Novelty effects in a multimodal warning signal

The warning signals of toxic insects are often 'multimodal', combining bright coloration with sounds or odours (or both). Pyrazine (a common insect warning odour) can elicit an intrinsic avoidance in domestic chicks Gallus gallus domesticus, both against novel coloured food, and also against food colours that are specifically associated with aposematism, namely yellow and red. In three experiments, we investigated the role of novelty in this innate bias against yellow coloured food in the presence of pyrazine. Naive chicks were familiarized either to pyrazine odour or to coloured food before being tested for a bias against yellow (warningly coloured) food as opposed to green (nonwarningly coloured) food. In experiment 1, pyrazine novelty was shown to be vital for eliciting a bias against yellow food. However, experiment 2 suggested that colour novelty was not important: chicks familiarized with coloured crumbs still avoided yellow crumbs when pyrazine was presented. In a third experiment that gave chicks an even greater degree of pre-exposure to coloured crumbs, the bias against yellow food eventually waned, although pyrazine continued to elicit an aversion to yellow even after birds had had experience of up to 24 palatable yellow crumbs. Pyrazine novelty has been an important pressure in the evolution of multimodal warning signals, and can continue to promote the avoidance of warningly coloured food, even when it is relatively familiar. The implications for warning signals are discussed. Copyright 1999 The Association for the Study of Animal Behaviour.     

Warning signals and predator-prey coevolution

Theories of the evolution of warning signals are typically expressed using analytic and computational models, most of which attribute aspects of predator psychology as the key factors facilitating the evolution of warning signals. Sherratt provides a novel and promising perspective with a model that considers the coevolution of predator and prey populations, showing how predators may develop a bias towards attacking cryptic prey in preference to conspicuous prey. Here, we replicate the model as an individual-based simulation and find, in accordance with Sherratt, that predators evolve a bias towards attacking cryptic prey. We then use a Monte Carlo simulation to calculate the relative survivorships of cryptic and conspicuous prey and stress that, as it stands, the model does not predict the evolution or stability of warning signals. We extend the model by giving predators continuous attack strategies and by allowing the evolution of prey conspicuousness: results are robust to the first modification but, in all cases, cryptic prey always enjoy a higher survivorship than conspicuous prey. When conspicuousness is allowed to evolve, prey quickly evolve towards crypsis, even when runaway coevolution is enabled. Sherratt's approach is promising, but other aspects of predator psychology, besides their innate response, remain vital to our understanding of warning signals.     

The Evolution of Multimodal Warning Displays

Multimodal warning displays combine visual signals with components produced in other sensory modalities, for instance, aposematically coloured insects often produce a pungent odour or harsh sound when they are attacked. Recent research has focussed upon a particular odour, pyrazine, which is commonly associated with warning coloration. Our experiments have shown that pyrazine elicits hidden unlearned biases against particular visual aspects of food in foraging domestic chicks. Here we asses the current state of our knowledge about these biases, reviewing our results using pyrazine and other odours, and also presenting new data showing that sound can produce similar effects. We will discuss potential psychological mechanisms by which these foraging biases are achieved in avian predators, and potential pathways for their evolution. This revised version was published online in July 2006 with corrections to the Cover Date.     

