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.     

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.     

Foraging Benefits in a Colour Polymorphic Neotropical Orb Web Spider

Conspicuous body colouration in sedentary predators such as orb web spiders seems paradoxical as potential prey can see and avoid the webs. Several studies have demonstrated that rather than deterring prey, the colours act as sensory traps for flower‐seeking insects. In chromatically polymorphic species, the existence of more than one colour morph may lead to differing levels of prey attraction. To explore these issues, we studied a neotropical orb web spider, Verrucosa arenata, which shows colour polymorphism with predominantly white or yellow abdomen colours. We asked whether a particular morph is dominant in the population, and whether a particular morph is associated with enhanced foraging success and body condition. Here we showed that although yellow morphs attracted more prey, white morphs were in better body condition. We showed that model prey such as honeybees are able to discriminate between the morphs. We discuss these findings in relation to the functional significance of bright body colouration and colour polymorphism in spiders.     

Does colour polymorphism enhance survival of prey populations?

That colour polymorphism may protect prey populations from predation is an old but rarely tested hypothesis. We examine whether colour polymorphic populations of prey exposed to avian predators in an ecologically valid visual context were exposed to increased extinction risk compared with monomorphic populations. We made 2976 artificial pastry prey, resembling Lepidoptera larvae, in four different colours and presented them in 124 monomorphic and 124 tetramorphic populations on tree trunks and branches such that they would be exposed to predation by free-living birds, and monitored their ‘survival’. Among monomorphic populations, there was a significant effect of prey coloration on survival, confirming that coloration influenced susceptibility to visually oriented predators. Survival of polymorphic populations was inferior to that of monomorphic green populations, but did not differ significantly from monomorphic brown, yellow or red populations. Differences in survival within polymorphic populations paralleled those seen among monomorphic populations; the red morph most frequently went extinct first and the green morph most frequently survived the longest. Our findings do not support the traditional protective polymorphism hypothesis and are in conflict with those of earlier studies. As a possible explanation to our findings, we offer a competing ‘giveaway cue’ hypothesis: that polymorphic populations may include one morph that attracts the attention of predators and that polymorphic populations therefore may suffer increased predation compared with some monomorphic populations.     

Individual selection, kin selection, and the shifting balance in the evolution of warning colours: the evidence from butterflies

It is difficult to imagine how warning colours evolve in unpalatable prey. Firstly, novel warningly coloured variants gain no protection from their colours, since predators have not previously encountered and learnt their colour patterns. This leads to a frequency-dependent disadvantage of a rare variant within a species. Secondly, novel warningly coloured variants may be more conspicuous than non-aposematic prey.
Nevertheless, it is obvious that many palatable butterflies have bright colours used in intraspecific communication and in duping predators. Other palatable butterflies are already warningly coloured. Should such butterflies evolve unpalatability, perhaps because of a host-plant shift, these bright colours would be preadapted to a warning role. Warning colours could then continue to evolve by enhancement of memorable characteristics of these patterns, or by mimicry.
Even within lineages of warningly coloured, unpalatable butterflies, colour patterns have continued to evolve rapidly. This diversity of warning colour patterns could have evolved in a number of ways, including individual and kin selection, and by the shifting balance. Evidence for these mechanisms is discussed, as are the similarities between the evolution of warning colours and more general evolutionary processes, including sexual selection and speciation.     

Contrast versus colour in aposematic signals

Conspicuousness is an important feature of warning coloration. One hypothesis for its function is that it increases signal efficacy by facilitating avoidance learning. An alternative, based on the handicap hypothesis, suggests that the degree of conspicuousness holds information directly about the quality of the prey, and that predators associate and learn about the conspicuousness of the coloration, and not the actual colour pattern. We studied the relative importance of signal contrast and the colours of signals for predator attention during discrimination. We used young chicks, Gallus gallus domesticus, as predators and small blue or red paper cones on either matching or contrasting paper backgrounds as stimuli associated with palatable or unpalatable chick crumbs. In four treatment groups, birds could use either cone and/or background colour, cone colour only, background colour only or cone-to-background contrast as cues for discrimination. Only birds in the contrast treatment failed to learn their discrimination task. Birds that had a choice between cone and background colour as cues used the cone colour and they learned the task faster than did birds that had to use background colour as a cue. The results suggest that birds primarily attend to the colours of signals and disregard contrast in discrimination tasks; they thus fail to support a handicap function of conspicuous aposematic coloration. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

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.     

