Aposematism: what should our starting point be?

The evolution of aposematism is considered to be a major evolutionary problem because if new aposematic forms emerged in defended cryptic populations, they would face the dual problems of rarity and conspicuousness. We argue that this commonly assumed starting point might not have wide validity. We describe a novel evolutionary computer model in which prey evolve secondary defences and become conspicuous by moving widely over a visually heterogeneous habitat. Unless crypsis imposes high opportunity costs (for instance, preventing prey from efficient foraging, thermoregulation and communication), costly secondary defences are not predicted to evolve at all. However, when crypsis imposes opportunity costs, prey evolve secondary defences that facilitate raised behavioural conspicuousness as prey exploit opportunities within their environment. Optimal levels of secondary defence and of behavioural conspicuousness increase with population sizes and the costs imposed by crypsis. When prey are already conspicuous by virtue of their behaviours, the evolution of aposematic appearances (bright coloration, etc.) is much easier to explain because aposematic traits add little further costs of conspicuousness, but can bring large benefits.     

Cryptic female Strawberry poison frogs experience elevated predation risk when associating with an aposematic partner

Population divergence in sexual signals may lead to speciation through prezygotic isolation. Sexual signals can change solely due to variation in the level of natural selection acting against conspicuousness. However, directional mate choice (i.e., favoring conspicuousness) across different environments may lead to gene flow between populations, thereby delaying or even preventing the evolution of reproductive barriers and speciation. In this study, we test whether natural selection through predation upon mate‐choosing females can favor corresponding changes in mate preferences. Our study system, Oophaga pumilio, is an extremely color polymorphic neotropical frog with two distinctive antipredator strategies: aposematism and crypsis. The conspicuous coloration and calling behavior of aposematic males may attract both cryptic and aposematic females, but predation may select against cryptic females choosing aposematic males. We used an experimental approach where domestic fowl were encouraged to find digitized images of cryptic frogs at different distances from aposematic partners. We found that the estimated survival time of a cryptic frog was reduced when associating with an aposematic partner. Hence, predation may act as a direct selective force on female choice, favoring evolution of color assortative mating that, in turn, may strengthen the divergence in coloration that natural selection has generated.     

Loss of conspicuous coloration has co-evolved with decreased body size in populations of poison dart frogs

Larger signal size is known to facilitate the learning process of predators to warning signals. Further, smaller objects are generally harder to detect than large, which suggests that smaller sized prey are less likely to benefit from an aposematic strategy compared to crypsis. However, whether body size changes in concert with shifts between crypsis and aposematism in natural populations, remains largely unexplored. I tested whether body size was larger in visually conspicuous population than in cryptic populations among recently diverged populations of the Strawberry Poison frog, Oophaga pumilio. By analysing spectral reflectance and body size data from individuals from 18 discrete populations I found a larger mean body size in conspicuous populations, which was confirmed by an analysis of a subset of 12 populations accounting for phylogenetic history. This shows that the loss of conspicuous colour likely co-evolved repeatedly with a decrease in body size. Thus, selection on body size may influence evolutionary shifts between aposematism and crypsis and vice versa.     

Evolution of color variation in dragon lizards: quantitative tests of the role of crypsis and local adaptation

Abstract Many animal species display striking color differences with respect to geographic location, sex, and body region. Traditional adaptive explanations for such complex patterns invoke an interaction between selection for conspicuous signals and natural selection for crypsis. Although there is now a substantial body of evidence supporting the role of sexual selection for signaling functions, quantitative studies of crypsis remain comparatively rare. Here, we combine objective measures of coloration with information on predator visual sensitivities to study the role of crypsis in the evolution of color variation in an Australian lizard species complex (Ctenophorus decresii). We apply a model that allows us to quantify crypsis in terms of the visual contrast of the lizards against their natural backgrounds, as perceived by potential avian predators. We then use these quantitative estimates of crypsis to answer the following questions. Are there significant differences in crypsis conspicuousness among populations? Are there significant differences in crypsis conspicuousness between the sexes? Are body regions “exposed” to visual predators more cryptic than “hidden” body regions? Is there evidence for local adaptation with respect to crypsis against different substrates? In general, our results confirmed that there are real differences in crypsis conspicuousness both between populations and between sexes; that exposed body regions were significantly more cryptic than hidden ones, particularly in females; and that females, but not males, are more cryptic against their own local background than against the background of other populations. Body regions that varied most in contrast between the sexes and between populations were also most conspicuous and are emphasized by males during social and sexual signaling. However, results varied with respect to the aspect of coloration studied. Results based on chromatic contrast (“hue’ of color) provided better support for the crypsis hypothesis than did results based on achromatic contrast (“brightness’ of color). Taken together, these results support the view that crypsis plays a substantial role in the evolution of color variation and that color patterns represent a balance between the need for conspicuousness for signaling and the need for crypsis to avoid predation.     

