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.     

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.     

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.     

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.     

Pyrazine odour makes visually conspicuous prey aversive

Unpalatable insects frequently adopt multimodal signals to ward off predators, incorporating sounds and odours into their colourful displays. Pyrazine is an odour commonly used in insect warning displays, and has previously been shown to elicit unlearned biases against common warning colours, e.g. yellow and red in naive predators. We designed two experiments to test for similar effects of pyrazine on the conspicuousness of prey, perhaps the most ubiquitous aspect of aposematic coloration. In the first experiment, we offered predators (Gallus gallus domesticus) a choice between conspicuous crumbs and cryptic crumbs in the presence or absence of pyrazine. In the second experiment, we manipulated the birds' experience of conspicuous prey during an initial training phase. Only in the presence of pyrazine did birds show a bias against conspicuously coloured food, and this occurred whether or not they had previously experienced food that contrasted with the background. This emergent behaviour relied upon the visual and odorous signal components being presented together. These unlearned, yet hidden, responses against conspicuousness demonstrate that there are initial benefits to prey being conspicuous when the multimodal nature of warning signals is accounted for.     

Batesian mimics influence the evolution of conspicuousness in an aposematic salamander

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

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.     

A role for phenotypic plasticity in the evolution of aposematism

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

Variation in predator species abundance can cause variable selection pressure on warning signaling prey

Predation pressure is expected to drive visual warning signals to evolve toward conspicuousness. However, coloration of defended species varies tremendously and can at certain instances be considered as more camouflaged rather than conspicuous. Recent theoretical studies suggest that the variation in signal conspicuousness can be caused by variation (within or between species) in predators' willingness to attack defended prey or by the broadness of the predators' signal generalization. If some of the predator species are capable of coping with the secondary defenses of their prey, selection can favor reduced prey signal conspicuousness via reduced detectability or recognition. In this study, we combine data collected during three large-scale field experiments to assess whether variation in avian predator species (red kite, black kite, common buzzard, short-toed eagle, and booted eagle) affects the predation pressure on warningly and non-warningly colored artificial snakes. Predation pressure varied among locations and interestingly, if common buzzards were abundant, there were disadvantages to snakes possessing warning signaling. Our results indicate that predator community can have important consequences on the evolution of warning signals. Predators that ignore the warning signal and defense can be the key for the maintenance of variation in warning signal architecture and maintenance of inconspicuous signaling.     

Signal conflict in spider webs driven by predators and prey

Variation in the sensory physiologies of organisms can bias the receptions of signals, driving the direction of signal evolution. Sensory drive in the evolution of signals may be particularly important for organisms that confront trade-offs in signal design between the need for conspicuousness to allow effective transfer of information and the need for crypsis of the signal to unintended receivers. Several genera of orb-weaving spiders include conspicuous silk designs, stabilimenta, in the centre of their webs. Stabilimenta can be highly visible signals to predators, warning them of the presence of a noxious, sticky silk web. However, stabilimenta can also be used by prey as a signal in avoidance of webs, creating a trade-off in signal visibility. I argue that the derived spectral properties of stabilimentum silk have resulted in part from this conflict. The innate colour preferences of insects, their ability to learn colours, and the spectral properties of flowers all suggest that the reflectance spectra of stabilimenta renders them relatively cryptic to many insect prey, while maintaining their visibility to vertebrate predators.     

The effects of predator learning, forgetting, and recognition errors on the evolution of warning coloration

This paper demonstrates that the specifics of predator avoidance learning, information loss, and recognition errors may heavily influence the evolution of aposematism. I establish a mathematical model of the change in frequency over time of bright individuals of a distasteful prey species. Warning color spreads through green beard selection as reformulated by Guilford (1990); bright colored forms gain an advantage due to their phenotypic resemblance to other bright forms, which have been sampled by the predator. I use a general classical conditioning model to examine gradual predator learning and forgetting, and then consider the extreme of one-trial learning and no forgetting over time that may occur with very toxic prey. The advantage of conspicuous coloration under these latter conditions depends upon its role in lowering a constant probability of the prey being misidentified and thus mistakenly attacked by a predator, a rarely emphasized factor in the evolution of warning coloration. This constant probability of mistaken attacks can also be interpreted as a constant probability that forgetting has occurred (forgetting does not increase with time) or a periodic decision by the predator to resample avoided prey. I show that when predators learn and forget gradually, as under the general classical conditioning model, it is very difficult for aposematic coloration to become established unless bright individuals cross an often high threshold frequency through chance factors. In contrast, the conditions expected with highly toxic prey promote the evolution of warning coloration more easily, by means from the fixation of very bright mutations to the fixation of successive mutations each of which causes a small increase in a prey's conspicuousness. The results therefore predict that aposematic coloration may have evolved in a different manner in different predator and prey systems. They also suggest that it may be extremely difficult for warning coloration to evolve in more mildly toxic or distasteful prey outside of a mimicry system.     