Perspective: the evolution of warning coloration is not paradoxical

Animals that are brightly colored have intrigued scientists since the time of Darwin, because it seems surprising that prey should have evolved to be clearly visible to predators. Often this self-advertisement is explained by the prey being unprofitable in some way, with the conspicuous warning coloration helping to protect the prey because it signals to potential predators that the prey is unprofitable. However, such signals only work in this way once predators have learned to associate the conspicuous color with the unprofitability of the prey. The evolution of warning coloration is still widely considered to be a paradox, because it has traditionally been assumed that the very first brightly colored individuals would be at an immediate selective disadvantage because of their greater conspicuousness to predators that are naive to the meaning of the signal. As a result, it has been difficult to understand how a novel conspicuous color morph could ever avoid extinction for long enough for predators to become educated about the signal. Thus, the traditional view that the evolution of warning coloration is difficult to explain rests entirely on assumptions about the foraging behavior of predators. However, we review recent evidence from a range of studies of predator foraging decisions, which refute these established assumptions. These studies show that: (1) Many predators are so conservative in their food preferences that even very conspicuous novel prey morphs are not necessarily at a selective disadvantage. (2) The survival and spread of novel color morphs can be simulated in field and aviary experiments using real predators (birds) foraging on successive generations of artificial prey populations. This work demonstrates that the foraging preferences of predators can regularly (though not always) result in the increase to fixation of a novel morph appearing in a population of familiar-colored prey. Such fixation events occur even if both novel and familiar prey are fully palatable and despite the novel food being much more conspicuous than the familiar prey. These studies therefore provide strong empirical evidence that conspicuous coloration can evolve readily, and repeatedly, as a result of the conservative foraging decisions of predators.     

Prey selection by wild birds can allow novel and conspicuous colour morphs to spread in prey populations

Conspicuous warning coloration helps to protect prey because it signals to potential predators that the prey is unprofitable. However, such signals only work once predators have come to associate the conspicuous colour with the unprofitability of the prey. The evolution of warning coloration is generally considered to be paradoxical, because it has traditionally been assumed that the first brightly coloured individuals would be at an immediate selective disadvantage because of their greater conspicuousness to predators that are naïve to the meaning of the signal. As a result, it has been difficult to understand how a novel conspicuous colour morph could ever avoid rapid extinction, and instead survive and spread in the population until predators have become educated about the signal. In the present study, we experimentally simulated the appearance of a single novel coloured mutant in small populations (20 individuals) of palatable artificial pastry "prey". The colour morph frequencies in each "generation" of prey (presented on successive days of a trial) were determined by the relative survival of the previous generation under predation by free-living birds. We found that the novel colour morphs regularly persisted and increased from a starting frequency of 1/20 to reach fixation (100%), despite being fully palatable, even when the novel morph was much more conspicuous against the background than the familiar morph. This was true for both green (not normally considered a warning colour) and red (a classic warning colour) novel morphs. Novel colours reached fixation significantly faster than could be accounted for by random drift, indicating differential predation in relation to prey colour by the birds. Our experiments show that the immediate demise of a fully palatable new prey morph is not an inevitable outcome of predator behaviour, because even very conspicuous prey can gain protection from conservative foragers, simply by being novel.     

Better to be bimodal: the interaction of color and odor on learning and memory

Defended prey frequently advertise to potential predators usingmultimodal warning displays. Signaling through more than onesensory pathway may enhance the rate of avoidance learning andthe memorability of these learned avoidances. If this is so,then mimetic insects would gain more protection from mimickinga multimodal rather than a monomodal model. Day-old domesticchicks (Gallus gallus domesticus) were used to examine whethera common insect warning odor (pyrazine) enhanced learning andmemorability of yellow prey, a common warning color. Pyrazineincreased the rate at which the chicks learned to avoid unpalatableyellow prey, and how well this learned avoidance was rememberedafter a 96-h interval. After 96 h, mimics of the multimodalprey were avoided, whereas mimics of the monomodal prey werenot. In the absence of pyrazine, chicks generalized their learnedavoidance of the unpalatable yellow prey to palatable greenprey; however, the presence of pyrazine reduced this color generalization.These results suggest that much is to be gained from signalingmultimodally, for both models and mimetic prey species. Thepresence of multimodal prey in the habitat may also advantagethe predators as it allows it them to distinguish more easilybetween palatable and unpalatable prey.     

