitat. We also studied the extent of the colour aposematic signal in the local insect community. Finally, we inspected the nanostructures responsible for this convergent colour signal, expected to highly differ between these phylogenetically distinct species.Our results provide direct evidence for a stronger salience of wing colouration than wing morphology, as well as stronger selection on imperfect than in perfect colour mimics. Additionally, investigations of how birds perceive wing colouration of the local insect community provides further evidence that a UV‐reflective white colouration is being selected as the colour aposematic signal of the mimicry ring. Using electron microscopy, we also suggest that damselflies have convergently evolved the warning colouration through a pre‐adaptation.These findings provide a solid complement to previous experimental evidence suggesting a key influence of the cognitive assessment of predators driving the evolution of aposematic signals and mimicry rings.

Ultraviolet components offer minimal contrast enhancement to an aposematic signal.

Aposematic and sexual signals are often characterized by bright, highly contrasting colors. Many species can see colors beyond the human visible spectrum, and ultraviolet (UV) reflection has been found to play an important role in communication and sexual selection. However, the role of UV in aposematic signals is poorly explored. Poison frogs frequently produce high‐contrast signals that have been linked to both aposematism and intraspecific communication. Yet despite considerable efforts studying interspecific and intraspecific diversity in color, poison frogs are not known to perceive UV, and UV reflection of the integument has not been described. We report UV‐reflective spots in a population of Oophaga sylvatica and quantify the effect of UV on visual contrast with models of avian vision. We found that the frogs are highly contrasting, but UV had a minimal effect on signal saliency. These data highlight the importance of considering UV reflectance within aposematic signals, but that UV should not necessarily be regarded as an independent signal.

Prey with hidden colour defences benefit from their similarity to aposematic signals.

Some camouflaged animals hide colour signals and display them only transiently. These hidden colour signals are often conspicuous and are used as a secondary defence to warn or startle predators (deimatic displays) and/or to confuse them (flash displays). The hidden signals used in these displays frequently resemble typical aposematic signals, so it is possible that prey with hidden signals have evolved to employ colour patterns of a form that predators have previously learned to associate with unprofitability. Here, we tested this hypothesis by conducting two experiments that examined the effect of predator avoidance learning on the efficacy of deimatic and flash displays. We found that the survival benefits of both deimatic and flash displays were substantially higher against predators that had previously learned to associate the hidden colours with unprofitability than against naive predators. These findings help explain the phenological patterns we found in 1568 macro-lepidopteran species on three continents: species with hidden signals tend to occur later in the season than species without hidden signals.

Wolf Howling and Emergency Sirens: A Hypothesis of Natural and Technical Convergence of Aposematic Signals.

Acoustic signals serving intraspecific communication by predators are perceived by potential prey as warning signals. We analysed the acoustic characteristics of howling of wolves and found a striking similarity to the warning sounds of technical sirens. We hypothesize that the effectivity of sirens as warning signals has been enhanced by natural sensory predisposition of humans to get alerted by howling of wolves, with which they have a long history of coexistence. Psychoacoustic similarity of both stimuli seems to be supported by the fact that wolves and dogs perceive the sound of technical sirens as a relevant releasing supernormal stimulus and reply to it with howling. Inspiration by naturally occurring acoustic aposematic signals might become an interesting example of biomimetics in designing new warning sound systems.

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

AbstractBioluminescence 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.

Interactions in multi-pattern M\xfcllerian communities support origins of new patterns, false structures, imperfect resemblance and mimetic sexual dimorphism

