Temperature,but Not Available Energy,Affects the Expression of a Sexually Selected Ultraviolet (UV) Colour Trait in Male European Green Lizards

Background

Colour signals are widely used in intraspecific communication and often linked to individual fitness. The development of some pigment-based (e.g. carotenoids) colours is often environment-dependent and costly for the signaller, however, for structural colours (e.g. ultraviolet [UV]) this topic is poorly understood, especially in terrestrial ectothermic vertebrates.

Methodology/Principal Findings

In a factorial experiment, we studied how available energy and time at elevated body temperature affects the annual expression of the nuptial throat colour patch in male European green lizards (Lacerta viridis) after hibernation and before mating season. In this species, there is a female preference for males with high throat UV reflectance, and males with high UV reflectance are more likely to win fights. We found that (i) while food shortage decreased lizards'' body condition, it did not affect colour development, and (ii) the available time for maintaining high body temperature affected the development of UV colour without affecting body condition or other colour traits.

Conclusions/Significance

Our results demonstrate that the expression of a sexually selected structural colour signal depends on the time at elevated body temperature affecting physiological performance but not on available energy gained from food per se in an ectothermic vertebrate. We suggest that the effect of high ambient temperature on UV colour in male L. viridis makes it an honest signal, because success in acquiring thermally favourable territories and/or effective behavioural thermoregulation can both be linked to individual quality.     

Too big for his boots: Are social costs keeping condition‐dependent status signalling honest in an Australian lizard?

Australian painted dragon lizards Ctenophorus pictus occur in three head colours (red, orange and yellow) that differ in their level of aggression (reds being most aggressive), hormone profile (reds having higher testosterone levels) and in their frequency in our study population over time. They are also polymorphic in bib colour; some males have a bright yellow area under the chin, while others lack this coloured area entirely. We show that red males with a bib are in better body condition than red males that lack a bib. This contrasts sharply to yellow males, in which males with a bib are in poorer condition than yellow males that lack a bib. Our analysis also shows that following exposure to a high percentage of red (more aggressive) neighbours, all males suffer a reduction in body condition, and importantly, males with a bib (regardless of their head colour) suffer a more severe loss of body condition than males that lack a bib. Finally, this condition loss is significantly higher for yellow bibbed males than for red bibbed males, suggesting that the cost of sporting a bib may be higher for them. Orange males showed a non‐significant difference in condition between bib morphs. Our analysis also shows that bibbed yellow males (the morph with lower body condition), but no other morph category, declined significantly in their frequency between 2 years.     

Predation and the relative importance of larval colour polymorphisms and colour polyphenism in a damselfly

Intraspecific body colour variation is common in many animal species. Predation could be a key selective agent giving rise to variation in body colour, and such variation could be due to genetics (polymorphisms) or phenotypic plasticity (polyphenisms). In this study we examined the degree of colour polymorphism and polyphenism in background colour matching in larvae of the damselfly Coenagrion armatum. In addition, we tested if predation risk is reduced when larvae are exposed to a matching compared to a non-matching background. By raising families of larvae at three different background colours we showed that polymorphism explained about 20 % of the total variation and polyphenism about 35 %. In a predation experiment with fish, we showed that larvae with a body colour matching the background had a higher survival success compared to larvae with a non-matching background colour. We suggest that the background matching is adaptive in terms of survival from predation and that colour diversity is maintained because of spatial and temporal variation in the background experienced by damselfly larvae under field conditions.     