Warning signals evolve to disengage Batesian mimics

Prey that are unprofitable to attack are typically conspicuous in appearance. Conventional theory assumes that these warning signals have evolved in response to predator receiver biases. However, such biases might be a symptom rather than a cause of warning signals. We therefore examine an alternative theory: that conspicuousness evolves in unprofitable prey to avoid confusion with profitable prey. One might wonder why unprofitable prey do not find a cryptic means to be distinct from profitable prey, reducing both their risk of confusion with profitable prey and their rate of detection by predators. Here we present the first coevolutionary model to allow for Batesian mimicry and signals with different levels of detectability. We find that unprofitable prey do indeed evolve ways of distinguishing themselves using cryptic signals, particularly when appearance traits can evolve in multiple dimensions. However, conspicuous warning signals readily evolve in unprofitable prey when there are more ways to look different from the background than to match it. Moreover, the more unprofitable the prey species, the higher its evolved conspicuousness. Our results provide strong support for the argument that unprofitable species evolve conspicuous signals to avoid confusion with profitable prey and indicate that peak shift in conspicuousness-linked traits is a major factor in its establishment.     

Conditions for the spread of conspicuous warning signals: a numerical model with novel insights

The initial evolution of conspicuous warning signals presents an evolutionary problem because selection against rare conspicuous signals is presumed to be strong, and new signals are rare when they first arise. Several possible solutions have been offered to solve this apparent evolutionary paradox, but disagreement persists over the plausibility of some of the proposed mechanisms. In this paper, we construct a deterministic numerical simulation model that allows us to derive the strength of selection on novel warning signals in a wide range of biologically relevant situations. We study the effects of predator psychology (learning, rate of mistaken attacks, and neophobia) on selection. We also study the how prey escape, predation intensity, number of predators, and abundance of different prey types affects selection. The model provides several important results. Selection on novel warning signals is number rather than frequency dependent. In most cases, there exists a threshold number of aposematic individuals below which aposematism is selected against and above which aposematism is selected for. Signal conspicuousness (which increases detection rate) and distinctiveness (which allows predator to distinguish defended from nondefended prey) have opposing effects on evolution of warning signals. A more conspicuous warning signal cannot evolve unless it makes the prey more distinctive from palatable prey, reducing mistaken attacks by predators. A novel warning signal that is learned quickly can spread from lower abundance more easily than a signal that is learned more slowly. However, the relative rate at which the resident signal and the novel signal are learned is irrelevant for the spread of the novel signal. Long-lasting neophobia can facilitate the spread of novel warning signals. Individual selection via the ability of defended prey to escape from predator is not likely to facilitate evolution of conspicuous warning signals if both the resident (cryptic) morph and the novel morph have the same escape probability. Predation intensity (defined as the proportion of palatable prey eaten by the predator) has a strong effect on selection. More intense predation results in strong selection against rare signals, but also strong selective advantage to common signals. The threshold number of aposematic individuals is lower when predation is intense. Thus, the evolution of warning signals may be more likely in environments where predation is intense. The effect of numbers of predators depends on whether predation intensity also changes. When predation intensity is constant, increasing numbers of predators raises the threshold number of aposematic individuals, and thus makes evolution of aposematism more difficult. If predation intensity increases in parallel with number of predators, the threshold number of aposematic individuals does not change much, but selection becomes more intense on both sides of the threshold.     

The coevolution of warning signals

It has long been recognized that defended prey tend to be conspicuous. Current theories suggest that the association ('aposematism') has arisen because predators more readily learn to avoid attacking defended phenotypes when they are conspicuous. In this paper, I consider why such psychology has evolved. In particular, I argue that aposematism may have evolved not because of an independent and pre-existing receiver bias, but because the conspicuousness of a prey item provides a reliable indicator of its likelihood of being defended. To develop my case I consider how warning signals might coevolve in a system containing a number of predators, whose foraging behaviour is also subject to selection. In these cases, models readily show that the greater the conspicuousness of a novel prey item, the more likely that it has been encountered by other predators and survived. As a consequence, naive predators should be less likely to attack highly conspicuous novel prey on encounter, or at least more inclined to attack them cautiously. This adaptive predator behaviour will greatly facilitate the spread of aposematic phenotypes from extreme rarity, which in turn will enhance selection for forms of predator behaviour under which aposematism will coevolve even more readily.     