Body size influences differently the detectabilities of colour morphs of cryptic prey

Body size and coloration may contribute to variation in performance and fitness among individuals; for example, by influencing vulnerability to predators. Yet, the combined effect of size and colour pattern on susceptibility to visual predators has received little attention, particularly in camouflaged prey. In the colour polymorphic pygmy grasshopper Tetrix subulata (Linnaeus, 1758), females are larger than males, although there is a size overlap between sexes. In the present study, we investigated how body size and colour morph influenced detection of these grasshoppers, and whether differences in protective value among morphs change with size. We conducted a computer‐based experiment and compared how human ‘predators’ detected images of large, intermediate or small grasshoppers belonging to black, grey or striped colour morphs when embedded in photographs of natural grasshopper habitats. We found that time to detection increased with decreasing size, that differences in time to detection of the black, grey and striped morphs depended differently on body size, and that no single morph provided superior or inferior protection in all three size classes. By comparing morph frequencies in samples of male and female grasshoppers from natural populations, we also examined whether the joint effects of size and colour morph on detection could explain evolutionary dynamics in the wild. Morph frequency differences between sexes were largely in accordance with expectations from the results of the detection experiment. The results of the present study demonstrate that body size and colour morph can interactively influence detection of camouflaged prey. This may contribute to the morph frequency differences between male and female pygmy grasshoppers in the wild. Such interactive effects may also influence the dynamics of colour polymorphisms, and contribute to the evolution of ontogenetic colour change and sexual dichromatism. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 112–122.     

Cryptic differences in colour among Müllerian mimics: how can the visual capacities of predators and prey shape the evolution of wing colours?

Antagonistic interactions between predators and prey often lead to co‐evolution. In the case of toxic prey, aposematic colours act as warning signals for predators and play a protective role. Evolutionary convergence in colour patterns among toxic prey evolves due to positive density‐dependent selection and the benefits of mutual resemblance in spreading the mortality cost of educating predators over a larger prey assemblage. Comimetic species evolve highly similar colour patterns, but such convergence may interfere with intraspecific signalling and recognition in the prey community, especially for species involved in polymorphic mimicry. Using spectrophotometry measures, we investigated the variation in wing coloration among comimetic butterflies from distantly related lineages. We focused on seven morphs of the polymorphic species Heliconius numata and the seven corresponding comimetic species from the genus Melinaea. Significant differences in the yellow, orange and black patches of the wing were detected between genera. Perceptions of these cryptic differences by bird and butterfly observers were then estimated using models of animal vision based on physiological data. Our results showed that the most strikingly perceived differences were obtained for the contrast of yellow against a black background. The capacity to discriminate between comimetic genera based on this colour contrast was also evaluated to be higher for butterflies than for birds, suggesting that this variation in colour, likely undetectable to birds, might be used by butterflies for distinguishing mating partners without losing the benefits of mimicry. The evolution of wing colour in mimetic butterflies might thus be shaped by the opposite selective pressures exerted by predation and species recognition.     