Spots and stripes: ecology and colour pattern evolution in butterflyfishes

The incredible diversity of colour patterns in coral reef fishes has intrigued biologists for centuries. Yet, despite the many proposed explanations for this diversity in coloration, definitive tests of the role of ecological factors in shaping the evolution of particular colour pattern traits are absent. Patterns such as spots and eyespots (spots surrounded by concentric rings of contrasting colour) have often been assumed to function for predator defence by mimicking predators'' enemies'' eyes, deflecting attacks or intimidating predators, but the evolutionary processes underlying these functions have never been addressed. Striped body patterns have been suggested to serve for both social communication and predator defence, but the impact of ecological constraints remains unclear. We conducted the first comparative analysis of colour pattern diversity in butterflyfishes (Family: Chaetodontidae), fishes with conspicuous spots, eyespots and wide variation in coloration. Using a dated molecular phylogeny of 95 species (approx. 75% of the family), we tested whether spots and eyespots have evolved characteristics that are consistent with their proposed defensive function and whether the presence of spots and body stripes is linked with species'' body length, dietary complexity, habitat diversity or social behaviour. Contrary to our expectations, spots and eyespots appeared relatively recently in butterflyfish evolution and are highly evolutionarily labile, suggesting that they are unlikely to have played an important part in the evolutionary history of the group. Striped body patterns showed correlated evolution with a number of ecological factors including habitat type, sociality and dietary complexity. Our findings question the prevailing view that eyespots are an evolutionary response to predation pressure, providing a valuable counter example to the role of these markings as revealed in other taxa.     

Phenotypic variation and promiscuity in a wild population of pure dingoes (Canis dingo)

Phenotypic diversity occurs in natural populations as a result of the interaction between an individual's genotype and the environment. Nevertheless, individual variation in phenotypic traits such as coat colour and body size is routinely used to differentiate between “pure” dingoes Canis dingo and dingo‐dog hybrids. Extensive anthropogenic impacts and widespread hybridization with domestic dogs has hindered our ability to study intact dingo populations and, therefore, most of our basic understanding of dingo biology (e.g., phenotypic variation, mating systems, genetic diversity) stems from observational studies on perturbed populations. We sampled a relatively undisturbed population of dingoes, from arid Australia, to determine their purity and genetic diversity. We explored their mating strategy using a pedigree built from genetic data and examined how phenotypic variation was influenced by age, sex, heterozygosity, and relatedness. Coat colour was our measure of phenotype and our population displayed four types (sandy, black & tan, white, and sable). All dingoes (n = 83) possessed a high level of dingo ancestry (mean purity > 90%) and were closely related to each other; with all but one individual related as full‐sibling or parent–offspring. Our pedigree shows both monogamous and promiscuous mating strategies exist within an undisturbed population. Variation in coat colour or body size cannot be used to infer a dingo's level of purity because the phenotype of pure dingoes is intrinsically variable. The breeding system of dingoes was long thought to be monogamous, but we provide genetic evidence for numerous mating strategies including both long‐term monogamy and extreme promiscuity.     

Proximate mechanisms of colour variation in the frillneck lizard: geographical differences in pigment contents of an ornament

Animal coloration has evolved in contexts such as communication, camouflage, and thermoregulation. Most studies of animal coloration focus on its adaptive benefits, whereas its underlying mechanisms have received less attention despite their potential influence on adaptive benefits. In fish and reptiles, for example, colour variation from yellow to red can be produced by carotenoid and/or pteridine pigments, which differ dramatically in the way they are obtained (carotenoids through diet and pteridines synthesized de novo). Hence, potential adaptive benefits could differ greatly depending on the relative contribution to coloration of different pigments. In the present study, we investigate the mechanisms underlying colour variation in the frill of the Australian frillneck lizard (Sauropsida: Chlamydosaurus kingii). Frill colour varies between populations across the species' range (red, orange, yellow or white). We argue that this geographical variation results from different concentrations of carotenoids and pteridines in the frill. Frill carotenoid concentrations were lower in eastern populations (yellow and white forms), and pteridines were present only in the red and orange forms, thereby explaining their redder hues. The observed geographical variation in frill carotenoids suggests variation in carotenoid availability across the species' range, which is backed up by the finding that plasma carotenoid concentrations were higher in the red (western) compared to the yellow (eastern) form. Although no correlations were found between individual colour measurements, frill pigments and plasma carotenoids, our results suggest that selective pressures vary across the species' range and we speculate that predation pressures and/or intrasexual signalling context differ between forms.     

