Evolutionary significance of ontogenetic colour change in animals

Ontogenetic colour changes are non-reversible colour changes associated with normal progressive development of an individual of a species. This paper provides the first review of the evolutionary significance of this phenomenon in animals. Proximate mechanisms and environmental cues are briefly discussed and a conceptual framework for understanding the ultimate reasons for ontogenetic colour change is established. Changes in size, vulnerability, reproductive status, habitat and metabolism are often associated with ontogenetic colour change and can aid in understanding its adaptive significance. Neutral or non-adaptive ontogenetic colour changes due to phylogenetic inertia and developmental constraints are also considered. Existing studies of ontogenetic colour changes in marine invertebrates, terrestrial invertebrates, fish, amphibians, reptiles, birds and mammals are discussed within this framework. A need is identified for more experimental tests of hypotheses for the significance of ontogenetic colour change.     

An overview of the relationships between mimicry and crypsis

There have been many different and conflicting definitions of mimicry. Some of the definitions of mimicry include crypsis and others do not. Each definition includes different groups of phenomena and uses different criteria to distinguish mimetic from non-mimetic phenomena. The confusion is eliminated by a consideration of the criteria of all definitions. This shows that there are in fact three major criteria dividing six phenomona, rather than a single dichotomy between mimicry and crypsis (Table 2). The criteria are defined by the results of a mistake in discrimination between the model and mimìc: (a) the mistake does or does not depend upon relationship between mimic and background; (b) the mistake has or has no effect on the population dynamics or evolution of the model and (c) the mistake affects dynamics or evolution of one or of many models. The main reason for the contusion about mimicry and crypsis is that each author's definition includes differing and partially overlapping subsets of the six classes: crypsis; masquerade; Batesism; Müllerism; polymorphism and convergence.     

An overview of the relationships between mimicry and crypsis

There have been many different and conflicting definitions of mimicry. Some of the definitions of mimicry include crypsis and others do not. Each definition includes different groups of phenomena and uses different criteria to distinguish mimetic from non-mimetic phenomena. The confusion is eliminated by a consideration of the criteria of all definitions. This shows that there are in fact three major criteria dividing six phenomona, rather than a single dichotomy between mimicry and crypsis (Table 2). The criteria are defined by the results of a mistake in discrimination between the model and mimìc: (a) the mistake does or does not depend upon relationship between mimic and background; (b) the mistake has or has no effect on the population dynamics or evolution of the model and (c) the mistake affects dynamics or evolution of one or of many models. The main reason for the contusion about mimicry and crypsis is that each author's definition includes differing and partially overlapping subsets of the six classes: crypsis; masquerade; Batesism; Müllerism; polymorphism and convergence.     

Progressive background in moths, and a quantitative measure of crypsis

A method is presented for quantitative estimation of the degree of crypsis of species seen by visual predators against known backgrounds. It is based upon a comparison between transects taken across animal and background colour patterns. The method was applied to day-resting moths in deciduous forest in New Jersey. Each species is found for two to four weeks at characteristic dates, and there is a constant turnover of species. In both moths and backgrounds there is a regular change in the colour pattern parameters from winter through spring to early summer. Moths are on average more cryptic at their normal dates than they would be if present earlier or later in the year. Species with known resting sites are on average more cryptic on their resting sites than other background habitats. Species that rest on more than one background habitat are less cryptic on their preferred habitats than are specialists. Species that rest under leaves and are not visible from above are not very cryptic. Specific v. general resemblance, disruptive coloration, and factors affecting 'aspect diversity' are discussed. The new method of estimating crypsis is useful for studies of crypsis as well as in sexual selection. It is necessary to know much about the resting sites and behaviour of moths, as well as other functions of colour patterns, to understand colour pattern evolution.     

Behavioural,ecological, and evolutionary aspects of diversity in frog colour patterns

The role of colours and colour patterns in behavioural ecology has been extensively studied in a variety of contexts and taxa, while almost overlooked in many others. For decades anurans have been the focus of research on acoustic signalling due to the prominence of vocalisations in their communication. Much less attention has been paid to the enormous diversity of colours, colour patterns, and other types of putative visual signals exhibited by frogs. With the exception of some anecdotal observations and studies, the link between colour patterns and the behavioural and evolutionary ecology of anurans had not been addressed until approximately two decades ago. Since then, there has been ever‐increasing interest in studying how colouration is tied to different aspects of frog behaviour, ecology and evolution. Here I review the literature on three different contexts in which frog colouration has been recently studied: predator–prey interactions, intraspecific communication, and habitat use; and I highlight those aspects that make frogs an excellent, yet understudied, group to examine the role of colour in the evolution of anti‐predation strategies and animal communication systems. Further, I argue that in addition to natural‐history observations, more experiments are needed in order to elucidate the functions of anuran colouration and the selective pressures involved in its diversity. To conclude, I encourage researchers to strengthen current experimental approaches, and suggest future directions that may broaden our current understanding of the adaptive value of anuran colour pattern diversity.     