Identifying the ecological conditions that select for intermediate levels of aposematic signalling

Chemically defended species often have conspicuous signals that warn potential predators of these defences. Recent evidence suggests that some such aposematic prey are not as conspicuous as possible, even though increased conspicuousness would bring additional anti-predator benefits. Here we present a simple model to explore the generality of these observations. Our model predicts that optimal fitness will often be achieved at an intermediate level of conspicuousness and not simply by maximising conspicuousness. This comes about because of the ubiquitous trade-off that increased conspicuousness has an ecological cost in increasing the encounter rate with predators, as well as a benefit in terms of enhancing learned aversion by predators of defended prey. However, importantly, we also predict that a small deviation away from maximal crypsis generally causes a decrease in fitness, even if a larger deviation would lead to an intermediate level of conspicuousness that maximises fitness. Hence, further consideration of whether intermediate levels of aposematism are as common in nature as predicted in this model will require consideration of the underlying evolution of appearance, and the plausibility of evolution across the fitness trough, from maximal crypsis to an intermediate level of aposematism.     

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

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

Aposematism and crypsis combined as a result of distance dependence: functional versatility of the colour pattern in the swallowtail butterfly larva

The idea that an aposematic prey combines crypsis at a distance with conspicuousness close up was tested in an experiment using human subjects. We estimated detectability of the aposematic larva of the swallowtail butterfly, Papilio machaon, in two habitats, by presenting, on a touch screen, photographs taken at four different distances and measuring the time elapsed to discovery. The detectability of larvae in these images was compared with images that were manipulated, using existing colours either to increase or decrease conspicuousness. Detection time increased with distance for all colourations. However, at the closest distance, detection time was longer for the larvae manipulated to be more cryptic than for the natural and more conspicuous forms. This indicates that the natural colouration is not maximally cryptic at a short distance. Further, smaller increments in distance were needed to increase detection time for the natural than for the conspicuous larva. This indicates that the natural colouration is not maximally conspicuous at longer distances. Taken together, we present the first empirical support for the idea that some colour patterns may combine warning colouration at a close range with crypsis at a longer range. The implications of this result for the evolution of aposematism are discussed.     

NOT EVERYTHING IS BLACK AND WHITE: COLOR AND BEHAVIORAL VARIATION REVEAL A CONTINUUM BETWEEN CRYPTIC AND APOSEMATIC STRATEGIES IN A POLYMORPHIC POISON FROG

Aposematism and crypsis are often viewed as two extremes of a continuum of visual conspicuousness to predators. Theory predicts that behavioral and coloration conspicuousness should vary in tandem along the conspicuousness spectrum for antipredator strategies to be effective. Here we used visual modeling of contrast and behavioral observations to examine the conspicuousness of four populations of the granular poison frog, Oophaga granulifera, which exhibits almost continuous variation in dorsal color. The patterns of geographic variation in color, visual contrast, and behavior support a gradient of overall conspicuousness along the distribution of O. granulifera. Red and green populations, at the extremes of the color distribution, differ in all elements of color, contrast, and behavior, strongly reflecting aposematic and cryptic strategies. However, there is no smooth cline in any elements of behavior or coloration between the two extremes. Instead populations of intermediate colors attain intermediate conspicuousness by displaying different combinations of aposematic and cryptic traits. We argue that coloration divergence among populations may be linked to the evolution of a gradient of strategies to balance the costs of detection by predators and the benefits of learned aversion.     

Size-dependent colouration balances conspicuous aposematism and camouflage

Colour is an important component of many different defensive strategies, but signal efficacy and detectability will also depend on the size of the coloured structures, and how pattern size interacts with the background. Consequently, size-dependent changes in colouration are common among many different species as juveniles and adults frequently use colour for different purposes in different environmental contexts. A widespread strategy in many species is switching from crypsis to conspicuous aposematic signalling as increasing body size can reduce the efficacy of camouflage, while other antipredator defences may strengthen. Curiously, despite being chemically defended, the gold-striped frog (Lithodytes lineatus, Leptodactylidae) appears to do the opposite, with bright yellow stripes found in smaller individuals, whereas larger frogs exhibit dull brown stripes. Here, we investigated whether size-dependent differences in colour support distinct defensive strategies. We first used visual modelling of potential predators to assess how colour contrast varied among frogs of different sizes. We found that contrast peaked in mid-sized individuals while the largest individuals had the least contrasting patterns. We then used two detection experiments with human participants to evaluate how colour and body size affected overall detectability. These experiments revealed that larger body sizes were easier to detect, but that the colours of smaller frogs were more detectable than those of larger frogs. Taken together our data support the hypothesis that the primary defensive strategy changes from conspicuous aposematism to camouflage with increasing size, implying size-dependent differences in the efficacy of defensive colouration. We discuss our data in relation to theories of size-dependent aposematism and evaluate the evidence for and against a possible size-dependent mimicry complex with sympatric poison frogs (Dendrobatidae).     

Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars

1. Aposematism is a widely used antipredator strategy in which an organism possesses both warning coloration and unprofitable characters. Theoretical evidence suggests that aposematic colour should develop when high opportunity costs imposed by crypsis force an organism to engage in conspicuous behaviours. Hence, it is expected that ontogenetic colour change (OCC) in larval insects should include aposematism when foraging needs compel behavioural modifications that preclude a continued state of crypsis. 2. To test this idea, I first investigated whether OCC in caterpillars of the panic moth Saucrobotys futilalis was indicative of a switch from cryptic to aposematic coloration. I then examined the context of panic moth OCC as it related to foraging patterns and behavioural conspicuousness. 3. Early Saucrobotys instars are a cryptic green, but later instars become progressively more orange and develop black spots. Early instar larvae forage cryptically on the inner parenchyma of silked-together host plant leaves to avoid predation, but are rapidly forced to engage in conspicuous foraging behaviours as they outgrow the resources afforded by their shelters. Both coloration and behaviour reach maximal conspicuousness in final instar larvae. 4. As predicted, OCC encompassed a change from crypsis to aposematism in Saucrobotys. Aposematic function was demonstrated by changes in both antipredator behaviour patterns and effectiveness of predator deterrence in early and late instars. Moreover, increased opportunity costs of crypsis and behavioural conspicuousness coincided with the onset of aposematic coloration. 5. This pattern of OCC suggests that aposematic coloration in Saucrobotys develops as a response to constraints imposed by crypsis. Moreover, my study illustrates the importance of the study of ontogenetic patterns in determining how behaviour, morphology, and predator responses interact to influence the initial evolution of phenomena such as aposematism.     

Experimental Approaches to Studying the Initial Evolution of Conspicuous Aposematic Signalling

Aposematism, where prey species conspicuously advertise their unprofitability to predators, is a widespread defensive strategy. One feature of an aposematic anti-predatory strategy that is especially puzzling is conspicuousness. While conspicuousness aids associative learning in predators, it involves being more visible, which probably increases predation risk. Although aposematism is an old evolutionary question, experimental studies to its evolution have been scarce. Only 11 experiments address the potential benefits of conspicuousness, which have successfully manipulated conspicuousness. This is probably because it is difficult to separate conspicuousness from other characters of aposematic prey, e.g. colour. Furthermore since predators and prey species have coexisted for a long time, and there might be special adaptations other than conspicuous signalling, our experimental results might be confounded with, e.g. predatory biases. In this review, I will examine the problems of studying the costs and benefits of conspicuousness as well as the initial evolution of conspicuousness and the recent progress in the study of aposematism. This revised version was published online in July 2006 with corrections to the Cover Date.     

Conspicuous visual signals do not coevolve with increased body size in marine sea slugs

Many taxa use conspicuous colouration to attract mates, signal chemical defences (aposematism) or for thermoregulation. Conspicuousness is a key feature of aposematic signals, and experimental evidence suggests that predators avoid conspicuous prey more readily when they exhibit larger body size and/or pattern elements. Aposematic prey species may therefore evolve a larger body size due to predatory selection pressures, or alternatively, larger prey species may be more likely to evolve aposematic colouration. Therefore, a positive correlation between conspicuousness and body size should exist. Here, we investigated whether there was a phylogenetic correlation between the conspicuousness of animal patterns and body size using an intriguing, understudied model system to examine questions on the evolution of animal signals, namely nudibranchs (opisthobranch molluscs). We also used new ways to compare animal patterns quantitatively with their background habitat in terms of intensity variance and spatial frequency power spectra. In studies of aposematism, conspicuousness is usually quantified using the spectral contrast of animal colour patches against its background; however, other components of visual signals, such as pattern, luminance and spectral sensitivities of potential observers, are largely ignored. Contrary to our prediction, we found that the conspicuousness of body patterns in over 70 nudibranch species decreased as body size increased, indicating that crypsis was not limited to a smaller body size. Therefore, alternative selective pressures on body size and development of colour patterns, other than those inflicted by visual hunting predators, may act more strongly on the evolution of aposematism in nudibranch molluscs.     