How bright and how nasty: explaining diversity in warning signal strength

The conspicuous displays that warn predators of defenses carried by potential prey have been of interest to evolutionary biologists from the time of Wallace and Darwin to the present day. Although most studies implicitly assume that these "aposematic" warning signals simply indicate the presence of some repellent defense such as a toxin, it has been speculated that the intensity of the signal might reliably indicate the strength of defense so that, for example, the nastiest prey might "shout loudest" about their unprofitability. Recent phylogenetic and empirical studies of Dendrobatid frogs provide contradictory views, in one instance showing a positive correlation between toxin levels and conspicuousness, in another showing a breakdown of this relationship. In this paper we present an optimization model, which can potentially account for these divergent results. Our model locates the optimal values of defensive traits that are influenced by a range of costs and benefits. We show that optimal aposematic conspicuousness can be positively correlated with optimal prey toxicity, especially where population sizes and season lengths vary between species. In other cases, optimal aposematic conspicuousness may be negatively correlated with toxicity; this is especially the case when the marginal costs of aposematic displays vary between members of different populations. Finally, when displays incur no allocation costs there may be no single optimum value for aposematic conspicuousness, rather a large array of alternative forms of a display may have equal fitness.     

Predator experience on cryptic prey affects the survival of conspicuous aposematic prey

Initially, aposematism, which is an unprofitable trait, e.g. noxiousness conspicuously advertised to predators, appears to be a paradox since conspicuousness should increase predation by naive predators. However, reluctance of predators for eating novel prey (e.g. neophobia) might balance the initial predation caused by inexperienced predators. We tested the novelty effects on initial predation and avoidance learning in two separate conspicuousness levels of aposematic prey by using a 'novel world' method. Half of the wild great tits (Parus major) were trained to eat cryptic prey prior to the introduction of an aposematic prey, which potentially creates a bias against the aposematic morph. Both prey types were equally novel for control birds and they should not have shown any biased reluctance for eating an aposematic prey. Knowledge of cryptic prey reduced the expected initial mortality of the conspicuous morph to a random level whereas control birds initially ate the conspicuous morph according to the visibility risk. Birds learned to avoid conspicuous prey in both treatments but knowledge of cryptic prey did not increase the rate of avoidance learning. Predators' knowledge of cryptic prey did not reduce the predation of the less conspicuous aposematic prey and additionally predators did not learn to avoid the less conspicuous prey. These results indicate that predator psychology, which was shown as reluctance for attacking novel conspicuous prey, might have been important in the evolution of aposematism.     

Diversity in warning coloration is easily recognized by avian predators

Warning coloration is a widespread strategy to alert predators about prey unprofitability. The success of this strategy partly depends on predators being able to learn and recognize certain signals as indicators of toxicity, and theory predicts that this is easier if signals converge on similar colours. However, the diversity in warning signal form is astonishing, contradicting predictions. Here, we quantified ladybird signal diversity with respect to avian vision, measuring how unique and discernible each signal is from one another. In addition, we measured signal conspicuousness against a series of backgrounds, namely an average green, average brown, and where we collected each species, to determine whether signals are more contrasting against the ladybirds’ local substrates than compared to average ones. This allowed us to establish whether there are local adaptations in conspicuousness that promote signal diversity. We found that while ladybird signals are unique and recognizable, specialist species are more contrasting against the background they are most commonly found on. However, overall our study suggests that warning signals have evolved to be effective against a wide range of natural backgrounds, partly explaining the success of this strategy in nature.     