Brown tawny owls moult more flight feathers than grey ones

The mechanisms by which melanin‐based colour polymorphism can evolve and be maintained in wild populations are poorly known. Theory predicts that colour morphs have differential sensitivity to environmental conditions. Recently it has been proposed that colour polymorphism covaries genetically with intrinsic and behavioural properties. Plumage moult is a costly and crucial somatic maintenance function in birds. We used a long‐term data set consisting of 761 observations on 307 individuals captured between 1985 and 2010 to examine differences in partial flight feather moult between grey (pale) and brown (pheomelanic dark) colour morphs of the tawny owl. We find that the brown morph consistently moult more primary flight feathers than the grey morph whereas there is no clear difference between colour morphs in the moulting of secondary feathers. Contrary to expectations, the difference in the number of moulted flight feathers between the morphs was independent of environmental conditions, as quantified by the abundance of prey. We discuss the potential physiological and behavioural causes for and costs of the observed difference in maintenance functions between colour morphs.     

Further evidence for apostatic selection by wild passerine birds -9 :1 experiments.

Apostatic selection occurs when predators concentrate disproportionately on the common varieties of non-mimetic polymorphic prey species. This has been tested in 14 experiments by presenting populations of green and brown lard-and-flour "baits" to inexperienced wild passerine birds in their normal surroundings. In seven experiments a 9 green : 1 brown population was presented for a number of days, followed by a 1 green : 9 brown population for a similar period. in the remaining seven experiments the populations were presented in the reverse order. The birds often had strong "natural" colour preferences (for example, blackbirds and songthrushes preferred browns) which were not caused by the relative conspicuousness of the two colours. The data within most of the experiments were very heterogeneous, but in every experiment there was good evidence that the birds tended to concentrate on the common colour. The consistency of the replicated experiements gives strong reason to believe that apostatic selection is a widespread phenomenon among avian predators, and provides an explanation for many of the non-mimetic colour and pattern polymorphisms found among their prey.     

Both novelty and conspicuousness influence selection by mammalian predators on the colour pattern of Plethodon cinereus (Urodela: Plethodontidae)

Predators influence the evolution of colour pattern in prey species, yet how these selective forces might differ among predators is rarely considered. In particular, prey colour patterns that indicate unpalatability to some predator species may not carry the same signal for other predators. We test several hypotheses of selection on patterning between mammal predators and the polymorphic salamander Plethodon cinereus, which, under an avian visual system appears as a mimic of the toxic newt Notophthalmus viridescens. We fit each hypothesis against field observations of mammalian attacks on salamander clay replicas. We then develop a novel analytical procedure that enables the combination of multiple non‐exclusive models in a likelihood framework. We find that mammals do not follow any single hypothesis proposed, including the hypothesis of mimicry. Instead, mammals in this system use visual cues while foraging to avoid unfamiliar, novel prey and attack conspicuous prey. We propose that mammals may help to maintain colour pattern polymorphism within populations of P. cinereus by avoiding novel, unfamiliar colour morphs. Additionally, selective pressures from multiple predators and variation in predator communities among sites may contribute to the maintenance of colour polymorphism within and among localities in this salamander species.     

Differential foraging success across a light level spectrum explains the maintenance and spatial structure of colour morphs in a polymorphic bird

Detectability of different colour morphs under varying light conditions has been proposed as an important driver in the maintenance of colour polymorphism via disruptive selection. To date, no studies have tested whether different morphs have selective advantages under differing light conditions. We tested this hypothesis in the black sparrowhawk, a polymorphic raptor exhibiting a discrete white and dark morph, and found that prey provisioning rates differ between the morphs depending on light condition. Dark morphs delivered more prey in lower light conditions, while white morphs provided more prey in brighter conditions. We found support for the role of breeding season light level in explaining the clinal pattern of variation in morph ratio across the species range throughout South Africa. Our results provide the first empirical evidence supporting the hypothesis that polymorphism in a species, and the spatial structuring of morphs across its distribution, may be driven by differential selective advantage via improved crypsis, under varying light conditions.     

Wild birds prefer the familiar morph when feeding on pastry-filled shells of the landsnail Cepaea hortensis (Müll.)