Behavioural elements reflect phenotypic colour divergence in a poison frog

The coexistence of both aposematic and cryptic morphs as different anti-predator strategies within a species seems to be an unusual phenomenon in nature. The strawberry poison frog, Oophaga pumilio, shows an astonishing colour diversity among populations in western Panama. In this study we selected a red and a green colour morph from two Panamanian islands (Isla Solarte and Isla Colón) for behavioural observations and measurements of conspicuousness. We found that red frogs were more visible to both conspecific frogs and potential predators than green frogs. Interestingly the difference in conspicuousness was most pronounced at the substrate that males used as principal calling places. Red males were more active and spent more time foraging than green males, which spent more time hidden. The association between conspicuousness of colouration and behaviour results in a more aposematic and a more cryptic anti-predator strategy. This is the first study which links differences in conspicuousness between animals on their natural backgrounds to differences in foraging as well as anti-predator behaviour and discusses the results in light of previous findings of toxicity analyses and potential costs and benefits of aposematism. To this end, our study adds a novel perspective for explaining extreme colour diversity between populations within an initially aposematic species.     

Can the dietary conservatism of predators compensate for positive frequency dependent selection against rare,conspicuous prey?

The evolution of conspicuous colouration in prey is puzzling because such coloration attracts the attention of predators. Anti-apostatic selection, in which rare prey forms are predated disproportionately often, is a second potential obstacle to the evolution of conspicuous colouration in prey, as bright novel prey forms are likely to be very rare when they first appear in populations. It has recently been postulated that dietary conservatism in predators, an extended feeding avoidance of novel prey, would allow novel conspicuous prey to survive and multiply despite anti-apostatic and conspicuousness effects. We tested this hypothesis for a novel prey type arising in an otherwise cryptic population, providing a direct test of whether anti-apostatic selection or the predators’ wariness to attack the novel prey type is the more important force acting on the novel conspicuous prey. We conducted our experiment in the “Novel World”; an experimental system designed to test predators’ foraging decisions in a large landscape. We found that the conspicuous, novel prey suffered high initial costs of conspicuousness compared with cryptic prey, since most of these prey were attacked during the first “generation”, with no opportunity to “reproduce”. However, a subset of the 17 birds (24%) were following a dietary conservative foraging strategy and they were reluctant to eat the novel prey. Interestingly these birds were not more neophobic or less explorative. Our data demonstrate how difficult it is for the novel conspicuous prey to survive in cryptic populations, but they also highlight the importance of the predator’s foraging strategies in helping to promote the evolution and maintenance of aposematism.     

THE DUAL BENEFITS OF APOSEMATISM: PREDATOR AVOIDANCE AND ENHANCED RESOURCE COLLECTION

Theories of aposematism often focus on the idea that warning displays evolve because they work as effective signals to predators. Here, we argue that aposematism may instead evolve because, by enhancing protection, it enables animals to become more exposed and thereby gain resource‐gathering benefits, for example, through a wider foraging niche. Frequency‐dependent barriers (caused by enhanced conspicuousness relative to other prey and low levels of predator education) are generally assumed to make the evolution of aposematism particularly challenging. Using a deterministic, evolutionary model we show that aposematic display could evolve relatively easily if it enabled prey to move more freely around their environments, or become exposed in some other manner that provides fitness benefits unrelated to predation risk. Furthermore, the model shows that the traits of aposematic conspicuousness and behavior which lead to raised exposure positively affect each other, so that the optimal level of both tends to increase when the traits exist together, compared to when they exist in isolation. We discuss the ecological and evolutionary consequences of aposematism. One conclusion is that aposematism could be a key evolutionary innovation, because by widening habitat use it may promote adaptive radiation as a byproduct of enhanced ecological opportunity.     

