Linking the evolution and form of warning coloration in nature

Many animals are toxic or unpalatable and signal this to predators with warning signals (aposematism). Aposematic appearance has long been a classical system to study predator–prey interactions, communication and signalling, and animal behaviour and learning. The area has received considerable empirical and theoretical investigation. However, most research has centred on understanding the initial evolution of aposematism, despite the fact that these studies often tell us little about the form and diversity of real warning signals in nature. In contrast, less attention has been given to the mechanistic basis of aposematic markings; that is, ‘what makes an effective warning signal?’, and the efficacy of warning signals has been neglected. Furthermore, unlike other areas of adaptive coloration research (such as camouflage and mate choice), studies of warning coloration have often been slow to address predator vision and psychology. Here, we review the current understanding of warning signal form, with an aim to comprehend the diversity of warning signals in nature. We present hypotheses and suggestions for future work regarding our current understanding of several inter-related questions covering the form of warning signals and their relationship with predator vision, learning, and links to broader issues in evolutionary ecology such as mate choice and speciation.     

Artificial neural networks and the study of evolution of prey coloration

In this paper, I investigate the use of artificial neural networks in the study of prey coloration. I briefly review the anti-predator functions of prey coloration and describe both in general terms and with help of two studies as specific examples the use of neural network models in the research on prey coloration. The first example investigates the effect of visual complexity of background on evolution of camouflage. The second example deals with the evolutionary choice of defence strategy, crypsis or aposematism. I conclude that visual information processing by predators is central in evolution of prey coloration. Therefore, the capability to process patterns as well as to imitate aspects of predator's information processing and responses to visual information makes neural networks a well-suited modelling approach for the study of prey coloration. In addition, their suitability for evolutionary simulations is an advantage when complex or dynamic interactions are modelled. Since not all behaviours of neural network models are necessarily biologically relevant, it is important to validate a neural network model with empirical data. Bringing together knowledge about neural networks with knowledge about topics of prey coloration would provide a potential way to deepen our understanding of the specific appearances of prey coloration.     

Constrained camouflage facilitates the evolution of conspicuous warning coloration

The initial evolution of aposematic and mimetic antipredator signals is thought to be paradoxical because such coloration is expected to increase the risk of predation before reaching a stage when predators associate it effectively with a defense. We propose, however, that constraints associated with the alternative strategy, cryptic coloration, may facilitate the evolution of antipredator signals and thus provide a solution for the apparent paradox. We tested this hypothesis first using an evolutionary simulation to study the effect of a constraint due to habitat heterogeneity, and second using a phylogenetic comparison of the Lepidoptera to investigate the effect of a constraint due to prey motility. In the evolutionary simulation, antipredator warning coloration had an increased probability to invade the prey population when the evolution of camouflage was constrained by visual difference between microhabitats. The comparative study was done between day-active lepidopteran taxa, in which camouflage is constrained by motility, and night-active taxa, which rest during the day and are thus able to rely on camouflage. We compared each of seven phylogenetically independent day-active groups with a closely related nocturnal group and found that antipredator signals have evolved at least once in all the diurnal groups but in none of their nocturnal matches. Both studies lend support to our idea that constraints on crypsis may favor the evolution of antipredator warning signals.     

Predator perception and the interrelation between different forms of protective coloration

Animals possess a range of defensive markings to reduce the risk of predation, including warning colours, camouflage, eyespots and mimicry. These different strategies are frequently considered independently, and with little regard towards predator vision, even though they may be linked in various ways and can be fully understood only in terms of predator perception. For example, camouflage and warning coloration need not be mutually exclusive, and may frequently exploit similar features of visual perception. This paper outlines how different forms of protective markings can be understood from predator perception and illustrates how this is fundamental in determining the mechanisms underlying, and the interrelation between, different strategies. Suggestions are made for future work, and potential mechanisms discussed in relation to various forms of defensive coloration, including disruptive coloration, eyespots, dazzle markings, motion camouflage, aposematism and mimicry.     