State-dependent risk-taking by predators in systems with defended prey

Even defended prey items may contain nutrients that can sustain predators in times of energetic need. Conversely, a well-fed predator might be expected to avoid attacking prey items that have a chance of being defended, particularly if there is an abundance of familiar palatable prey to support it. To further understand the implications of optimal state-dependent foraging behaviour by predators in systems that contain defended prey, I developed a stochastic dynamic programming model. This state-dependent approach formally accounts for the trade-off between avoiding starvation and minimising harm from attacking defended prey. It predicts that the mean attack probability of predators on defended models and their undefended mimics should decline in a sigmoidal fashion with increasing availability of alternative undefended prey, and that the foraging decisions of predators should in general be relatively insensitive to the probability that a potentially defended prey item is indeed defended. Some implications of these predictions are that conspicuous warning signals are more likely to evolve in systems that contain an abundance of alternative undefended prey, and that imperfect mimicry will provide almost complete protection to the mimic when predators are readily supported by alternative food sources. Somewhat surprisingly, increasing the density of nutritious undefended mimics while keeping the densities of all other prey types constant tended to decrease the attack rates of predators on encounter with mimics and their defended models. This increase in dietary conservatism arose because in these cases there would be more prey available to sustain the predator if it ever found itself critically low in energy.     

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.     

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.     

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.     

The evolution of warning signals as reliable indicators of prey defense

It is widely argued that defended prey have tended to evolve conspicuous traits because predators more readily learn to avoid defended prey when they are conspicuous. However, a rival theory proposes that defended prey have evolved such characters because it allows them to be distinguished from undefended prey. Here we investigated how the attributes of defended (unprofitable) and undefended (profitable) computer-generated prey species tended to evolve when they were subject to selection by foraging humans. When cryptic forms of defended and undefended species were similar in appearance but their conspicuous forms were not, defended prey became conspicuous while undefended prey remained cryptic. Indeed, in all of our experiments, defended prey invariably evolved any trait that enabled them to be distinguished from undefended prey, even if such traits were cryptic. When conspicuous mutants of defended prey were extremely rare, they frequently overcame their initial disadvantage by chance. When Batesian mimicry of defended species was possible, defended prey evolved unique traits or characteristics that would make undefended prey vulnerable. Overall, our work supports the contention that warning signals are selected for their reliability as indicators of defense rather than to capitalize on any inherent educational biases of predators.     

Evolutionary consequences of a search image

Many predators are able to become better at spotting cryptic prey by recognising specific clues, but by concentrating on one prey type they will become worse at spotting other prey types. This phenomenon is known as the formation of a search image for a certain prey by a predator and is related to apostatic selection. Here, we study the evolution of a search image in the predator by formulating and analysing a mathematical model. The predator forages for two prey types and is able to form an independent search image for both prey. The results show that the evolutionary dynamics can be divided into two parts: a fast and a slow part. At first selection pressure will be strong towards a stable ratio of prey, which is the same as the ratio found for the unbeatable prey choice for predators with a Holling type II functional response. Following this, the slow dynamics will keep this ratio constant independent of the trait values, but the predator will slowly evolve towards a stronger search image and ultimately become a specialist predator or slowly evolve towards generalist with a weak search image. In conclusion, the formation of a search image causes the predator to control the prey densities such that the ratio of available prey is kept constant by the predator.     

Mixed-phenotype grouping: the interaction between oddity and crypsis

Aggregations of different-looking animals are frequently seen in nature, despite well-documented selection pressures on individuals to maintain phenotypically homogenous groups. Two well-known theories, the ‘confusion effect’ (reduced ability of a predator to accurately target an individual in a group) and the ‘oddity effect’ (preferential targeting of phenotypically distinct, ‘odd’, individuals) act together to predict the evolution of behaviours in prey that lead to groups of animals that are homogeneous in appearance. In contrast, a recently proposed mechanism suggests that mixed groups could be maintained if one species in a mixed group is more conspicuous against the habitat than the other, as confusion effects generated by the conspicuous species impede predator targeting of the cryptic species; thus, cryptic species benefit from association with conspicuous ones. We test these contrasting predictions from the perspective of both predators and prey, and show that cryptic individual Daphnia are at reduced risk of predation from three-spine sticklebacks Gasterosteus aculeatus when in mixed-phenotype groups, a risk that is reduced further as the number of conspicuous individuals increases, supporting the hypothesis for the evolution of mixed groups. In contrast, while the preference for associating with colour-matched conspecifics by mollies (Poecilia sphenops) was reduced when they were cryptic, we found no evidence for active association with conspicuous conspecifics. We conclude that prey animals must balance the relative risks of oddity and conspicuousness in their social decisions, and that this could potentially lead to the evolution of mixed-phenotype grouping as a response to predation risk alone.