Inversely related aposematic traits: reduced conspicuousness evolves with increased toxicity in a polymorphic poison-dart frog

Prevailing theory contends that aposematic coloration evolves in tandem with toxicity so that the evolution of increased toxicity will accompany the evolution of greater conspicuousness. Although variation in aposematic coloration within single species should be selectively constrained, because individuals varying from a predator-recognized warning signal will incur greater risk of predation, several species of poison-dart frogs display remarkable phenotypic variation. This variation may have evolved to match different levels of toxicity, and these species provide excellent opportunities to examine the evolution of aposematic coloration. Here, I test whether increased conspicuousness in the granular poison-dart frog evolved in tandem with increased toxicity. Contrary to classical predictions, toxicity assays, spectral reflectance measurements, and phylogenetic reconstruction reveal that the less conspicuous color morphs are actually significantly more toxic than the brightest, most conspicuous phenotypes and that the more toxic, less-conspicuous form evolved from a less toxic, more conspicuous ancestor. Through gas chromatography--mass spectrometry analysis of toxin profiles, I traced the increase in toxicity in the less-conspicuous populations to an acquisition of specific alkaloids, some of which are proven convulsants. These results challenge the tenet that increased conspicuousness always evolves with increased toxicity and support the idea that once aposematism has been established in a species, phenotypic variation may evolve from brightness and toxicity becoming decoupled.     

Aposematism and crypsis are not enough to explain dorsal polymorphism in the Iberian adder

Aposematic organisms can show phenotypic variability across their distributional ranges. The ecological advantages of this variability have been scarcely studied in vipers. We explored this issue in Vipera seoanei, a species that exhibits five geographically structured dorsal colour phenotypes across Northern Iberia: two zigzag patterned (Classic and Cantabrica), one dorsal-strip patterned (Bilineata), one even grey (Uniform), and one melanistic (Melanistic). We compared predation rates (raptors and mammals) on plasticine models resembling each colour phenotype in three localities. Visual modelling techniques were used to infer detectability (i.e. conspicuousness) of each model type for visually guided predators (i.e. diurnal raptors). We hypothesize that predation rates will be lower for the two zigzag models (aposematism hypothesis) and that models with higher detectability would show higher predation rates (detectability hypothesis). Classic and Bilineata models were the most conspicuous, while Cantabrica and Uniform were the less. Melanistic presented an intermediate conspicuousness. Predation rate was low (3.24% of models) although there was variation in attack frequency among models. Zigzag models were scarcely predated supporting the aposematic role of the zigzag pattern in European vipers to reduce predation (aposematism hypothesis). From the non-zigzag models, high predation occurred on Bilineata and Melanistic models, and low on Uniform models, partially supporting our detectability hypothesis. These results suggest particular evolutionary advantages for non-zigzag phenotypes such as better performance of Melanistic phenotypes in cold environments or better crypsis of Uniform phenotypes. Polymorphism in V. seoanei may respond to a complex number of forces acting differentially across an environmental gradient.     

The interplay between multiple predators and prey colour divergence

Evolutionary divergence in the coloration of toxic prey is expected when geographic variation in predator composition and behavior favours shifts in prey conspicuousness. A fundamental prediction of predator‐driven colour divergence is that the local coloration should experience lower predation risk than novel prey phenotypes. The dorsal coloration of the granular poison frog varies gradually from populations of conspicuous bright red frogs to populations of dull green and relatively cryptic frogs. We conducted experiments with clay models in four populations to examine the geographic patterns of taxon‐specific predation. Birds avoided the local phenotype while lizards consistently selected for decreased conspicuousness and crab predation did not depend on frog coloration. Importantly, birds and lizards favoured low conspicuousness in populations where relatively cryptic green morphs have evolved. This study provides evidence for the interplay among distinct selective pressures, from multiple‐predator taxa, acting on the divergence in protective coloration of prey species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 580–589.     

The effect of metapopulation dynamics on the survival and spread of a novel, conspicuous prey

Animals that deploy chemical defences against predators often signal their unprofitability using bright colouration. This pairing of toxicity and conspicuous patterning is known as aposematism.Explaining the evolution and spread of aposematic traits in previously cryptic species has been the focus of much empirical and theoretical work over the last two decades. Existing research concerning the initial evolution of aposematism does not however properly consider that many aposematic species (such as members of the hymenoptera, the lepidoptera, and amphibia) are highly mobile. We argue in this paper that the evolution of aposematic displays is therefore often best understood within a metapopulation framework; hence in this paper we present the first explicit metapopulation model of the evolution of aposematism. Our most general finding is that migration tends to reduce the probability that an aposematic prey can increase from rarity and spread across a large population. Hence, the best case scenarios for the spread of aposematism required fixation of the aposematic form in one or more isolated sub-habitats prior to some event which subsequently enabled migration. We observed that changes in frequency of new aposematic forms within source habitats are likely to be nonmonotonic. First, aposematic prey tend to decline in frequency as they migrate outwards from the source habitat to neighbouring sink habitats, but subsequently they increase in relative abundance in the source, as the descendents of earlier migrants migrate back from newly converted sub-populations. This pattern of initial loss and subsequent gain between new source and neighbouring sink habitats is then repeated as the aposematic form spreads via a moving cline.