Towards an ecology of protective coloration

The strategies underlying different forms of protective coloration are well understood but little attention has been paid to the ecological, life-history and behavioural circumstances under which they evolve. While some comparative studies have investigated the ecological correlates of aposematism, and background matching, the latter particularly in mammals, few have examined the ecological correlates of other types of protective coloration. Here, we first outline which types of defensive coloration strategies may be exhibited by the same individual; concluding that many protective coloration mechanisms can be employed simultaneously, particularly in conjunction with background matching. Second, we review the ecological predictions that have been made for each sort of protective coloration mechanism before systematically surveying phylogenetically controlled comparative studies linking ecological and social variables to antipredator defences that involve coloration. We find that some a priori predictions based on small-scale empirical studies and logical arguments are indeed supported by comparative data, especially in relation to how illumination affects both background matching and self-shadow concealment through countershading; how body size is associated with countershading, motion dazzle, flash coloration and aposematism, although only in selected taxa; how immobility may promote background matching in ambush predators; and how mobility may facilitate motion dazzle. Examination of nearly 120 comparative tests reveals that many focus on ecological variables that have little to do with predictions derived from antipredator defence theory, and that broad-scale ecological studies of defence strategies that incorporate phylogenetics are still very much in their infancy. We close by making recommendations for future evolutionary ecological research.     

Pupal warning color development in above-ground pupating species but cryptic color in ground-surface pupating species of the nine-spotted diurnal moths (Erebidae: Arctiinae: Syntomini)

Insects usually have cryptic colors to avoid detection by visually hunting predators. However, if the insects acquire toxic or repellent substances against predators, some of them develop conspicuous coloration to exhibit their unpalatability. Such warning colors allow insects to survive. In the nine-spotted diurnal moths (Erebidae: Arctiinae: Syntomini), we found the above-ground pupating species to have conspicuous colored pupae, but the ground-surface pupating species to have cryptic colored pupae. In this study, the relationships between unpalatability and coloration of these pupae are examined among three species of Amata and one species of Syntomoides. Pupae of the two species (A. germana and A. flava) are conspicuous in their color pattern with seven black dotted lines longitudinally on their pale-yellow bodies. These pupae are exposed to the aerial predators in a coarse silk mesh hanging from leaves and/or branches. The other two species (A. fortunei and S. imaon) pupate in spaces under stones, fallen twigs and leaves on the ground surface, and the pupae in a coarse silk cocoon is cryptic dark brown. Their pupation site selections are reproduced in the rearing glass vessels. Palatability assessment using lizards as a potential predator suggests that pupae of A. germana, A. flava and A. fortunei are unpalatable and the lizard's feeding response decreases with experience. However, pupae of S. imaon are all eaten (palatable). Finally, the possible evolutionary scenario of pupal colors of these four species is discussed in relation to pupation site selection and palatability.     

Community structure and the evolution of aposematic coloration

Studies on the evolution of aposematic coloration (prey coloration advertising for unpalatability) have mainly focused on predator psychology in simplified single-prey species systems. We chose, instead, to model population dynamics on the community level. We studied the invasion by an aposematic phenotype in the presence and absence of another prey species. The single-prey and two-prey models differed in two major ways. First, with two prey species the invasion was possible only with a weak aposematic signal, whereas with a single prey species there was no such an upper limit for signal strength. Second, with a single prey species, increase of the aposematic phenotype always resulted in rapid extinction of the predator. Resource value and growth rate of the alternative prey species affected the invasion. These results suggest that community structure is an important determinant of the conditions for invasion of aposematism, and may have contributed to its initial evolution.     

The roles of morphological traits,resource variation and resource partitioning associated with the dietary niche expansion in the fish‐eating bat Myotis pilosus

Niche expansion and shifts are involved in the response and adaptation to environmental changes. However, it is unclear how niche breadth evolves and changes toward higher‐quality resources. Myotis pilosus is both an insectivore and a piscivore. We examined the dietary composition and seasonality in M. pilosus and the closely related Myotis fimbriatus using next‐generation DNA sequencing. We tested whether resource variation or resource partitioning help explain the dietary expansion from insects to fish in M. pilosus. While diet composition and diversity varied significantly between summer and autumn, the proportion of fish‐eating individuals did not significantly change between seasons in M. pilosus. Dietary overlap between M. pilosus and M. fimbriatus during the same seasons was much higher than within individual species across seasons. We recorded a larger body size, hind foot length, and body mass in M. pilosus than in M. fimbriatus and other insectivorous trawling bats from China. Similar morphological differences were found between worldwide fishing bats and nonfishing trawling bats. Our results suggest that variation in insect availability or interspecific competition may not play important roles in the dietary expansion from insects to fish in M. pilosus. Myotis pilosus has morphological advantages that may help it use fish as a diet component. The morphological advantage promoting dietary niche evolution toward higher quality resources may be more important than variation in the original resource and the effects of interspecific competition.     