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.     

The heritable basis and cost of colour plasticity in coastrange sculpins

Both genetic and plastic traits contribute to adaptation in novel environments. Phenotypic plasticity can facilitate adaptation by allowing for existence in a wider range of conditions and a faster response to environmental change than gene‐based selection. Coastrange sculpins (Cottus aleuticus) colonize new and variable streams arising in the wake of receding glaciers in south‐east Alaska, and substrate‐matching plasticity may enhance colonization success by reducing detection by visual predators. As part of a long‐term study of the fitness consequences of colour plasticity and its capacity to respond to both positive and negative selection, we investigated whether it is heritable and costly. We raised full‐sib broods of sculpins in the laboratory: one half of each brood was raised in white containers, the other half in black. After 4 months, we digitally analysed their colour and found significant but weak heritability in both baseline colour and colour plasticity. To investigate the cost of colour plasticity, we compared the growth and mortality rates of juvenile sculpins reared under constant substrate colours to those reared on substrates that changed colour frequently, and compared growth rates among sculpin that differed in their colour change ability. We found evidence of small costs of plasticity, consistent with other studies of natural populations. Evidence of heritable genetic variation for plasticity and small costs to its maintenance and expression contributes to explanations of how plasticity is variable and persistent among wild populations and underscores its ability to respond both positively and negatively to selection in variable habitats.     

Losing the trait without losing the signal: Evolutionary shifts in communicative colour signalling

Colour signalling traits are often lost over evolutionary time, perhaps because they increase vulnerability to visual predators or lose relevance in terms of sexual selection. Here, we used spectrometric and phylogenetic comparative analyses to ask whether four independent losses of a sexually selected blue patch are spectrally similar, and whether these losses equate to a decrease in conspicuousness or to loss of a signal. We found that patches were lost in two distinct ways: either increasing reflectance primarily at very long or at very short wavelengths, and that species with additional colour elements (UV, green and pink) may be evolutionary intermediates. In addition, we found that patch spectral profiles of all species were closely aligned with visual receptors in the receiver's retina. We found that loss of the blue patch makes males less conspicuous in terms of chromatic conspicuousness, but more conspicuous in terms of achromatic contrast, and that sexual dimorphism often persists regardless of patch loss. Dorsal surfaces were considerably more cryptic than were ventral surfaces, and species in which male bellies were the most similar in conspicuousness to their dorsal surfaces were also the most sexually dimorphic. These results emphasize the consistent importance of sexual selection and its flexible impact on different signal components through evolutionary time.     

The adaptive significance of colour pattern polymorphism in the Australian scincid lizard Lampropholis delicata

Females of Lampropholis delicata are dimorphic for colour pattern, the difference between morphs being the presence or absence of a distinct white mid-lateral stripe. A less distinct striped morph occurs also in males. We evaluated alternative hypotheses for the maintenance of this polymorphism by examining temporal and spatial variation in morph frequency, testing for differential selection among morphs using data on body size and reproductive traits from preserved specimens, and experimentally manipulating colour pattern in free-ranging lizards of both sexes, to assess the influence of the lateral stripe on survival rates. We found that the relative frequency of striped individuals varied among populations and decreased from north to south in both sexes, coincident with an increasing incidence of regenerated tails. Morph frequencies did not change through time within a population. Striped gravid females appeared to survive better and produced larger clutches than did non-striped females. In our experimental study, the relationship between survival and colour morph differed between the two sexes; males painted with a white lateral stripe had lower survival than control (brown stripe) males, but survival did not differ between striped and control females. The different response in the two sexes may be due partly to differences in temperature and microhabitat selection. We propose that the white lateral stripe decreases susceptibility to predators in gravid females but increases risk of predation in males, especially in combination with low temperatures. The polymorphism might be maintained by: (1) opposing fitness consequences of the stripe in males and females; (2) sex-specific habitat selection; and (3) gene flow in combination with spatial variation in relative fitness of the two morphs.     