Colour polymorphisms in prey could be maintained if predators concentrate on common morphs and confer a selective advantage on rare morphs. We describe experiments to test whether wild birds feed on pastry-stuffed shells of Cepaea hortensis in a manner that might lead to such apostatic selection. The birds were first given a 'pre-training' choice test of a shell population with equal numbers of yellow unbandeds and yellow five-bandeds; they were then trained on one morph alone, given a second choice test, trained on the other morph and, finally, given a third choice test. The birds preferred five-bandeds in five of the six pre-training tests. In all six experiments the first training session increased the birds' preferences for the morph that was familiar. The results were less clear-cut when selection during pre-training was compared with selection after the second training session. However, a comparison between selection after each of the two training sessions showed that in all six experiments the results were in the direction predicted from the hypothesis that familiar morphs are preferred. This set of experiments is one of the few in which behaviour which could lead to apostatic selection has been tested with morphs that differ in pattern. The findings support the idea that polymorphism in Cepaea could be maintained by apostatic selection.     

Differential predation on the two colour morphs of Nicaraguan Crater lake Midas cichlid fish: implications for the maintenance of its gold‐dark polymorphism

Predation can play an important role in the evolution and maintenance of prey colour polymorphisms. Several factors are known to affect predator choice, including the prey's relative abundance and conspicuousness. In polymorphic prey species, predators often target the most common or most visible morphs. To test if predator choice can explain why in Midas cichlid fish the more visible (gold) morph is also more rare than the inconspicuous dark morph, we conducted predation experiments using two differently coloured wax models in Nicaraguan crater lakes. Contrary to expectations, we observed an overall higher attack rate on the much more abundant, yet less conspicuous dark models, and propose frequency‐dependent predation as a potential explanation for this result. Interestingly, the attack rate differed between different types of predators. While avian predators were biased towards the abundant and less colourful dark morphs, fish predators did not show a strong bias. However, the relative attack rate of fish predators seemed to vary with the clarity of the water, as attack rates on gold models went up as water clarity decreased. The relative differential predation rates on different morphs might impact the relative abundance of both colour morphs and thus explain the maintenance of the colour polymorphism. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 123–131.     

Predator-prey relationships and the evolution of colour polymorphism: a comparative analysis in diurnal raptors

Genetically based variation in coloration occurs in populations of many organisms belonging to various taxa, including birds, mammals, frogs, molluscs, insects and plants. Colour polymorphism has evolved in raptors more often than in any other group of birds, suggesting that predator–prey relationships was a driving evolutionary force. Individuals displaying a new invading colour morph may enjoy an initial foraging advantage because prey have difficulties in learning the colour of a rare morph (apostatic selection), or because morphs provide alternative foraging benefits allowing differently coloured individuals to exploit distinct food niches (disruptive selection). Plumage polymorphism should therefore have evolved in species that prey upon animals having the physiological ability to distinguish between differently coloured predators but also to flee once a predator has been detected. From this assumption, we can predict that closely related polymorphic and monomorphic species prey upon different animals. They may also differ in morphology, because foraging upon different prey may require different foraging modes, and in turn different morphological structures. We tested these two predictions in a comparative study of raptors. As expected, polymorphic and monomorphic species had a different diet, and there was a difference in wing length between polymorphic and monomorphic species within two genera ( Buteo and Accipiter ). Across all raptors for which phylogenetic relationships are known, polymorphic species preyed more often upon mammals than did monomorphic ones. These two types of raptor did not differ in the frequency of birds, insects and reptiles in their diets. We discuss these results in the light of the hypothesis that predator–prey relationships played a role in the evolution of colour polymorphism. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 565–578.     