The protective value of conspicuous signals is not impaired by shape, size, or position asymmetry

Various conspicuous signals in nature promote initial and learnedavoidance by predators. It is widely thought that such signalsare most effective when highly symmetrical in features suchas size and shape, supported by recent laboratory experimentswith domestic chicks and artificial prey. However, no studyhas investigated the effect of asymmetry on conspicuous signalsin a natural setting, where viewing distances, angles, predatorspecies, and light conditions vary and where predators encounterprey sequentially rather than simultaneously. We undertook 2field experiments with artificial gray-scale prey, marked witha pair of white markings presented to wild avian predators,to test the effect of asymmetry on the survival value of conspicuoussignals in the field. Experiment 1 had treatments with symmetricalspots or with spots asymmetrical in area between 5 and 50%.All marked treatments survived better than unmarked controls,but there was no benefit of being symmetrical. Experiment 2tested the effect of possessing markings asymmetrical for shapeor position and any additive effect of these 2 features. Again,symmetry conferred no benefit and targets with markings asymmetricalfor position and/or shape survived equally well as those withsymmetrical arrangements. These findings indicate that asymmetryin warning signals may not be costly to prey in nature or beof less importance compared with other features of the signal,such as color and overall size.     

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.     

Ecological factors influencing the evolution of insects' chemical defenses

How insect defense chemicals have evolved has remained relativelyunderstudied, compared with the evolution of aposematic signalsof such defenses. Because there is mounting evidence that chemicaldefenses can generally be expected to be costly, understandingthe evolution of such defenses and their maintenance in theface of the potential for automimicry (signaling by individualsthat do not invest in defense) is nontrivial. One potentialexplanation is that chemically defended insects suffer lessfrom predation than those that do not invest in chemical defenses.Here, we use a series of models to explore aspects of the evolutionof such costly chemical defenses. Our models predict that investmentin costly defenses can occur across a wide range of predationintensities; however, if predation intensity is low, then thedefense has to be very effective to be selected, unless thedefense is very cheap. Furthermore, the evolution of antipredatorydefenses will be relatively insensitive to the severity of anymechanism, whereby prey pay a cost every time they use theirdefense against an attacking predator even if they survive theattack, but sensitive to the form of the relationship betweeninitial investment in constituting the defense and survivalbenefit. Once defense becomes common in the prey population,prey may get a frequency-dependent benefit if predators learnto avoid prey of this type after several attacks. Finally, wepredict that increasing the rate of avoidance learning by predatorsencourages reduced investment in antipredatory defenses by prey.The potential for these predictions to be tested empiricallyis discussed.     

Exposure to predators does not lead to the evolution of larger brains in experimental populations of threespine stickleback

Natural selection is often invoked to explain differences in brain size among vertebrates. However, the particular agents of selection that shape brain size variation remain obscure. Recent studies suggest that predators may select for larger brains because increased cognitive and sensory abilities allow prey to better elude predators. Yet, there is little direct evidence that exposure to predators causes the evolution of larger brains in prey species. We experimentally tested this prediction by exposing families of 1000–2000 F2 hybrid benthic‐limnetic threespine stickleback to predators under naturalistic conditions, along with matched controls. After two generations of selection, we found that fish from the predator addition treatment had significantly smaller brains (specifically smaller telencephalons and optic lobes) than fish from the control treatment. After an additional generation of selection, we reared experimental fish in a common environment and found that this difference in brain size was maintained in the offspring of fish from the predator addition treatment. Our results provide direct experimental evidence that (a) predators can indeed drive the evolution of brain size–‐but not in the fashion commonly expected and (b) that the tools of experimental evolution can be used to the study the evolution of the vertebrate brain.     

Diversity of warning signal and social interaction influences the evolution of imperfect mimicry

Mimicry, the resemblance of one species by another, is a complex phenomenon where the mimic (Batesian mimicry) or the model and the mimic (Mullerian mimicry) gain an advantage from this phenotypic convergence. Despite the expectation that mimics should closely resemble their models, many mimetic species appear to be poor mimics. This is particularly apparent in some systems in which there are multiple available models. However, the influence of model pattern diversity on the evolution of mimetic systems remains poorly understood. We tested whether the number of model patterns a predator learns to associate with a negative consequence affects their willingness to try imperfect, novel patterns. We exposed week‐old chickens to coral snake (Micrurus) color patterns representative of three South American areas that differ in model pattern richness, and then tested their response to the putative imperfect mimetic pattern of a widespread species of harmless colubrid snake (Oxyrhopus rhombifer) in different social contexts. Our results indicate that chicks have a great hesitation to attack when individually exposed to high model pattern diversity and a greater hesitation to attack when exposed as a group to low model pattern diversity. Individuals with a fast growth trajectory (measured by morphological traits) were also less reluctant to attack. We suggest that the evolution of new patterns could be favored by social learning in areas of low pattern diversity, while individual learning can reduce predation pressure on recently evolved mimics in areas of high model diversity. Our results could aid the development of ecological predictions about the evolution of imperfect mimicry and mimicry in general.     