Habitat heterogeneity, predation and gene flow: colour polymorphism in the isopod, Idotea baltica

The colour polymorphic isopod Idotea baltica inhabits the brown alga Fucus vesiculosus which is often colonised by the white epizoite Electra crustulenta (Bryozoa). In an experiment the predation risk for the different colour morphs of I. baltica was highly dependent on background colouration. Morph frequencies and Electra density varied substantially among 10 collecting sites but correlated poorly with each other, suggesting that local selection for cryptic colouration may be counteracted by gene flow. Indeed, estimates based on four polymorphic allozymes suggested rate of gene flow to be high. These results support the hypothesis that locally varying selection for cryptic colouration counteracted by gene flow contributes to the maintenance of colour polymorphism in I. baltica. The visual differences between the microhabitats and the differential microhabitat use between males and females seem to result in different patterns of selection on males and females for cryptic colouration. Also this is likely to play an important role for the polymorphism.     

Tests of search image and learning in the wild: Insights from sexual conflict in damselflies

Search image formation, a proximal mechanism to maintain genetic polymorphisms by negative frequency‐dependent selection, has rarely been tested under natural conditions. Females of many nonterritorial damselflies resemble either conspecific males or background vegetation. Mate‐searching males are assumed to form search images of the majority female type, sexually harassing it at rates higher than expected from its frequency, thus selectively favoring the less common morph. We tested this and how morph coloration and behavior influenced male perception and intersexual encounters by following marked Ischnura elegans and noting their reactions to conspecifics. Contrary to search image formation and associative learning hypotheses, although males encountered the minority, male‐like morph more often, sexual harassment and clutch size were similar for both morphs. Prior mating attempts or copula with morphs did not affect a male''s subsequent reaction to them; males rarely attempted matings with immature females or males. Females mated early in the day, reducing the opportunity for males to learn their identity beforehand. Once encountered, the male‐like morph was more readily noticed by males than the alternative morph, which once noticed was more likely to receive mating attempts. Flexible behavior gave morphs considerable control over their apparency to males, influencing intersexual encounters. Results suggested a more subtle proximal mechanism than male learning maintains these color polymorphisms and call for inferences of learning to be validated by behavior of wild receivers and their signalers.     

Experimental manipulation reveals differential effects of colour pattern on survival in male and female pygmy grasshoppers

Populations of pygmy grasshoppers, Tetrix subulata, exhibit genetically coded discontinuous variation in colour pattern. To determine whether the dynamics of this polymorphism is likely to be affected by selective processes, rather than by stochastic events, we experimentally manipulated colour patterns of free-ranging grasshoppers and then calculated and controlled for differences in capture probabilities between categories of individuals before estimating and testing for differences in survival using mark–recapture data and program SURGE . We found that paint treatment had a significant effect on survival, and that the relationship between colour pattern and survival was different in males and females. Our analyses also revealed significant differences between sexes in relative frequencies of natural colour morphs, body size, activity pattern, dispersal distance and microhabitat use. These findings accord with the hypothesis that colour pattern and behaviour jointly determine susceptibility to visual predators. Our data enable us to reject the null-hypothesis that colour pattern is a selectively neutral character and that the polymorphism is maintained solely by stochastic processes, such as random genetic drift and founder events. Indeed, the effect of dorsal coloration on survival, together with associations between colour pattern and many biologically important traits (body size, behaviour, thermal capacity, physiology and reproductive performance), suggests that colour pattern is likely to significantly influence individual fitness, and that the polymorphism must be maintained by some active process, such as spatially variable selection in combination with gene flow. The possible role of colour polymorphism as an intermediate stage in the evolution of sexual dichromatism in animals is discussed.     

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.     

Asymmetry in size, shape, and color impairs the protective value of conspicuous color patterns

The received view of protective coloration in animals is thatconspicuous colors and patterns have evolved because they elicitavoidance behavior in potential predators. In the present study,we examine the spontaneous response of naive predators (Gallusgallus domesticus) to artificial prey to test the hypothesisthat deviations from bilateral symmetry of signaling patternelements may negatively influence the avoidance-inducing effectof conspicuous color patterns. Chicks displayed stronger aversionsto artificial "butterfly" prey items possessing symmetric colorpattern elements than to those possessing asymmetric signalswith pattern elements of different color or shape. Althoughthey attacked signals with a size asymmetry of 5% at the samerate as symmetric signals, signals with a size asymmetry of7.5% or more were attacked more often than were symmetric signals.These results suggest that the protective value of conspicuouscolor patterns is impaired by asymmetry in color, shape, andsize of color pattern elements. Our findings also argue againstthe notion that animals have inherent preferences for symmetricover asymmetric objects, and demonstrate the existence of athreshold for asymmetry detection, beyond which further incrementsin asymmetry have no influence on signal efficacy.     