Disruptive viability selection on a black plumage trait associated with dominance

Traits used in communication, such as colour signals, are expected to have positive consequences for reproductive success, but their associations with survival are little understood. Previous studies have mainly investigated linear relationships between signals and survival, but both hump‐shaped and U‐shaped relationships can also be predicted, depending on the main costs involved in trait expression. Furthermore, few studies have taken the plasticity of signals into account in viability selection analyses. The relationship between signal expression and survival is of particular interest in melanin‐based traits, because their main costs are still debated. Here, we first determined the main factors explaining variability in a melanin‐based trait linked to dominance: the bib size of a colonial bird, the sociable weaver Philetairus socius. We then used these analyses to obtain a measure representative of the individual mean expression of bib size. Finally, we used capture–recapture models to study how survival varied in relation to bib size. Variation in bib size was strongly affected by year and moderately affected by age, body condition and colony size. In addition, individuals bearing small and large bibs had higher survival than those with intermediate bibs, and this U‐shaped relationship between survival and bib size appeared to be more pronounced in some years than others. These results constitute a rare example of disruptive viability selection, and point towards the potential importance of social costs incurred by the dominance signalling function of badges of status.     

Dressed to impress: breeding plumage as a reliable signal of innate immunity

Animal signals involved in sexual selection are often indicators of individual quality. The assumption that sexual characters such as breeding plumage may indicate immune state has rarely been tested in free‐living migratory birds, particularly in relation to innate immunity. If sexual characters indeed reflect immune condition, then these could be used to evaluate individual quality. Melanin is a common pigment used in animal communication that mitigates the effects of oxidative stress and has positive effects on energy homeostasis, important functions during the strenuous activity of long‐distance flights. However, melanin is also immunosuppressive, and the melanised patches of breeding plumage may to some extent compromise immune responsiveness. We studied melanin‐based secondary sexual characters (SSC) in a long‐distance migratory wader, the black‐tailed godwit Limosa limosa, and found that breeding plumage features of male and female godwits are linked to components of innate immunity. Males with a larger colour extension had higher circulating levels of haptoglobin and hemolysis activity, while they also presented a lower body condition; whereas females presented a negative trend between colour and bar extension and hemolysis activity, and a positive trend for natural antibodies. The association between signal, immune state and physical condition in males suggests a cost for signal production and immune condition during prenuptial migration. Sex differences in how signals relate with immune capacity are a likely consequence of sex‐specific signalling roles and energy demands. Our results indicate that male godwit breeding plumage reflects innate immunity state, and is therefore a likely signal for females to use during mate choice as an honest indicator of male's capacity to allocate energy/resources to both expensive traits during periods of energetic constraint.     

Variability,heritability and condition-dependence of the multidimensional male colour phenotype in a passerine bird

Elaborate ornamental traits are commonly assumed to be honest signals of individual quality, owing to the presumed costs involved in their production and/or maintenance. Such traits are often highly variable, possibly because of condition-dependence and/or high underlying genetic variation, and it has been suggested that their expression should be more sensitive to condition and/or more heritable than non-ornamental traits. Many bird species display colourful plumage with multiple distinct patches of different developmental origins, forming complex colour phenotypes. Despite this complexity, colourful ornaments are often studied in isolation, without comparison to suitable non-ornamental controls. Based on plumage reflectance data collected over 8 years, we assessed the signalling potential of the multidimensional male colour phenotype in a tropical bird: the purple-crowned fairy-wren Malurus coronatus. Specifically, we tested the predictions that the expression of putative ornamental colours (purple and black – the breeding colours – and blue) is (1) more variable, (2) more heritable and (3) more condition-dependent compared to year-round non-ornamental colours (buff-white and brown). Our results show that ornamental colours exhibit greater levels of variability, and some chromatic components of purple and blue colouration appear slightly heritable (h² = 0.19–0.30). However, contrary to predictions of heightened condition-dependence in ornaments, only brightness of the buff-white and brown colouration increased with male body condition, although brightness of the purple colouration was related to male age as expected. Despite partial support for predictions, the lack of consistent patterns illustrates the complexity of visual signals and highlights the need to study colour phenotypes in their entirety.Subject terms: Behavioural ecology, Evolutionary ecology, Ecological genetics, Quantitative trait, Sexual selection     

Spots, stripes, tail tips and dark eyes: Predicting the function of carnivore colour patterns using the comparative method