Automimicry destabilizes aposematism: predator sample-and-reject behaviour may provide a solution

Aposematism, the use of conspicuous colours to advertise unpalatability to predators, is perhaps the most studied signalling system in nature. However, its evolutionary stability remains paradoxical. The paradox is illustrated by the problem of automimicry. Automimics are palatable individuals within a population of unpalatable aposematics. Automimics benefit from predators avoiding warning coloration without carrying the models' cost of unpalatability, and should increase in the population, destabilizing the signalling system, unless selected against in some way. Cautious sampling, instead of avoidance, by predators may offer a solution to this problem. Here, we investigate the effect of automimic frequency on predator sampling behaviour, and whether predator sampling behaviour may provide a selection pressure against mimics. Domestic chicks (Gallus gallus domesticus) were subjected to the task of discriminating between green (signalling) and untreated brown chick crumbs. Some of the green crumbs were quinine treated and thus unpalatable. The frequency of palatable signalling prey items varied in four treatments; all unpalatable, low automimic frequency, high automimic frequency and all palatable. The results show that predator sampling behaviour is sensitive to automimic frequency and that predators may discriminate between models and mimics through sampling, and thereby benefit unprofitable prey. The results suggest somewhat surprisingly that aposematic signalling is stable only because of the actions of those predators not actually deterred by warning signals.     

Predator mixes and the conspicuousness of aposematic signals

Conspicuous warning signals of unprofitable prey are a defense against visually hunting predators. They work because predators learn to associate unprofitability with bright coloration and because strong signals are detectable and memorable. However, many species that can be considered defended are not very conspicuous; they have weak warning signals. This phenomenon has previously been ignored in models and experiments. In addition, there is significant within- and among-species variation among predators in their search behavior, in their visual, cognitive, and learning abilities, and in their resistance to defenses. In this article we explore the effects of variable predators on models that combine positive frequency-dependent, frequency-independent, and negative frequency-dependent predation and show that weak signaling of aposematic species can evolve if predators vary in their tendency to attack defended prey.     

Non-warning odors trigger innate color aversions--as long as they are novel

Warning signals made by unpalatable insects to potential predatorscommonly target more than one sense: such signals are "multimodal." Pyrazines are odors produced by warningly colored insects whenattacked, and have been shown to interact with food coloration,biasing avian predators against novel and typically aposematicfood. However, at present it is not known whether this is anadaptation by prey to exploit a general feature of avian psychology,or an evolutionary response by birds to enhance their avoidanceof unpalatable prey. Here we investigate the effect of otherodors on the innate responses of naive domestic chicks (Gallusgallus domesticus) to food that is of novel color, or of acolor that is associated with warning coloration, yellow. Inthe first experiment, we demonstrate that natural and artificialodors that have no association with aposematism in the wildcan produce biases against both novel colored foods and yellowcolored foods. In a second experiment, we also show that odor novelty is vital for eliciting such effects. These results supportthe idea that warning odors have evolved in response to preexistingpsychological biases against novel odors in predators, ratherthan predators evolving specific responses against odors associatedwith unpalatable prey.     

Aposematic coloration, luminance contrast, and the benefits of conspicuousness

Many organisms use warning, or aposematic, coloration to signaltheir unprofitability to potential predators. Aposematicallycolored prey are highly visually conspicuous. There is considerableempirical support that conspicuousness promotes the effectivenessof the aposematic signal. From these experiments, it is welldocumented that conspicuous, unprofitable prey are detectedsooner and aversion learned faster by the predator as comparedwith cryptic, unprofitable prey. Predators also retain memoryof the aversion longer when prey is conspicuous. The presentstudy focused on the elements of conspicuousness that conferthese benefits of aposematic coloration. Drawing on currentunderstanding of animal vision, we distinguish 2 features ofwarning coloration: high chromatic contrast and high brightness,or luminance, contrast. Previous investigations on aposematicsignal efficacy have focused mainly on the role of high chromaticcontrast between prey and background, whereas little researchhas investigated the role of high luminance contrast. Usingthe Chinese mantid as a model predator and gray-painted milkweedbugs as model prey, we found that increased prey luminance contrastincreased detection of prey, facilitated predator aversion learning,and increased predator memory retention of the aversive response.Our results suggest that the luminance contrast component ofaposematic coloration can be an effective warning signal betweenthe prey and predator. Thus, warning coloration can even evolveas an effective signal to color blind predators.     

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.     

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.     

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.