Mimicry is a hot spot of evolutionary research, but de novo origins of aposematic patterns, the persistence of multiple patterns in Müllerian communities, and the persistence of imperfect mimics still need to be investigated. Local mimetic assemblages can contain up to a hundred of species, their structure can be a result of multiple dispersal events, and the gradual build-up of the communities. Here, we investigate the structure of lowland and mountain mimetic communities of net-winged beetles by sampling the Crocker Range in north-eastern Borneo and neighbouring regions. The local endemics evolved from the Bornean lowland fauna which is highly endemic at the species level. We inferred that metriorrhynchine net-winged beetles evolved in high elevations yellow/black and reticulate aposematic high-contrast signals from a widespread low-contrast brown/black pattern. As the mountain range is ~ 6 million years old, and these patterns do not occur elsewhere, we assume their in situ origins. We demonstrate that a signal with increased internal contrast can evolve de novo in a mimetic community and can persist despite its low frequency. Additionally, a similar aposematic signal evolves from different structures and its similarity is imperfect. The community with multiple patterns sets conditions for the evolution of aposematic sexual dimorphism as demonstrated by the yellow/black male and reticulate female pattern of Micronychus pardus. These insights elucidate the complex character of the evolution of mimetic signalling in the dynamically diversifying biota of high tropical mountains.

Pattern contrast influences wariness in na\xefve predators towards aposematic patterns

An apparent and common feature of aposematic patterns is that they contain a high level of achromatic (luminance) contrast, for example, many warning signals combine black spots and stripes with a lighter colour such as yellow. However, the potential importance of achromatic contrast, as distinct from colour contrast, in reducing predation has been largely overlooked. Here, using domestic chicks as a model predator, we manipulated the degree of achromatic contrast in warning patterns to test if high luminance contrast in aposematic signals is important for deterring naïve predators. We found that the chicks were less likely to approach and eat prey with high contrast compared to low contrast patterns. These findings suggest that aposematic prey patterns with a high luminance contrast can benefit from increased survival through eliciting unlearned biases in naïve avian predators. Our work also highlights the importance of considering luminance contrast in future work investigating why aposematic patterns take the particular forms that they do.

A ketocarotenoid-based colour polymorphism in the Sira poison frog Ranitomeya sirensis indicates novel gene interactions underlying aposematic signal variation.

The accumulation of red ketocarotenoids is an important component of coloration in many organisms, but the underlying mechanisms are poorly understood. In some organisms, ketocarotenoids are sequestered from the diet and can accumulate when enzymes responsible for carotenoid breakdown are disrupted. In other organisms, ketocarotenoids are formed endogenously from dietary precursors via oxidation reactions carried out by carotenoid ketolase enzymes. Here, we study the genetic basis of carotenoid coloration in an amphibian. We demonstrate that a red/yellow polymorphism in the dendrobatid poison frog Ranitomeya sirensis is due to the presence/absence of ketocarotenoids. Using whole-transcriptome sequencing of skins and livers, we found that a transcript encoding a cytochrome P450 enzyme (CYP3A80) is expressed 3.4-fold higher in livers of red frogs versus yellow. As CYP3A enzymes are known carotenoid ketolases in other organisms, our results point to CYP3A80 as a strong candidate for a carotenoid ketolase in amphibians. Furthermore, in red frogs, the transcript encoding the carotenoid cleavage enzyme BCO2 is expressed at a low level or as a splice variant lacking key catalytic amino acids. This suggests that BCO2 function may be disrupted in red frogs, providing a mechanism whereby the accumulation of ketocarotenoids and their dietary precursors may be enhanced.

Snake coloration does not influence children’s detection time

ABSTRACT Although snakes play key roles in the functioning of various ecosystems, they have been among the most persecuted groups of animals. To enhance conservation efforts, we employed research on perceptions about snakes differing in body coloration. We investigated the bright coloration hypothesis, which suggests that bright (aposematic) coloration triggers fear in humans due to an evolved aversion for aposematic signals. The sample was 77 Slovak preschool children. The detection times for aposematically and cryptically colored snakes were similar. The only exception was that aposematically colored snakes were detected quicker among cryptic non-snake animals than among aposematic non-snake animals. These results provide mixed support for the bright coloration hypothesis. This suggests that snakes, unlike non-snake animals, capture visual attention irrespective of their color, which can be utilized in selection of flagship species to increase conservation efforts.