Animal colour patterns are adaptive for three reasons: camouflage, communication and physico-physiological functions. This study proposes a conceptual framework for predicting the main adaptive function of carnivore colour patterns based on three factors: visibility, shape and location on the body, as well as, their behavioural ecological correlates. Using a comparative phylogenetic approach, the colour patterns present on the body, the tail and the eyes of 200 species of mammalian carnivores were analysed. Their evolutionary history was reconstructed using MacClade and Maddison's concentrated-changes test was used to test the association between species' colour patterns and their behavioural ecology on a composite phylogeny for all the Carnivora. The results for dark spots, vertical stripes, horizontal stripes, ringed tails, black tail tips, white tail tips, dark eye contour and dark eye patches, are presented. The comparative analyses indicate that spotted, vertically striped and horizontally striped coats evolved for camouflage. Tail markings seem to have evolved for intra- and/or inter-specific communication, while dark markings near and around the eyes are associated with variables consistent with a physico-physiological function. These findings suggest that both the physical environment and animal behaviour are important selective factors driving the evolution of animal colour patterns and that both need to be taken into consideration in future studies of animal coloration.     

Carotenoid coloration in great black‐backed gull Larus marinus reflects individual quality

Carotenoids are a large group of biochemicals, with similar properties, synthesised by bacteria, fungi, algae and plants. Vertebrates obtain these biologically active pigments through the diet, and they are a disproportionately common component of animal colour signals and play important roles in immune functions and as antioxidants. Carotenoids are believed to be a limited resource and because of the trade‐off between allocation of carotenoids to signals and to other functions, carotenoid based signals are often thought to be handicap signals. The purpose of this study was to investigate the signalling potential of carotenoid‐based tissue coloration in the great black‐backed gull Larus marinus. The intensity of carotenoid‐based coloration in bill, gape and eye‐ring coloration was investigated in relation to body condition, reproductive parameters, levels of immune activity, and sexual dimorphism. In males there was a positive relationship between colour intensity and body condition, but in females no such relationship was found. However, females with high colour intensity had larger eggs and clutches. Additionally, females with high red scores tended to have high density of circulating lymphocytes. There was no sexual dimorphism in coloration and there was a negative relationship between colour intensity and sampling time, which indicates that this coloration is most intensely expressed early in the breeding season. The results in this study suggest that carotenoid‐based coloration in great black‐backed gull are partly condition dependent and reveal information about individual quality in both males an females. Hence, it might have evolved as an important signal for assessing the quality of potential mates.     

Carotenoid coloration in great black-backed gull Larus marinus reflects individual quality

Carotenoids are a large group of biochemicals, with similar properties, synthesised by bacteria, fungi, algae and plants. Vertebrates obtain these biologically active pigments through the diet, and they are a disproportionately common component of animal colour signals and play important roles in immune functions and as antioxidants. Carotenoids are believed to be a limited resource and because of the trade-off between allocation of carotenoids to signals and to other functions, carotenoid based signals are often thought to be handicap signals. The purpose of this study was to investigate the signalling potential of carotenoid-based tissue coloration in the great black-backed gull Larus marinus . The intensity of carotenoid-based coloration in bill, gape and eye-ring coloration was investigated in relation to body condition, reproductive parameters, levels of immune activity, and sexual dimorphism. In males there was a positive relationship between colour intensity and body condition, but in females no such relationship was found. However, females with high colour intensity had larger eggs and clutches. Additionally, females with high red scores tended to have high density of circulating lymphocytes. There was no sexual dimorphism in coloration and there was a negative relationship between colour intensity and sampling time, which indicates that this coloration is most intensely expressed early in the breeding season. The results in this study suggest that carotenoid-based coloration in great black-backed gull are partly condition dependent and reveal information about individual quality in both males an females. Hence, it might have evolved as an important signal for assessing the quality of potential mates.     

Adaptive body patterning,three‐dimensional skin morphology and camouflage measures of the slender filefish Monacanthus tuckeri on a Caribbean coral reef