Ecology of the fruit-colour polymorphism in Rubus spectabilis

Although some studies have focused on the colour polymorphisms of flowers and fruits, little is known of their ecological and evolutionary significance. We investigated the potential contribution of several factors to the maintenance of fruit-colour polymorphism in Rubus spectabilis, a common shrub in the temperate rainforests of southeast Alaska. Fruits occur in two colours (red and orange), whose frequencies vary geographically. The two colour morphs have similar size, weight, seed load and nutrient composition. Colour preferences of avian frugivores, in the aviary and in the field, varied among individuals, but the majority favoured red fruits. Seed predators (mostly rodents) did not discriminate between seeds from different morphs. The effect of seed passage through the digestive tract of frugivores (birds and bears) on germination was similar for both morphs, although there were significant differences among frugivores. The type of soil on which the seeds are deposited influenced their germination behaviour, suggesting that some soils could favour one morph over the other. Such differences may contribute to the regional differences in frequencies of the two morphs. This study emphasizes the need to investigate fruit and seed characteristics that correlate with fruit colour; the colour preferences of consumers is only one of several selection pressures that determine the frequency distribution of fruit colours. This revised version was published online in July 2006 with corrections to the Cover Date.     

Differential predation on colour morphs of the Midas cichlid, Cichlasoma citrinellum

Predation has often been invoked as a selective agent affecting colour patterns in a wide range of organisms, but data relating susceptibility to predation and objective measures of conspicuousness are rare. To investigate relative crypticity in free-swimming fishes, two colour morphs of the Midas cichlid were exposed to predation by largemouth bass, Micropterus salmoides. The two colour morphs, normal and amelanic golds, were viewed by predators in ponds against a uniform, natural background. Swimming pools, 4 m in diameter, were stocked with equal numbers of gold and normal juvenile Midas cichlids. Bass took a significantly higher proportion of normal-coloured fishes (69·2% of fish) than gold morphs overall, and in a significantly higher proportion of trials (68·8% of experiments). No differences were found between colour morphs in their behaviour or in the willingness of bass to attack either morph. The significance of these results are discussed in relation to the visual system of the predator and the relative conspicuousness of the prey colour patterns.     

The evolution of colour polymorphism in British winter‐active Lepidoptera in response to search image use by avian predators

Phenotypic polymorphism in cryptic species is widespread. This may evolve in response to search image use by predators exerting negative frequency‐dependent selection on intraspecific colour morphs, ‘apostatic selection’. Evidence exists to indicate search image formation by predators and apostatic selection operating on wild prey populations, though not to demonstrate search image use directly resulting in apostatic selection. The present study attempted to address this deficiency, using British Lepidoptera active in winter as a model system. It has been proposed that the typically polymorphic wing colouration of these species represents an anti‐search image adaptation against birds. To test (a) for search image‐driven apostatic selection, dimorphic populations of artificial moth‐like models were established in woodland at varying relative morph frequencies and exposed to predation by natural populations of birds. In addition, to test (b) whether abundance and degree of polymorphism are correlated across British winter‐active moths, as predicted where search image use drives apostatic selection, a series of phylogenetic comparative analyses were conducted. There was a positive relationship between artificial morph frequency and probability of predation, consistent with birds utilizing search images and exerting apostatic selection. Abundance and degree of polymorphism were found to be positively correlated across British Lepidoptera active in winter, though not across all taxonomic groups analysed. This evidence is consistent with polymorphism in this group having evolved in response to search image‐driven apostatic selection and supports the viability of this mechanism as a means by which phenotypic and genetic variation may be maintained in natural populations.     

Colour biases in territorial aggression in a Neotropical cichlid fish

Discrete colour morphs have provided important insights into the evolution of phenotypic diversity. One of the mechanisms that can help to explain coexistence of ecologically similar colour morphs and incipient species is (colour) biased aggression, which has the potential to promote continued existence of the morphs in a frequency-dependent manner. I addressed colour biases in territorial aggression in a field-based study on a Neotropical cichlid fish species, Amphilophus sagittae, which has two ecologically indistinguishable colour morphs that mate assortatively. I found that A. sagittae, in particular females, were more aggressive towards models of their own colour than those mimicking colours of the other morph. Such a behavioural pattern should result in a selection regime that benefits the rarer morph, and hence could help explain how novel, rare phenotypes may avoid competitive exclusion.