Studies of colour polymorphism in some marginal populations of the aposematic jersey tiger moth Callimorpha quadripunctaria

Callimorpha quadripunctaria (Lepidoptera, Arctiidae) is both genetically polymorphic for hindwing colour and well protected from predators. Polymorphic populations are, however, only found in the extreme northwest of its extensive distribution in Europe and Asia Minor. Use of a colour analyser confirmed the existence of three reasonably discrete colour classes: bright red, orange and yellow. These could each be subdivided into two further groupings of phenotypes, one of moths of pure colour and the other with a secondary colour. The species is polymorphic in SW England, where it became well established in villages and towns around the Exe estuary in the late 19th century. It now extends about 30 km east and west along the south coast of Devon and up to a similar distance inland along the river valleys. The rate of spread is consistent with the substantial dispersal of up to 500 m detected in a capture-recapture experiment performed at Exeter over the whole flight period in August 1984. This experiment also found no differences in timing of emergence, survivorship or within-habitat movement between the sexes or the colour classes. Males may show a higher rate of emigration than females. The species is polymorphic throughout S Devon. Its stronghold to the west of the Exe basin is characterized by a comparatively uniform morph frequency with 5045% red, 20–40% orange and 10–20% yellow. Yellow moths have their highest frequency in this area, red moths in the east and west and orange to the north. Adult activity is concentrated in the 2–3 h after dusk. Air temperatures of higher than 15°C are probably critical to pairing which involves sex pheromones released by females. This may be an important factor limiting the species' range. Our results suggest that climatic selection pressures involving non-visual differences in fitness account for the geographical variation. The lack of daytime activity of moths in comparison to that found by other workers on Rhodes and which is likely in other warmer climates suggests the hypothesis that expression of the polymorphism is favoured in the marginal populations of NW Europe by a relaxation of the stabilizing influence on the warning coloration exerted by visual predators.     

Evolutionary drivers of seasonal plumage colours: colour change by moult correlates with sexual selection,predation risk and seasonality across passerines

Some birds undergo seasonal colour change by moulting twice each year, typically alternating between a cryptic, non‐breeding plumage and a conspicuous, breeding plumage (‘seasonal plumage colours’). We test for potential drivers of the evolution of seasonal plumage colours in all passerines (N = 5901 species, c. 60% of all birds). Seasonal plumage colours are uncommon, having appeared on multiple occasions but more frequently lost during evolution. The trait is more common in small, ground‐foraging species with polygynous mating systems, no paternal care and strong sexual dichromatism, suggesting it evolved under strong sexual selection and high predation risk. Seasonal plumage colours are also more common in species predicted to have seasonal breeding schedules, such as migratory birds and those living in seasonal climates. We propose that seasonal plumage colours have evolved to resolve a trade‐off between the effects of natural and sexual selection on colouration, especially in seasonal environments.     

Sexual dichromatism and differential conspicuousness in two populations of the common collared lizard (Crotaphytus collaris) from Utah and New Mexico, USA

The common collared lizard (Crotaphytus collaris) exhibits considerable geographical colour variation, particularly among males. Populations of this diurnal saxicolous iguanian inhabit patches of rocky habitat throughout the species’ broad distribution in North America and are anticipated to experience local differences in selective pressures that influence colouration. Specifically, while social interactions might favour conspicuous colouration, crypsis may be advantageous in interactions with visually orienting predator and prey species. To address the local relationship between lizard and substrate colouration we compared the reflectance spectra of two geographically distant and phenotypically divergent populations of collared lizards with the rocky substrates they inhabit. Our northern study population (C. c. auriceps in eastern Utah) occurs on red rocks, where males exhibit boldly coloured turquoise bodies and bright yellow heads. In contrast, our southern study population (C. c. fuscus in southern New Mexico) lives on grey and tan rocks, and males in this location exhibit subdued brown and tan dorsal colours. Spectral comparisons revealed that males in the northern population contrasted strongly with their local rocks, whereas males in the southern population matched their rock colours with reasonably good fidelity. This relationship held under a variety of lighting conditions. Females in both populations were less conspicuously coloured than males, although northern females contrasted more with their rocks than did southern females. In addition, sexual dichromatism was pronounced in the northern population but minimal in the southern population. Finally, sexual size and weight dimorphism was strong in the southern population while being virtually absent in the northern population. A comparison of the local predator and prey assemblages suggests that the conspicuous and sexually dichromatic colouration of the northern population may have evolved in response to reduced pressure from visually orienting predators as well as reduced dependence on saurian prey. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77 , 67–85     