Evolving the selfish herd: emergence of distinct aggregating strategies in an individual-based model

From zebra to starlings, herring and even tadpoles, many creatures move in an organized group. The emergent behaviour arises from simple underlying movement rules, but the evolutionary pressure which favours these rules has not been conclusively identified. Various explanations exist for the advantage to the individual of group formation: reduction of predation risk; increased foraging efficiency or reproductive success. Here, we adopt an individual-based model for group formation and subject it to simulated predation and foraging; the haploid individuals evolve via a genetic algorithm based on their relative success under such pressure. Our work suggests that flock or herd formation is likely to be driven by predator avoidance. Individual fitness in the model is strongly dependent on the presence of other phenotypes, such that two distinct types of evolved group can be produced by the same predation or foraging conditions, each stable against individual mutation. We draw analogies with multiple Nash equilibria theory of iterated games to explain and categorize these behaviours. Our model is sufficient to capture the complex behaviour of dynamic collective groups, yet is flexible enough to manifest evolutionary behaviour.     

Perspective: repression of competition and the evolution of cooperation

Abstract Repression of competition within groups joins kin selection as the second major force in the history of life shaping the evolution of cooperation. When opportunities for competition against neighbors are limited within groups, individuals can increase their own success only by enhancing the efficiency and productivity of their group. Thus, characters that repress competition within groups promote cooperation and enhance group success. Leigh first expressed this idea in the context of fair meiosis, in which each chromosome has an equal chance of transmission via gametes. Randomized success means that each part of the genome can increase its own success only by enhancing the total number of progeny and thus increasing the success of the group. Alexander used this insight about repression of competition in fair meiosis to develop his theories for the evolution of human sociality. Alexander argued that human social structures spread when they repress competition within groups and promote successful group-against-group competition. Buss introduced a new example with his suggestion that metazoan success depended on repression of competition between cellular lineages. Maynard Smith synthesized different lines of thought on repression of competition. In this paper, I develop simple mathematical models to illustrate the main processes by which repression of competition evolves. With the concepts made clear, I then explain the history of the idea. I finish by summarizing many new developments in this subject and the most promising lines for future study.     

To quiver or to shiver: increased melanization benefits thermoregulation,but reduces warning signal efficacy in the wood tiger moth

Melanin production is often considered costly, yet beneficial for thermoregulation. Studies of variation in melanization and the opposing selective forces that underlie its variability contribute greatly to understanding natural selection. We investigated whether melanization benefits are traded off with predation risk to promote observed local and geographical variation in the warning signal of adult male wood tiger moths (Parasemia plantaginis). Warning signal variation is predicted to reduce survival in aposematic species. However, in P. plantaginis, male hindwings are either yellow or white in Europe, and show continuous variation in melanized markings that cover 20 to 90 per cent of the hindwing. We found that the amount of melanization increased from 40 to 59 per cent between Estonia (58° N) and north Finland (67° N), suggesting melanization carries thermoregulatory benefits. Our thermal measurements showed that more melanic individuals warmed up more quickly on average than less melanic individuals, which probably benefits flight in cold temperatures. With extensive field experiments in central Finland and the Alpine region, we found that more melanic individuals suffered increased predation. Together, our data suggest that warning signal efficiency is constrained by thermoregulatory benefits. Differences in relative costs and benefits of melanin probably help to maintain the geographical warning signal differences.     

Effects of predation,parasites, and phylogeny on the evolution of bright coloration in north american male passerines

Summary Numerous mechanisms have been proposed to account for the evolution of cryptic and bright coloration in passerine birds. The Hamilton-Zuk revealing handicap model holds that cyclic interactions between hosts and parasites maintain additive genetic variance in secondary sexual traits and adaptive mate choice of resistant genotypes ensues (Hamilton and Zuk, 1982). Here I report no support for this model using various within-taxa techniques to test the functional relationship between the prevalence of hematozoan parasites and male brightness in many species of North American passerines. I establish that phylogeny and predation risk are most strongly associated with variation in male coloration. Ground-nesting passerines are considerably more cryptic than off-ground nesters, and there is evidence that ground-nesting passerines are under greater predation risk. Predation risk may limit the role of sexual selection in the development of bright coloration.