The slender filefish is a master of adaptive camouflage and can change its appearance within 1–3 s. Videos and photographs of this animal's cryptic body patterning and behavior were collected in situ under natural light on a Caribbean coral reef. We present an ethogram of body patterning components that includes large‐ and small‐scale spots, stripes and bars that confer a variety of cryptic patterns amidst a range of complex backgrounds. Field images were analyzed to investigate two aspects of camouflage effectiveness: (1) the degree of colour resemblance between animals and their nearby visual stimuli; and (2) the visibility of each fish's actual body outline vs. its illusory outline. Most animals more closely matched the colour of nearby visual stimuli than that of the surrounding background. Three‐dimensional dermal flaps complement the melanophore skin patterns by enhancing the complexity of the fish's physical skin texture to disguise its actual body shape, and the morphology of these structures was studied. The results suggest that the body patterns, skin texture, postures and swimming orientations putatively hinder both the detection and recognition of the fish by potential visual predators. Overall, the rapid speed of change of multiple patterns, colour blending with nearby backgrounds, and the physically complicated edge produced by dermal flaps effectively camouflage this animal among soft corals and macroalgae in the Caribbean Sea.     

Pairing context determines condition-dependence of song rate in a monogamous passerine bird

Condition-dependence of male ornaments is thought to provide honest signals on which females can base their sexual choice for genetic quality. Recent studies show that condition-dependence patterns can vary within populations. Although long-term association is thought to promote honest signalling, no study has explored the influence of pairing context on the condition-dependence of male ornaments. In this study, we assessed the influence of natural variation in body condition on song rate in zebra finches (Taeniopygia guttata) in three different situations: during short and long encounters with an unfamiliar female, and within heterosexual mated pairs. We found consistent individual differences in male directed and undirected song rate. Moreover, body condition had a positive effect on song rate in paired males. However, male song rate was not influenced by body condition during short or long encounters with unfamiliar females. Song rate appears to be an unreliable signal of condition to prospective females as even poor-condition birds can cheat and sing at a high rate. By contrast, paired females can reliably use song rate to assess their mate''s body condition, and possibly the genetic quality. We propose that species'' characteristics, such as mating system, should be systematically taken into account to generate relevant hypotheses about the evolution of condition-dependent male ornaments.     

Body‐colour variation in an orb‐web spider and its effect on predation success

Animal body coloration serves several functions such as thermoregulation, camouflage, aposematism, and intraspecific communication. In some orb‐web spiders, bright and conspicuous body colours are used to attract prey. On the other hand, there are other species whose body colour does not attract prey. Using a spider species showing individual body‐colour variation, the present study aimed to determine whether or not the variation in body colour shows a correlation with predation rates. We studied the orb‐web spider (Cyclosa argenteoalba) using both field observations and T‐maze experiments, in which the prey were exposed to differently coloured spiders. Cyclosa argenteoalba has silver‐ and black‐coloured areas on its dorsal abdomen, with the ratio of these two colours varying continuously among individuals. The bright and conspicuous silver area reflects ultraviolet light. Results of both field observations and colour choice experiments using Drosophila flies as prey showed that darker spiders have a greater chance of capturing prey than silver spiders. This indicates that body‐colour variation affects predation success among individuals and that the bright silver colour does not function to attract prey in C. argenteoalba.     

Condition-dependent variation in the blue-ultraviolet coloration of a structurally based plumage ornament

After years of investigation into the function of sexually dimorphic ornamental traits, researchers are beginning to understand how bright plumage colour in birds acts as an intraspecific signal. This work has focused primarily on pigment-based ornaments because they are highly variable in patch size, hue and brightness for some species. In contrast, structurally based ornaments have been little studied, in part because they do not appear to be as variable as pigment-based ornaments. We investigated a structurally based plumage ornament in a wild population of blue grosbeaks (Guiraca caerulea), a sexually dimorphic passerine. We report plumage variation that extends into the ultraviolet region of the spectrum. The pattern of covariation between four out of five elements of plumage variation suggests that structurally based ornamentation is pushed towards extreme expression of the trait as predicted by the sexual selection theory. The ''bluest'' birds have the highest percentage of blue feathers on the body. These ornamental feathers reflect light maximally at the shortest wavelengths (ultraviolet), with the greatest intensity and the greatest contrast. Age may have some effect on expression of blueness. In addition, plumage variables are correlated with growth bars in tail feathers (a record of nutritional condition during moult in a non-ornamental trait). This suggests that the ornament is partially condition dependent. Thus, blue plumage in male grosbeaks may serve as an honest indicator of age and quality.     

Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird

Categorizing individuals into discrete forms in colour polymorphic species can overlook more subtle patterns in coloration that can be of functional significance. Thus, quantifying inter-individual variation in these species at both within- and between-morph levels is critical to understand the evolution of colour polymorphisms. Here we present analyses of inter-individual colour variation in the Reunion grey white-eye (Zosterops borbonicus), a colour polymorphic wild bird endemic to the island of Reunion in which all highland populations contain two sympatric colour morphs, with birds showing predominantly grey or brown plumage, respectively. We first quantified colour variation across multiple body areas by using a continuous plumage colour score to assess variation in brown-grey coloration as well as smaller scale variation in light patches. To examine the possible causes of among-individual variation, we tested if colour variation in plumage component elements could be explained by genotypes at two markers near a major-effect locus previously related to back coloration in this species, and by other factors such as age, sex and body condition. Overall, grey-brown coloration was largely determined by genetic factors and was best described by three distinct clusters that were associated to genotypic classes (homozygotes and heterozygote), with no effect of age or sex, whereas variation in smaller light patches was primarily related to age and sex. Our results highlight the importance of characterizing subtle plumage variation beyond morph categories that are readily observable since multiple patterns of colour variation may be driven by different mechanisms, have different functions and will likely respond in different ways to selection.     

Sexual dimorphism and intra-populational colour pattern variation in the aposematic frog Dendrobates tinctorius

Despite the predicted purifying role of stabilising selection against variation in warning signals, many aposematic species exhibit high variation in their colour patterns. The maintenance of such variation is not well understood, but it has been suggested to be the result of an interaction between sexual and natural selection. This interaction could also facilitate the evolution of sexual dichromatism. Here we analyse in detail the colour patterns of the poison frog Dendrobates tinctorius and evaluate the possible correlates of the variability in aposematic signals in a natural population. Against the theoretical predictions of aposematism, we found that there is enormous intra-populational variation in colour patterns and that these also differ between the sexes: males have a yellower dorsum and bluer limbs than females. We discuss the possible roles of natural and sexual selection in the maintenance of this sexual dimorphism in coloration and argue that parental care could work synergistically with aposematism to select for yellower males.     

Fractal nature of protein surface roughness: a note on quantification of change of surface roughness in active sites,before and after binding

Year 2010 marked the 25th year since we came to know that roughness of a protein surface has fractal symmetry. Ever since the publication of Lewis and Rees' paper, hundreds of works from a spectrum of perspectives have established that fractal dimension (FD) can be considered as a reliable marker that describes roughness of protein surface objectively. In this article, we introduce readers to the fundamentals of fractals and present categorical biophysical and geometrical reasons as to why FD‐based constructs can describe protein surface roughness more accurately. We then review the commonality (and the lack of it) between numerous approaches that have attempted to investigate protein surface with fractal measures, before exploring the patterns in the results that they have produced. Apart from presenting the genealogy of approaches and results, we present an analysis that quantifies the difference in surface roughness in stretches of protein surface containing the active site, before and after binding to ligands, to underline the utility of FD‐based measures further. It has been found that surface stretches containing the active site, in general, undergo a significant increment in its roughness after binding. After presenting the entire repertoire of FD‐based surface roughness studies, we talk about two yet‐unexplored problems where application of FD‐based techniques can help in deciphering underlying patterns of surface interactions. Finally, we list the limitations of FD‐based constructs and put down several precautions that one must take while working with them. Copyright © 2013 John Wiley & Sons, Ltd.     

Modulatory Communication Signal Performance Is Associated with a Distinct Neurogenomic State in Honey Bees

Studies of animal communication systems have revealed that the perception of a salient signal can cause large-scale changes in brain gene expression, but little is known about how communication affects the neurogenomic state of the sender. We explored this issue by studying honey bees that produce a vibratory modulatory signal. We chose this system because it represents an extreme case of animal communication; some bees perform this behavior intensively, effectively acting as communication specialists. We show large differences in patterns of brain gene expression between individuals producing vibratory signal as compared with carefully matched non-senders. Some of the differentially regulated genes have previously been implicated in the performance of other motor activities, including courtship behavior in Drosophila melanogaster and Parkinson''s Disease in humans. Our results demonstrate for the first time a neurogenomic brain state associated with sending a communication signal and provide suggestive glimpses of molecular roots for motor control.