A bee’s eye view of remarkable floral colour patterns in the south-west Australian biodiversity hotspot revealed by false colour photography

Background and AimsColour pattern is a key cue of bee attraction selectively driving the appeal of pollinators. It comprises the main colour of the flower with extra fine patterns, indicating a reward focal point such as nectar, nectaries, pollen, stamens and floral guides. Such advertising of floral traits guides visitation by the insects, ensuring precision in pollen gathering and deposition. The study, focused in the Southwest Australian Floristic Region, aimed to spot bee colour patterns that are usual and unusual, missing, accomplished by mimicry of pollen and anthers, and overlapping between mimic-model species in floral mimicry cases.MethodsFloral colour patterns were examined by false colour photography in 55 flower species of multiple highly diverse natural plant communities in south-west Australia. False colour photography is a method to transform a UV photograph and a colour photograph into a false colour photograph based on the trichromatic vision of bees. This method is particularly effective for rapid screening of large numbers of flowers for the presence of fine-scale bee-sensitive structures and surface roughness that are not detectable using standard spectrophotometry.Key ResultsBee- and bird-pollinated flowers showed the expected but also some remarkable and unusual previously undetected floral colour pattern syndromes. Typical colour patterns include cases of pollen and flower mimicry and UV-absorbing targets. Among the atypical floral colour patterns are unusual white and UV-reflecting flowers of bee-pollinated plants, bicoloured floral guides, consistently occurring in Fabaceae spp., and flowers displaying a selective attractiveness to birds only. In the orchid genera (Diuris and Thelymitra) that employ floral mimicry of model species, we revealed a surprising mimicry phenomenon of anthers mimicked in turn by model species.ConclusionThe study demonstrates the applicability of ‘bee view’ colour imaging for deciphering pollinator cues in a biodiverse flora with potential to be applied to other eco regions. The technique provides an exciting opportunity for indexing floral traits on a biome scale to establish pollination drivers of ecological and evolutionary relevance.     

Testing the role of background matching and self‐shadow concealment in explaining countershading coloration in wild‐caught rainbowfish

Countershading, or dorsal pigmentary darkening (DPD), describes a form of vertically varying coloration, where an animal typically has a dark dorsal surface and a paler ventral side, and is widespread among mammals, birds, reptiles, fishes and insects. DPD is thought to confer concealment from predators and, in terrestrial systems, there is good evidence that the dark–light transition in body coloration acts to conceal the body's shadow. Surprisingly few studies of DPD have been conducted in aquatic environments, and thus it is not known whether the mechanisms of concealment are similar to those that operate in terrestrial habitats. In this study, we determined the role of the light environment and predation risk in determining DPD in wild‐caught populations of a freshwater fish, the western rainbowfish (Melanotaenia australis). We also examined the underlying mechanisms of DPD for concealment by testing the assumptions of background matching and self‐shadow concealment. In a subsequent experiment, we determined whether any observed variation in DPD was maintained when the visual background was manipulated in the laboratory (to induce a change in body coloration). We found that both the amount of downwelling irradiance and the level of predation risk at the collection site affected skin darkness (dorsal, ventral and overall), whereas the ratio of dorsoventral coloration (DPD) was not affected by the parameters considered. The laboratory experiment revealed that fish changed their body coloration to match their visual background, and did so by altering the relative ratio of dorsoventral skin darkness. In contrast with research on terrestrial animals, our findings suggest that the most likely method of achieving crypsis is through background matching, rather than self‐shadow concealment. It is thus possible that differences in the optical characteristics of terrestrial and aquatic environments, and/or variation in the angles at which prey are typically viewed and attacked, have resulted in divergent mechanisms of using DPD to attain crypsis. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 915–928.