Evolution of switchable aposematism: insights from individual-based simulations

Some defended prey animals can switch on their normally hidden aposematic signals. This switching may occur in reaction to predators’ approach (pre-attack signals) or attack (post-attack signals). Switchable aposematism has been relatively poorly studied, but we can expect that it might bring a variety of benefits to an aposmetic organism. First, the switching could startle the predators (deimatism). Second, it could facilitate aversive learning. Third, it could minimize exposure or energetic expense, as the signal can be switched off. These potential benefits might offset costs of developing, maintaining and utilizing the switchable traits. Here we focused on the third benefit of switchability, the cost-saving aspect, and developed an individual-based computer simulation of predators and prey. In 88,128 model runs, we observed evolution of permanent, pre-attack, or post-attack aposematic signals of varying strength. We found that, in general, the pre-attack switchable aposematism may require moderate predator learning speed, high basal detectability, and moderate to high signal cost. On the other hand, the post-attack signals may arise under slow predator learning, low basal detectability and high signal cost. When predator population turnover is fast, it may lead to evolution of post-attack aposematic signals that are not conforming to the above tendency. We also suggest that a high switching cost may exert different selection pressure on the pre-attack than the post-attack switchable strategies. To our knowledge, these are the first theoretical attempts to systematically explore the evolution of switchable aposematism relative to permanent aposematism in defended prey. Our simulation model is capable of addressing additional questions beyond the scope of this article, and we open the simulation software, program manual and source code for free public use.

Spontaneous color preferences in rhesus monkeys: What is the advantage of primate trichromacy?

Color perception and color signaling play an important role in various aspects of animal behavior. However, in mammals, trichromatic vision characterized by three retinal photopigments tuned to peak short, middle and long wavelengths is limited only to some primate species. In Old and New World primates a second photopigment has appeared repeatedly during phylogeny, allowing red colors to be distinguished from yellows and greens.Several hypotheses aspire to explain the adaptive benefits of trichromatic vision for primates. The predominant one is foraging adaptation for facilitation visual detection of fruits or young leaves. Alternative explanations are based on the function of red color in aposematic signaling or its role in socio-sexual communication.We tested spontaneous color preference in macaque monkeys (Macaca mulatta) for both food and non-food objects in a laboratory environment. We hypothesized that preference for or avoidance of red color together with the context of such behavior may help us to understand what the adaptive advantage leading to a rapid expansion of a gene for a second pigment in the long-wavelength region was.We found neither preference nor avoidance toward red color in non-food objects, but we found a significant preference for red color in food; therefore, we suggest that the results support the foraging hypothesis in macaque monkeys.

A Quantitative Analysis of Micrurus Coral Snakes Reveals Unexpected Variation in Stereotyped Anti-Predator Displays Within a Mimicry System.

SynopsisWarning signals in chemically defended organisms are critical components of predator–prey interactions, often requiring multiple coordinated display components for effective communication. When threatened by a predator, venomous coral snakes (genus Micrurus) display a vigorous, non-locomotory thrashing behavior that has previously been qualitatively described. Given the high contrast and colorful banding patterns of these snakes, this thrashing display is hypothesized to be a key component of a complex aposematic signal under strong stabilizing selection across species in a mimicry system. By experimentally testing snake response across simulated predator cues, we analyzed variation in the presence and expression of a thrashing display across five species of South American coral snakes. Although the major features of the thrash display were conserved across species, we found that predator cue type, snake body size, and species identity predict significant inter- and intraspecific variation in the propensity to perform a display, the duration of thrashing, and the curvature of snake bodies. We also found an interaction between curve magnitude and body location that clearly shows which parts of the display vary most across individuals and species. Our results suggest that contrary to the assumption that all Micrurus species and individuals perform the same display, a high degree of variation exists despite presumably strong selection to conserve a common signal. This quantitative behavioral characterization presents a new framework for analyzing the non-locomotory motions displayed by snakes in a broader ecological context, especially for signaling systems with complex interaction across multiple modalities.